Emotion and CONSCIOUSNESS

EMOTION AND CONSCIOUSNESS

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Edited by

LISA FELDMAN BARRETT PAULA M. NIEDENTHAL PIOTR WINKIELMAN

 

THE GUILFORD PRESS New York London

© 2005 The Guilford Press
A Division of Guilford Publications, Inc. 72 Spring Street, New York, NY 10012 http://www.guilford.com

All rights reserved

No part of this book may be reproduced, translated, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher.

Printed in the United States of America
This book is printed on acid-free paper. Lastdigitisprintnumber: 9 8 7 6 5 4 3 2 1 Library of Congress Cataloging-in-Publication Data

Emotion and consciousness / edited by Lisa Feldman Barrett, Paula M. Niedenthal & Piotr Winkielman.

p. cm.
Includes bibliographical references and index.
ISBN 1-59385-188-X (cloth)
1. Consciousness. 2. Emotions. 3. Emotions and cognition.

I. Barrett, Lisa Feldman. II. Niedenthal, Paula M. III. Winkielman, Piotr.
BF311.E4855 2005
152.4—dc22

2005001276

About the Editors

About the Editors

Lisa Feldman Barrett, PhD, completed her doctoral training at the Univer- sity of Waterloo, Canada, and is now a professor of psychology at Boston College. Her major research focus addresses questions about the experience of emotion from social-psychological, psychophysiological, cognitive science, and neuroscience perspectives. Dr. Barrett’s research has been funded by the National Science Foundation, and she currently holds an Independent Research Scientist Award from the National Institute of Mental Health. She is currently a fellow of the American Psychological Society and a consulting editor for Emotion, the Journal of Personality and Social Psychology, Personality and Social Psychology Bulletin, and Personality and Social Psychology Review, and edited, with Peter Salovey, The Wisdom in Feeling: Psychological Processes in Emotional Intelligence (2002, Guilford Press).

Paula M. Niedenthal, PhD, received her doctorate in social psychology from the University of Michigan and was an assistant professor at Johns Hopkins University until she moved to Indiana University in 1993. She was promoted to full professor there in 1998 but, while on sabbatical in Aix-en-Provence, decided to relocate to France. Dr. Niedenthal is now Director of Research in the National Centre for Scientific Research (CNRS) and is a member of the Laboratory in Social and Cognitive Psychology at Blaise Pascal University, Clermont-Ferrand, France. Author of more than 65 academic articles and chapters and several books, she has recently been associate editor of the journals Cognition and Emotion and Personality and Social Psychology Bulletin. Dr. Niedenthal is a fellow of the Society for Personality and Social Psychology and is currently at work on a textbook on the study of emotion

in social psychology with colleagues Silvia Krauth-Gruber and François Ric, both at René Descartes University, Paris.

v

vi About the Editors

Piotr Winkielman, PhD, completed his doctorate at the University of Michigan and received postdoctoral training in social neuroscience at The Ohio State University, after attending the University of Warsaw in Poland and the University of Bielefeld in Germany for his undergraduate studies. He is now an associate professor of psychology at the University of California–San Diego. Dr. Winkielman’s current research focuses on the relation between emotion, cognition, body, and consciousness using psychological and psychophysiological approaches. His research has been supported by the National Science Foundation and National Alliance for Autism Research and he has served on the editorial boards of the Journal of Personality and Social Psychology and Personality and Social Psychology Bulletin.

Contributors

Contributors

Ralph Adolphs, PhD, Department of Neurology, Division of Cognitive Neuroscience and Behavioral Neurology, University of Iowa College of Medicine, Iowa City, Iowa, and Department of Psychology and Neurosci- ence,California Institute of Technology, Pasadena, California

Anthony P. Atkinson, PhD, Department of Psychology, University of Durham Science Site, Durham, United Kingdom

Jo-Anne Bachorowski, PhD, Department of Psychology, Vanderbilt University, Nashville, Tennessee

Lisa Feldman Barrett, PhD, Department of Psychology, Boston College, Chestnut Hill, Massachusetts

Lawrence W. Barsalou, PhD, Department of Psychology, Emory University, Atlanta, Georgia

Kent C. Berridge, PhD, Department of Psychology, University of Michigan, Ann Arbor, Michigan

Mark E. Bouton, PhD, Department of Psychology, University of Vermont, Burlington, Vermont

Todd S. Braver, PhD, Department of Psychology, Washington University, St. Louis, Missouri

David B. Centerbar, PhD, Department of Psychology, University of Virginia, Charlottesville, Virginia

Louis C. Charland, PhD, Department of Philosophy, Department of Psychiatry, and Faculty of Health Sciences, University of Western Ontario, London, Ontario, Canada

vii

viii Contributors

Gerald L. Clore, PhD, Department of Psychology, University of Virginia, Charlottesville, Virginia

Beatrice de Gelder, PhD, Faculty of Social and Behavioral Sciences, Tilburg University, Tilburg, The Netherlands

Jeremy R. Gray, PhD, Department of Psychology, Yale University, New Haven, Connecticut

Silvia Krauth-Gruber, PhD, Social Psychology Laboratory, René Descartes University, Paris, France

Daniel Lundqvist, PhD, Psychology Section, Department of Clinical Neuroscience, Karolinska Institute, Stockholm, Sweden

Steven B. Most, PhD, Department of Psychology, Yale University, New Haven, Connecticut

Roland Neumann, PhD, Department of Psychology, Würzburg University, Würzburg, Germany

Paula M. Niedenthal, PhD, Laboratory of Social and Cognitive Psychology, Blaise Pascal University, Clermont-Ferrand, France

Arne Öhman, PhD, Psychology Section, Department of Clinical Neuroscience, Karolinska Institute, Stockholm, Sweden

Michael J. Owren, PhD, Department of Psychology, Cornell University, Ithaca, New York

Elizabeth A. Phelps, PhD, Department of Psychology, New York University, New York, New York

Jesse J. Prinz, PhD, Department of Philosophy, University of North Carolina, Chapel Hill, North Carolina

Drew Rendall, PhD, Department of Psychology and Neuroscience, University of Lethbridge, Lethbridge, Alberta, Canada

François Ric, PhD, Social Psychology Laboratory, René Descartes University, Paris, France

Michael D. Robinson, PhD, Department of Psychology, North Dakota State University, Fargo, North Dakota

Alexandre Schaefer, PhD, Department of Psychology, Yale University, New Haven, Connecticut

Klaus R. Scherer, PhD, Department of Psychology, University of Geneva, Geneva, Switzerland

Contributors ix

Eliot R. Smith, PhD, Department of Psychology, Indiana University, Bloomington, Indiana

Justin Storbeck, MA, Department of Psychology, University of Virginia, Charlottesville, Virginia

Julia L. Wilbarger, PhD, Department of Psychology, University of Wisconsin–Madison, Madison, Wisconsin

Piotr Winkielman, PhD, Department of Psychology, University of California–San Diego, San Diego, California

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Contents

CHAPTER 1.

CHAPTER 2.

CHAPTER 3.

CHAPTER 4.

Contents

Introduction 1

LISA FELDMAN BARRETT, PAULA M. NIEDENTHAL, and PIOTR WINKIELMAN

PART I. COGNITION AND EMOTION

Embodiment in the Acquisition and Use 21 of Emotion Knowledge
PAULA M. NIEDENTHAL, LAWRENCE W. BARSALOU,
FRANÇOIS RIC, and SILVIA KRAUTH-GRUBER

The Interaction of Emotion and Cognition: 51 Insights from Studies of the Human Amygdala
ELIZABETH A. PHELPS

Affect and the Resolution of Cognitive Control Dilemmas 67

JEREMY R. GRAY, ALEXANDRE SCHAEFER, TODD S. BRAVER, and STEVEN B. MOST

CHAPTER 5.

CHAPTER 6.

CHAPTER 7.

Caught by the Evil Eye: Nonconscious Information 97 Processing, Emotion, and Attention to Facial Stimuli
DANIEL LUNDQVIST and ARNE ÖHMAN

Nonconscious Emotions: New Findings and Perspectives 123 on Nonconscious Facial Expression Recognition and Its
Voice and Whole-Body Contexts
BEATRICE DE GELDER

Visual Emotion Perception: Mechanisms and Processes 150

ANTHONY P. ATKINSON and RALPH ADOLPHS xi

PART II. UNCONSCIOUS EMOTIONAL PROCESSING

xii

Contents

CHAPTER 8.

CHAPTER 9.

CHAPTER 10.

CHAPTER 11.

CHAPTER 12.

CHAPTER 13.

CHAPTER 14.

CHAPTER 15.

CHAPTER 16.

PART III. UNCONSCIOUS EMOTIONAL BEHAVIOR

Conscious and Unconscious Emotion in Nonlinguistic 185 Vocal Communication
MICHAEL J. OWREN, DREW RENDALL,
and JO-ANNE BACHOROWSKI

Behavior Systems and the Contextual Control of Anxiety, 205 Fear, and Panic
MARK E. BOUTON

PART IV. THE EXPERIENCE OF EMOTION

Emotion Experience and the Indeterminacy of Valence 231

LOUIS C. CHARLAND

Feeling Is Perceiving: Core Affect and Conceptualization 255 in the Experience of Emotion
LISA FELDMAN BARRETT

PART V. PERSPECTIVES ON
THE CONSCIOUS–UNCONSCIOUS DEBATE

Emotion Processes Considered from the Perspective 287 of Dual-Process Models
ELIOT R. SMITH and ROLAND NEUMANN

Unconscious Processes in Emotion: The Bulk of the Iceberg 312

KLAUS R. SCHERER

Emotion, Behavior, and Conscious Experience: 335 Once More without Feeling
PIOTR WINKIELMAN, KENT C. BERRIDGE,
and JULIA L. WILBARGER

Emotions, Embodiment, and Awareness 363

JESSE J. PRINZ

Seven Sins in the Study of Unconscious Affect 384

GERALD L. CLORE, JUSTIN STORBECK, MICHAEL D. ROBINSON, and DAVID B. CENTERBAR

Index 409

Introduction

CHAPTER 1 Introduction

LISA FELDMAN BARRETT PAULA M. NIEDENTHAL PIOTR WINKIELMAN

The idea that emotion reflects a combination of conscious and unconscious processes dates back to the beginning of Western philosophy, when Plato and Aristotle noticed that some emotions, such as anger, can arise via care- ful deliberation (e.g., about injustice), via an impulsive reaction (e.g., to pain), or via a combination of both. Scientific interest in the role of con- sciousness in emotion was perhaps first stimulated by William James, who asserted that emotion is a conscious perception of bodily changes, which themselves can have unconscious origins. This interest in the interplay between conscious and unconscious contributions to emotional responding has reemerged in recent years, as scientists have placed the study of emo- tion at the center of scientific inquiry about the human condition, and as the study of consciousness has, again, become scientifically respectable. Fields with broadly differing epistemological frameworks (e.g., cultural anthropology, philosophy, psychology, cognitive science, and various forms of neuroscience) all study something called “emotion.” And, as emotion research in these fields progresses at many levels of analysis, questions about the relationship between emotion and consciousness remain at the center of the investigations (even if only to highlight that consciousness is not the defining feature of an emotional state). Questions about the inter- play of emotion and consciousness have expanded from examining the place of conscious feelings in emotional responding to include related

1

2 Introduction

issues, such as (1) how unconscious analysis of the incoming stimulus might produce emotional responses, (2) how conscious processes regulate emo- tional responding (and vice versa), (3) the role of consciousness in the inte- gration of emotion and cognition, (4) the role of bodily responses in con- scious and unconscious aspects of emotion, (5) how unconscious processes produce a conscious feeling of emotion, and so on.

Unfortunately, it is commonplace for researchers who work on these diverse questions to proceed independently of one another, and to focus on one question in the absence of addressing the others. Often, theoretical models of this and that phenomenon do not have sufficient contact with one another to allow for development of large-scale theory building about emo- tion. Further, the existing models often fail to keep pace with the flood of experimental findings that have been generated. In addition to these prob- lems of communication, progress in understanding the nature of emotion is hampered by disagreements about how the two critical terms, emotion and consciousness, should be defined. It often seems as if researchers who approach the study of emotion from different perspectives and who define these terms differently, inhabit different planets that orbit one another but rarely, if ever, make contact.

The present volume came about as an attempt to address these issues and bring needed coherence to the scientific study of emotion and con- sciousness. This interdisciplinary book brings together researchers who are working on different components of emotion processing and presents the major themes guiding their research. These major themes are represented by the five sections into which the volume is organized. Parts I through IV—Cognition and Emotion, Unconscious Emotional Processing: Percep- tion of Visual Stimuli, Unconscious Emotional Behavior, and The Experi- ence of Emotion—offer an up-to-date review of research relevant to different conscious and unconscious components of emotion. Part IV, Per- spectives on the Conscious–Unconscious Debate, specifically discusses which emotion processes are conscious and unconscious and provides vari- ous perspectives on how these processes configure to produce an “emotion episode.” To bring further coherence and clarity to the volume, the authors were asked to answer the following three questions either within the text of their chapter or in the boxes within the chapters. The first question addressed the definition of emotion (“What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happiness?”). The second question addressed how the concept of consciousness is understood (“Define your terms: conscious, unconscious, awareness. Or say why you do not use the terms.”). The third question asked authors to consider how conscious and unconscious emotion-related processes are configured in their chapter

Introduction 3

(“Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address the issue of consciousness specifi- cally, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?”).

The three overarching questions and the major themes of the volume emerged at the end of a 3-day conference held in the Auvergne region of France in September 2003, at which all authors presented the substance of their chapters. The most remarkable aspect of the conference was discover- ing the similarity in concerns across theorists. Rather than a set of unre- lated talks by neuroscientists, social psychologists, animal behaviorists, cog- nitive psychologists, and philosophers, the talks revealed enormous areas of commonality among the contributors. In fact, the conference confirmed our belief that the field is “ready” for a systematic attempt to integrate the vari- ous themes of research on conscious and unconscious processes in emotion. In what follows, we give a short preview of the major themes of the five sections and the sixteen chapters. As we preview the chapters, we hope that the reader will notice the coherence of the message that emerges from the book, despite the diversity of topics and the authors’ differing disciplin- ary orientations.

THE CHAPTERS

Cognition and Emotion

Part I of the volume deals with the interaction between processes that have been conventionally called emotion and cognition. Together, these three chapters begin to characterize the possible relationships between thinking and feeling and, in so doing, sketch a broad framework for understanding the emergence and interplay of conscious and unconscious processes in emotional responding. Clarifying this relationship sets the stage for chap- ters that directly address how conscious and unconscious processes might interact to produce an experience that can be reported.

In Chapter 2, Paul N. Niedenthal, Lawrence W. Barsalou, François Ric, and Sylvia Krauth-Gruber introduce an idea that appears in several chapters (e.g., Anthony P. Atkinson & Ralph Adolphs, Chapter 7; Daniel Lundqvist & Arne Öhman, Chapter 5; Beatrice de Gelder, Chapter 6; Lisa Feldman Barrett, Chapter 11; Jesse J. Prinz, Chapter 15)—that (1) perceiving someone else’s emotion, (2) having an emotional response or a subjective feeling state, and (3) using emotion knowledge in conceptual tasks, all draw on fundamen- tally the same process that relies on somatosensory and motor representa- tions (or embodiments). Niedenthal and colleagues review considerable evi-

4 Introduction

dence in support of the notion that emotional processing is embodied. First, they review research showing that individuals embody the emotional ges- tures of other people, including facial expressions, posture, and vocal affect. They then build on these findings to argue that imitative behavior produces a corresponding state in the perceiver, leading to the general suggestion that embodied knowledge produces felt emotional states. They summarize evi- dence in support of the idea that both facial and postural poses facilitate the experience of emotions. The reverse is also true. Having participants imag- ine emotionally evocative situations to induce an emotional state produces changes in the body, although those changes are often nonspecifically associ- ated with pleasant and unpleasant affect rather than distinct profiles of dis- crete emotions of anger, sadness, fear, and so on. Finally, Niedenthal et al. discuss how physical actions (e.g., arm flexion or extension, posing facial mus- cles) influence how well participants identify positive and negative informa- tion, how they evaluate stimuli (whether they like an ideograph or find a car- toon funny), and how well they remember details from an evocative story. Taken together, these behavioral results validate the plausibility of an em- bodiment view of emotional processing.

In the next section of their chapter, Niedenthal and colleagues explain how embodied representations can constitute the core conceptual content of emotion knowledge. The general point is that the body provides a funda- mental way of representing knowledge about emotion. Such a view of emo- tional processing, they contend, allows theorists to identify more precisely which processes are, or can be, unconscious and which are conscious. In particular, Niedenthal et al. return to William James’s notion that parts of embodied emotion are unconscious, or can be so, until attention is directed to them. Subjective feelings of emotion, such as the perception of bodily changes, are always conscious. In this, Niedenthal et al. agree with other contributors (e.g., Barrett, Chapter 11) that individual and cultural differ- ences in emotion can best be conceptualized in terms of the representa- tions that guide the direction and interpretation of the content of conscious perception.

In Chapter 3, Elizabeth A. Phelps begins with the observation that the neural systems believed to underlie “emotional” processes overlap exten- sively with those that are involved in “cognition,” leading to questions of whether or not these are really separate processing domains. Phelps echoes a point advanced several years ago by Lane, Nadel, Allen, and Kaszniak (2000), which is consistent with other contributors to this volume, all of whom suggest that the neural architecture involved with emotional pro- cessing overlaps significantly with that which is related to cognitive pro- cessing (Atkinson & Adolphs, Chapter 7; Jeremy R. Gray, Alexandre Schaefer, Todd S. Braver, & Steven B. Most, Chapter 4; Phelps, Chapter 3;

Introduction 5

Piotr Winkielman, Kent C. Berridge, & Julia L. Wilbarger, Chapter 14). Specifically, Phelps’s chapter focuses on the functions of the human amyg- dala, a small structure in the medial temporal lobe that is the centerpiece of many emotion models and that figures prominently in many of the chapters in this volume. Phelps advances the popular view that the amygdala is a brain region whose primary function is linked to emotion. She discusses how the amygdala is intimately involved in directing behavioral responses to the emotional significance of a stimulus in a way that is unconscious, unintentional, and may be independent from the process that generates conscious experience of emotion. Her review of her recent research on instructed fear (i.e., the valenced consequences of a stimulus are conveyed through language rather than direct experience) indicates that the amyg- dala also plays a role in the expression of fears that are learned symbolically (via involvement of the hippocampus) and that depend on awareness and interpretation in a way that is reminiscent of the rule-based processing dis- cussed by Eliot R. Smith and Roland Neumann (Chapter 12). Finally, Phelps discusses how the amygdala influences attention and perception (a point underscored in several other chapters as well) and modulates long- term memory by modulating the storage of hippocampal-dependent mem- ories. As a result of these modulatory mechanisms, individuals are more likely to become aware of emotional events as they occur.

In Chapter 3, Gray, Schaefer, Braver, and Most discuss how affect functions to resolve “control dilemmas”—that is, situations in which the organism is prepared to do more than one thing. First, they propose how affect can resolve control dilemmas that may be conscious; for example, approach–avoidance conflicts. Although a person may be strongly moti- vated to both approach and withdraw from something, presumably because multiple processing systems for positive and negative affect exist within the brain (Cacioppo, Gardner, & Bernston, 1999), it is impossible to do so simultaneously. Gray and colleagues also review recent findings from their laboratory that suggest that approach-related affective states (e.g., amuse- ment) enhance verbal working memory, whereas withdrawal-related states (e.g., anxiety) enhance spatial working memory. These findings are broadly consistent with the idea that threat can enhance visual processing, presum- ably because it is important to know where a threat is located.

Second, Gray and colleagues discuss how affect can resolve uncon- scious control dilemmas, such as those that involve selective attention. For example, individuals demonstrate the phenomenon of attentional capture when threatening information preferentially draws their attention. Current affective states, mood, or chronic affective styles might help to resolve such instances, freeing individuals from the constraints of the immediate fea- tures of the external environment. The general idea that runs throughout

6 Introduction

this chapter, then, is that affect impacts thought and behavior by “tuning” the more cognitive parts of the system to prioritize some functions over others, perhaps when other forms of conflict management, such as conten- tion scheduling, fail to work. Gray et al. suggest (as do others in this vol- ume, e.g., Louis C. Charland, Chapter 10; Barrett, Chapter 11) that affect is a type of valuation function that allows the individual to regulate the influ- ence of internal and external constraints (i.e., the demands of the situation as well as the subjective importance of the event).

Unconscious Emotional Processing: Perception of Visual Stimuli

Part II of the volume describes the mechanisms implicated in the act of perceiving an emotional episode in another person. The chapters in this section (Lundqvist & Öhman, Chapter 5; de Gelder, Chapter 6; and Atkinson & Adolphs, Chapter 7) emphasize the early perceptual contribu- tions to emotional responding (in contrast to the relatively later, more con- ceptual processing that involves knowledge and memory; e.g., Niedenthal et al., Chapter 2) and fill in some of the detail that other chapters draw on when discussing the interplay of the two (e.g., Phelps, Chapter 3; Smith & Neumann, Chapter 12; and Klaus R. Scherer, Chapter 13).

The three chapters included in this section have several points in com- mon. Most importantly, all discuss the time-line for assessing the evaluative significance of a visual stimulus (primarily the processing of static faces, because that is the focus of most research). These chapters address the early processes that allow a person (1) to code the evaluative significance of visual stimuli, or (2) to detect fear, depending on the underlying assump- tions. The early or “low” pathway (involving the superior colliculus and pulvinar nucleus of the thalamus) unconsciously conveys low-frequency information to the amygdala for the initial coding of evaluative significance. This mechanism mediates affective reactions to a stimulus even before it is registered in consciousness, and allows people with blindsight to code the affective significance of things they cannot consciously see. De Gelder, in particular, reviews the literature that investigates the existence of such a pathway, and whether there are additional sensory contributions to blind- sight, such as subjective feelings. This pathway is activated within the first 100 milliseconds of evaluative processing. By approximately 300 millisec- onds, higher-frequency visual information is conveyed via a later or “high” pathway that provides object-identification information to the visual cortex. This information combines with feedback from the amygdala to the visual cortex, which modulates sensory processing by directing attention to those aspects of the environment that are most salient to the organism for dealing with threatening information. It is via these connections that the amygdala

Introduction 7

evaluates facets of the affective significance of complex objects (such as faces).

De Gelder and Atkinson and Adolphs (Chapters 6 and 7) are similar in other respects as well. Both discuss whether the scientific findings on emo- tion perception of static faces generalizes to understanding dynamic facial and body movements. In daily life, information from the face is processed in the context of information coming from other modalities, such as body movements, voice, and so on. Although scientific investigations tend to focus on how organisms process information from one sensory system at a time (usually the visual system in humans, the auditory system in rats), information processing in everyday life is typically multimodal. Thus this is an important emerging area of research in understanding emotion percep- tion. Both chapters also discuss how perception might interact with the subjective experience of emotion or feelings. De Gelder suggests that feel- ings help guide people with blindsight. Atkinson and Adolphs point out overlap in neural areas involved in emotion perception and those corre- lated with the subjective experience of emotion, suggesting that the two processes may inform one another. This emphasis on embodiment in per- ception and experience of emotion is a unifying theme in many of the chap- ters.

Lundqvist and Öhman (Chapter 5) begin their chapter by identifying an assumption that is largely agreed upon by emotion researchers (although there are alternative points of view, e.g., Michael J. Owren, Drew Rendall, and Jo-Anne Backorowski, Chapter 8; Barrett, Chapter 11). These authors argue that humans emit stereotypic behaviors that encode and signal the presence of specific emotions, and that this ability evolved in concert with efficient routines for automatically decoding facial signals. Evolution has equipped humans with an expressive face to send emotional signals, as well as a highly efficient system for decoding these signals and therefore recog- nizing threatening versus friendly faces. Lundqvist and Öhman review research in which faces depicting emotional configurations, presented under conditions that prevent their representation in conscious awareness, evoke psychophysical and neural responses that reflect nonspecific emo- tional (some might say affective) activation. The emotional expression on a face (threatening or friendly) regulates subsequent visual processing in a preattentive way. As a result, threatening faces (when compared to friendly faces) stand out more from the background and are easier to detect. More- over, Lundqvist and Öhman outline how specific features of the face preattentively direct subsequent processing. In particular, eyebrows are important for conveying affective importance (followed by mouth and eyes). They go on to provide a model for facial signal decoding that inte- grates LeDoux’s (1996) research on the subcortical route for evaluation of

8 Introduction

incoming sensory information with Haxby, Hoffman, and Gobbini’s (2000) model of face processing. Early sensory processing extracts information about the threat or safety value of facial signal in a preattentive way, and then directs the way that facial information is subsequently processed in the inferior occipital gyrus and superior temporal sulcus.

Unconscious Emotional Behavior

Part III of the volume deals more directly with emotion-related behaviors. Both chapters (Owren, Rendall, & Bachorowski, Chapter 8, and Mark E. Bouton, Chapter 9) discuss emotional behaviors in a way that is consistent with the basic assumption of appraisal theories of emotion: Stimuli do not have intrinsic value; rather, the meaning of a stimulus is determined by a particular organism in a particular context at a particular point in time. Both highlight the importance of context in determining the value of a stimulus, and in doing so, are consistent with other contributions to this volume (e.g., Barrett, Chapter 11). Both chapters have the potential to change how scientists define meaning, by suggesting that what a stimulus means depends on the organism’s affective response to it. Furthermore, both suggest that affective meaning is, for most part, unconscious (although conscious feelings that derive from the initial assessment of affective mean- ing can play a role in meaning making, e.g., Gerald L. Clore, Justin Storbeck, Michael D. Robinson, & David B. Centerbar, Chapter 16).

In Chapter 8, Owren, Rendell, and Bachorowski introduce a some- what different set of assumptions about unconscious emotion processing than those discussed in the chapters on emotion perception. Rather than assuming that a person emits behavior that encodes his or her emotional state, such that his or her emotions can be decoded and recognized by another person, or that threat information can be extracted from behavioral signals, Owren and colleagues suggest that the meaning of any signal (e.g., a sound or visual image) is determined by the affective change it induces in the perceiver. In particular, Owren and colleagues propose that affect induction may play a key role in the communicative value of mammalian vocalizations. Instead of viewing mammalian vocalizations as a sort of sym- bol-like language (where one call means there is a predator, another call means that there is food, and so on), Owren and colleagues argue that sounds act on the nervous system, either directly because of their intrinsic acoustic properties, or indirectly because people have learned that certain sounds (e.g., the distinctive features of a person’s voice) consistently predict threat or reward. Repeated pairings of individually distinctive sounds with positive or negative outcomes give the sounds themselves come to have predictive value for subsequent affective outcomes.

Introduction 9

In these ways, mammals can influence the affective states and behav- iors of others by the sounds that they make, and they do so in a way that can be disconnected from their own internal state. For example, a parent can speak to a child in a soothing tone (despite his or her own fatigue or frustra- tion) and hug or help the child in repeated occasions, such that the parent’s voice comes to have affective meaning for the child. Another example: A presidential candidate can discuss policies that will have negative conse- quences for you and your family; in a short time, the very sound of his or her voice becomes aversive. As these two examples illustrate, the vocal- izer’s signals may have affective consequences that are consciously and deliberately chosen, or that can be unintended. Either way, however, the affective consequences of the signal for the listener are often unconscious and automatic in that the listener has no initial control over the effects of the incoming signal. Owren and colleagues build on this argument to sug- gest that affect induction is one way that affective communication takes place: through a completely implicit mechanism on both sides of the com- munication.

Although a vocalization need not always reflect the internal state of the sender, at times it certainly can reflect that state, resulting in a completely unconscious form of affective communication. If a sender’s affective state leads to a particular kind of expressive behavior (e.g., to yell at a child), this behavior can have a negative affective impact on the receiver (based on the acoustic properties of the sound, or because the receiver has learned that punishment will follow). This transaction, then, constitutes a completely unconscious process in which the affective state of one person is communi- cated to and impacts the affective state of another. Such a process also sug- gests a plausible mechanism for understanding how affective states can be shared. In clinical psychology, there is a saying that people often end up making others feel the way they do. Perhaps this is one mechanism (even the main mechanism) by which this contagion takes place.

In Chapter 9, Bouton directly addresses issues of classical condition- ing and emotional response. In doing so, he provides an important ground- ing for other chapters in this volume (such as Owren et al., Chapter 8) that appeal to some form of classical conditioning in explaining how a stimulus comes to evoke a response. Bouton reviews important findings from his research in animal learning and discusses how they may be instructive for emotion theory. He discusses how emotion-related behaviors deal with a given evocative unconditioned stimulus, and reviews literature to demon- strate that the constellation of behavior elicited depends on contextual fac- tors. Context can be defined in several ways: (1) as distance from a motiva- tional object (a predator or food), (2) as the interoceptive state at the time of learning, and (3) in terms of time (e.g., the duration of the conditioned stim-

10 Introduction

ulus, or, said another way, the time between the appearance of the condi- tioned stimulus and the appearance of the unconditioned stimulus, which, in turn, evokes the emotional response).

Bouton further discusses how specific types of context influence an emotional response to the conditioned stimulus. First, he presents evidence that one form of emotional responding—anxiety—results from the direct association between the context (i.e., conditioned stimuli [CS] of long dura- tion) and the unconditioned stimulus (US). In doing so, he links anxiety to the phenomenon of reinstatement (in which an extinguished response returns if the animal is merely reexposed to the US alone) and suggests that anxiety (i.e., responses to CS of long duration) is mediated by the bed nucleus of the stria terminalis (BNST, part of the extended amygdala) and the hippocampus. In fact, reinstatement effects may be a form of back- ground contextual conditioning that is mediated by the hippocampus (Phil- lips & LeDoux, 1994).

Second, Bouton suggests that another form of emotional responding— panic—results from an association between the context and retrieval of par- ticular CS–US pairings. Here, context works as cue to retrieve current meaning of a CS after it has been conditioned in one context and extin- guished in another. The context controls whether the organism responds negatively to the CS (because the CS–US association is retrieved from memory) or not (because the CS–no US association is retrieved). Said another way, context can directly determine which meaning of the CS is retrieved after extinction. In doing so, Bouton links panic to the phenome- non of renewal (in which a change of context after extinction can cause a robust return of conditioned responding) and suggests that this form of responding is amygdala mediated, although it is possible that areas of the medial prefrontal cortex might be involved (Milad & Quirk, 2002; Morgan, Romanski, & LeDoux, 1993).

The Experience of Emotion

The next two chapters deal with how conscious and unconscious processes contribute to the experience of emotion. For the average person, emotional feelings are the most salient and defining feature of “having” an emotion. Although there is more to emotion than just the subjective component, the experience of emotion is a psychological phenomenon that is worthy of sci- entific investigation in its own right.

In Chapter 10, Charland presents readers with a provocative look at the nature of valenced feelings. He marshals an argument, primarily on philosophical grounds, that pleasant and unpleasant (hedonic) feelings are

Introduction 11

not an intrinsic property or quality of raw (first-order) emotion experience (as claimed by Barrett, Chapter 11; Cacioppo et al., 1999; Russell, 2003), but are rather created by evaluating and interpreting the emotion experi- ence when that experience is represented in second-order awareness. In other words, valence is not a property of feeling but an interpretation of a feeling as good or bad. Charland argues that valence is laden with personal meaning and is inseparably tied to an experience of the personal signifi- cance of what emotion experience means for us at a particular point in time. In Charland’s view, valence is an appraisal of first-order, raw feelings (which he defines according to Lambie & Marcel, 2002). Valence does not exist prior to reporting on feeling—it is a property of self-report. In this way, valence, as a property of second-order experience, is probably a func- tion of attention. Charland’s view provides a counterpoint that should cause emotion researchers to pause before too quickly accepting the now popular view that stimuli are evaluated for their ability to predict threat or safety, thereby inducing an affective response by a preattentive, automatic, or implicit means of processing (Lundqvist & Öhman, Chapter 5; de Gelder, Chapter 6; Atkinson & Adolphs, Chapter 7; Barrett, Chapter 11; Winkielman, Berridge, & Wilbarger, Chapter 14). His view also challenges the idea that the meaning of a stimulus is defined by the affective reaction that it induces (Owren, Rendell, & Bachorowski, Chapter 8). Furthermore, Charland highlights the important observation that raw feelings (whatever their content, be it pleasure–displeasure, arousal–activation, anger, sad- ness, fear, etc.) can be judged on moral grounds, on how expected or un- expected they were, on how socially appropriate they are, and so on. Therefore, it is important to distinguish the contents of initial raw feel- ings from subsequent judgments of their desirability (e.g., Barrett, 1996), even if those judgments then go on to influence raw feelings in a recursive way.

In Chapter 11, Barrett begins with a critical examination of a guiding assumption within many scientific models of emotion (and one that appears in several chapters in this volume): People experience emotion because people have “emotions”—internal mechanisms that, once triggered, cause observable changes in behavior and feeling. She questions the view that the experience of emotion issues from separate mechanisms for anger, sadness, fear, and so on, and outlines an alternative hypothesis. Specifically, she sug- gests that the basic building blocks for emotional life are affective (i.e., involve core positive and negative affect) and conceptual (i.e., involve pro- cesses of categorization and interpretation). Barrett builds upon Russell’s (2003; Russell & Barrett, 1999) idea of core affect by suggesting that evaluative processing produces an ongoing stream of neurophysiologi-

12 Introduction

cal change (i.e., change in a person’s homeostatic state) that can evoke evolutionarily tuned behaviors for dealing with stimuli of significant value. These changes are then available for representation (although not neces- sarily) in awareness as feelings of pleasure–displeasure and activation– deactivation. She also argues that the experience of emotion is psychologi- cally constructed via the same processes that influence the experience of color and people’s experience of each other. Conceptual knowledge about emotion (i.e., emotion categories that are acquired in childhood and vary across cultures) shapes the perception of core affect into an experience of emotion in much the same way that category knowledge about people shapes our perceptions of other people’s behavioral actions into meaningful acts. Simply put, then, people experience an emotion when they categorize an instance of affective feeling.

With this framework, Barrett suggests that the content and structure of category knowledge about emotion determine the content of what people feel. She argues that conceptualizing involves sensory–motor representa- tions (drawing on Barsalou’s situated conceptualization view, as discussed in Niedenthal et al., Chapter 2), such that conceptual knowledge about emotion can seamlessly shape the perception of core affect into the experi- ence of an emotion. In her view, the experience of emotion is a perceptual act, guided by embodied conceptual knowledge about emotion. The result is a model of emotion experience that has much in common with the social- psychological literature on person perception and with literature on em- bodied conceptual knowledge as it has recently been applied to social psy- chology (e.g., Niedenthal et al., Chapter 2). What differentiates her model from these existing models of emotion experience is the emphasis on cate- gorization processes as constituting a core mechanism driving the differen- tiation of emotion experience. Like other contributors to this volume, Barrett situates her theory in William James’s original ideas about the embodiment of experienced emotion.

Perspectives on the Conscious–Unconscious Debate

The final section of this volume is devoted to examining various issues that relate to conscious and unconscious emotion. First, each chapter discusses the ways in which conscious and unconscious processes configure to pro- duce an emotional response (however it is defined). Second, each critically examines the idea that feelings are presumed to have a causal status with regard to emotion, questioning whether feelings really are the main media- tors between emotion and behavior. Finally, several of the chapters ask the provocative question about whether it is meaningful to talk about “uncon- scious” emotion.

Introduction 13

Smith and Neumann (Chapter 12) frame many existing models of emo- tion in a general dual-process framework. First, they discuss an associative system that records information slowly and builds up representations based on a large sample of experiences, and that produces “schematic processing” by filling in information quickly and automatically in a preconscious, pattern-completion sort of way. Associative processing operates automati- cally and preconsciously to structure people’s conscious experience, with little dependence on attention or cognitive resources. Smith and Neumann argue that associative processing also serves an alarm function, and this idea provides a framework for integrating material from other chapters that discusses the role of the amygdala in affect or emotion generation. Second, they discuss a rule-based system that is involved in a kind of emotion gen- eration in which events can be learned quickly, even after a single trial, that requires attention and other cognitive resources for its operation, and that is often associated with a sense of subjective effort.

By discussing emotion in dual-process terms, Smith and Neumann integrate the science of emotion into a larger framework that makes contact with other major theories of the human mind. Importantly, they point out that emotion theorists should resist the tendency to refer to associative pro- cessing as emotion elicitation, and to rule-based processing as emotion reg- ulation. In addition to the more automatic forms of emotion generation, it is possible to “think” oneself into an emotion by remembering a past event or by imagining something yet to happen. In fact, remembering prior emo- tional events and imagining hypothetical events are two of the most popu- lar ways of inducing emotion in the lab. Similarly, there are both rule-based forms of regulation (e.g., such as the reappraisal strategy investigated by Gross (1999, 2002) and Ochsner, Bunge, Gross, and Gabrieli (2002) and associative forms of regulation (as in contextual conditioning and extinction, as discussed by Bouton, Chapter 9).

In Chapter 13, Scherer discusses how unconscious and conscious pro- cesses configure to produce an emotional response, and concludes that the majority of emotional work is done by unconscious processes. He suggests that the emotion process for an individual begins with evaluating the signif- icance of a stimulus event. By evaluation, Scherer means something more complex that a simple “good for me/bad for me” judgment. Rather, he sug- gests that people automatically judge the stimulus event according to a set of appraisal rules or criteria (e.g., novelty, agreeableness, goal conducive- ness, and so on). These appraisals of stimulus meaning result in differ- entiated emotion. In his view, appraisals also cause specific preparatory responses associated with proprioceptive information that, when synchro- nized with conceptual knowledge about emotion, produces a conscious experience of emotion.

14 Introduction

Scherer’s model, as a type of appraisal model, is rooted in the view that the meaning of a stimulus for a given person in a given context at a particu- lar point in time elicits an emotional response, such that the character of that response is dictated by the contextual constraints. In principle, Scherer’s view admits great flexibility in emotional responding, although he organizes emotional responses into the familiar set of “basic” categories. In this, as in several other points, Scherer’s model bears some similarity to those of other theorists in this volume. He argues that emotional responses occur only when a stimulus has significant consequences in relation to a person’s needs, goals, or values; in this way emotion may be a sign of a potential control dilemma, as characterized by Gray et al. in Chapter 4. At the heart of Scherer’s model are two types of processing mechanisms that determine the emotional value of a stimulus—pattern matching and rule- based inference—and these are emblematic of the dual-process foundation of many emotion models (as discussed by Smith & Neumann, Chapter 12). Finally, Scherer proposes the intriguing idea that an identifiable emotional response results from a sort of perceptual binding that takes place when several types of information are synchronized. In this, he foreshadows the importance of understanding how cross-modal processing proceeds in emotional responding.

In Chapter 14, Winkielman, Berridge, and Wilbarger present the argu- ment that affective states can drive behavior in the absence of con- scious feeling. First they discuss evolutionary and functional considerations regarding the independence of mechanisms that control basic affective reactions from those of consciousness. They then present a functional neu- roanatomical model of unconscious affect, in which they identify the subcortical areas that are essential for triggering basic affective reactions and the cortical systems that support the conscious experience of affect. They suggest a functional decoupling of affect state and affective feelings based on evidence from neuropsychology, neuroscience, and experimental psychology that is consistent with the elicitation–experience distinction drawn by Prinz in Chapter 15. Their view is largely consistent other contri- butors who address emotion perception (Lundqvist & Öhman, Chapter 5; de Gelder, Chapter 6; Atkinson & Adolphs, Chapter 7), emotion and aware- ness (Phelps, Chapter 3), and affective responding (Owren et al., Chapter 8; Barrett, Chapter 11), although they stand in contrast to some of the ideas presented in Charland (Chapter 10). Furthermore, Winkielman et al. argue that these findings support the existence of unconscious emotion as well, with the argument that mechanisms responsible for differentiated emotion responding (e.g., fear, anger, disgust) can function in organisms that differ widely in their capacity for conscious experience and often do not require elaborated cortical processing. This position is in contrast to other that of

Introduction 15

other contributors (Barrett, Chapter 11; Clore, Storbeck, Robinson, & Centerbar, Chapter 16) who allow for unconscious affect but not uncon- scious emotion as coordinated packets of distinctive responses. Finally, Winkielman et al. present a functional discussion of when and why an affec- tive state is likely to be represented in awareness (or not). The basic idea is that to be conscious, affect needs to be represented by a hierarchical sys- tem of subcortical and cortical networks as well as integrated with higher- order categorical processes.

Prinz, in Chapter 15, also discusses two types of pathways in emotion processing that are similar to, but do not overlap with, the associative and rule-based processes discussed by Smith and Neumann (Chapter 12) and Scherer (Chapter 13). First, Prinz argues that some paths are involved in emotion elicitation of which a person is not aware. Similar to Scherer, Prinz argues that these paths produce a small set of “basic” emotion categories that can be distinguished by their behavioral and autonomic patterns (although there may be some heterogeneity within a category). Yet, no sin- gle somatic component corresponds to an emotional state on its own. Rather, Prinz echoes Scherer in suggesting that some sort of integration is necessary. Second, he argues that a separate path is involved in the con- scious perception of these embodied states. He draws an analogy between emotion processing and visual processing, where emotion elicitation is more like early visual processing, and the conscious experience of emotion is more like mid-level visual processing in which patterns of responses are perceived. As suggested by other authors contributing to this volume, per- ception requires attention, although attention need not be effortful or intentional. All told, Prinz outlines a model of emotion that is similar to that of William James and consistent with other views of embodied emotional processing that are discussed in this volume.

In the concluding chapter, Clore, Storbeck, Robinson, and Centerbar call attention to and question seven of the assumptions (“sins”) that ground much of the existing research on emotion and that characterize many (although certainly not all) of the perspectives offered in this volume. Each challenge does find common ground, however, with at least one other con- tribution in this volume. First, Clore et al. question whether emotion can truly be considered implicit or unconscious. They suggest that although most emotional processes are unconscious, there may be no unconscious emotions per se. In this, they agree with Barrett (Chapter 11). Second, Clore et al. question the tendency to treat subcortical processing (i.e., involving the amygdala) in humans as the locus of “real” emotion, with cor- tical contributions serving only a regulatory function after the fact. In addi- tion, they make the provocative claim that the particular subcortical route discovered by LeDoux, which serves as the centerpiece of emotional pro-

16 Introduction

cessing in many of the chapters in this volume, really has limited influence on emotion-related processing in humans. Third, Clore et al. question the causal status of affective feelings. In their view, an unconscious affective state can have a direct influence on behavior. In this, Clore et al. seem to agree with Barrett (Chapter 11) and Winkielman et al. (Chapter 14). But Clore et al. also allow that unconscious affect can indirectly influence behavior through conscious feeling. In particular, these authors argue that conscious feelings are a potent tool for ensuring that explicit judgments and choices are consistent with the judgments and choices that are derived from unconscious affect. In this sense, feelings can be used to resolve any control dilemmas (Gray et al., Chapter 4) that may be in evidence. More- over, Clore et al. suggest that feelings of arousal play a role in attention and that unconscious components of arousal play a role in memory. To some extent, this view agrees with points made by Phelps (Chapter 3).

Fourth, Clore et al. argue against the notion that preferences precede inferences, instead arguing that evaluative processing is a special case of semantic processing. Fifth, they argue against the idea that expressive actions (such as arm flexions) have direct, fixed effects on affective state. Instead, they suggest that affect is elicited by a mind in context, and they review data showing how the influence of a physical action on affect depends on the contextual meaning of an action. This view seems entirely consistent with Owren et al. (Chapter 8), and also with contemporary views of embodied conceptual processing, such those advanced by Niedenthal et al. (Chapter 2) and Barrett (Chapter 11) who see embodied processes as largely driven by contextual considerations. Sin #6 addresses the common wisdom that the amygdala is adequate to trigger emotion. Instead, Clore et al. argue that semantic processing appears to be necessary for affective computations involving visual stimuli. They seem to base this argument on the fact that areas of the visual association cortex (linked with stimulus rec- ognition) are important in the amygdala’s response to stimuli. Certainly, the amygdala alone is not sufficient for affective computations, but it would certainly seem necessary, and the difference between the position ad- vanced by Clore et al. and that represented in other chapters in this volume is one of emphasis more than kind.

Finally, Clore et al. argue that appraisal theories have been fundamen- tally misunderstood; the claims made by appraisal theorists have generally not concerned the processes involved in generating emotion, as intimated by Prinz (Chapter 15) and many other critics. Rather, these theories reveal the structure of emotion—the rules about which emotions are felt when. In this sense, appraisals describe the structure of emotion in terms of its cog- nitive, perceptual, or situational causes, but not in terms of some temporal flow of processes.

Introduction 17

COMING TOGETHER

Due to the exquisite balance of similarity and difference—in focus, in level of analysis, and in mechanistic accounts—we believe that the chapters in this volume contain a research agenda and a set of core themes and integra- tive theories for future work on emotion and consciousness. It has often been said that the literature on emotion is a group of descriptions of very small pieces of the very large “elephant” that is emotion (e.g., Russell & Barrett, 1999). For this very reason, some researchers prefer to avoid theo- rizing about emotion altogether, even when developing influential theories of memory, attention, or social cognition. Emerging from this volume, we believe, is a semblance of an elephant.

One reason for the elephant’s emergence is that broader models can now account for, and integrate findings across, levels of analysis, so that psychological concepts of thinking and feeling, conscious and unconscious can be biologically grounded. One example of a broad model that emerges from several chapters is the “embodiment” perspective, which explains fundamental and sweeping concepts such as empathy, emotion perception, emotion experience, perspective taking, emotional learning, and conflict resolution with an increasingly similar set of assumptions and mechanisms. A core affect perspective (Russell, 2003) also holds some promise for inte- grating findings across several key literatures involved with understanding emotion-related processing. This perspective is broadly consistent with the data discussed in many chapters of this volume, and in neurobiological models of emotion-related processing (e.g., Rolls, 1999). Of course, there may be other models, as well.

That being said, many features of the elephant need to be empirically established. Although the contributors to the present volume do not always agree in the content of their arguments, we moved toward agreement on what the central arguments are and how to resolve them. This consensus means, we hope, that future debates in the area of emotion can begin to use the same language and take place within compatible scopes of inquiry— rather than on different planets.

REFERENCES

Aristotle. (1941). On the soul. In R. McKeon (Ed.), The basic works of Aristotle. New York: Random House.

Barrett, L. F. (1996). Hedonic tone, perceived arousal, and item desirability: Three components of self-reported mood. Cognition and Emotion, 10, 47–68.

Cacioppo, J. T., Gardner, W. L., & Bernston, G. G. (1999). The affect system has par-

18 Introduction

allel and integrative processing components: Form follows function. Journal of

Personality and Social Psychology, 76, 839–855.
Gross, J. J. (1998). Antecedent- and response-focused emotion regulation: Diver-

gent consequences for experience, expression, and physiology. Journal of Per-

sonality and Social Psychology, 74, 224–237.
Gross, J. J. (2002). Emotion regulation: Affective, cognitive, and social conse-

quences. Psychophysiology, 39, 281–291.
Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural

system for face perception. Trends in Cognitive Sciences, 4, 223–233. Lambie, J. A., & Marcel, A. J. (2002). Consciousness and emotion experience: A

theoretical framework. Psychological Review, 109, 219–259
Lane, R. D., Nadel, L., Allen, J. J. B., & Kaszniak, A. W. (2000). The study of emo- tion from the perspective of cognitive neuroscience. In R. D. Lane & L. Nadel (Eds.), Cognitive neuroscience of emotion (pp. 3–11). New York: Oxford Uni-

versity Press.
LeDoux, J. E. (1996). The emotional brain: The mysterious underpinnings of emo-

tional life. New York: Simon & Schuster.
Milad, M. R. & Quirk, G. J. (2002). Neurons in medial prefrontal cortex signal

memory for fear extinction. Nature, 240, 70–74.
Morgan, M. A., Romanski, L. M., & LeDoux, J. E. (1993). Extinction of emotional

learning: Contribution of medial prefrontal cortex. Neuroscience Letters, 163,

109–113.
Ochsner, K. N., Bunge, S. A., Gross, J. J., & Gabrieli, J. D. E. (2002). Rethinking

feelings: An fMRI study of the cognitive regulation of emotion. Journal of

Cognitive Neuroscience, 14(8), 1215–1229.
Phillips, R. G., & LeDoux, J. E. (1994). Lesions of the dorsal hippocampal forma-

tion interfere with background but not foreground contextual fear condition-

ing. Learning and Memory, 1, 34–44.
Rolls, E. T. (1999). The brain and emotion. New York: Oxford University Press. Russell, J. A. (2003). Core affect and the psychological construction of emotion. Psy-

chological Review, 110, 145–172.
Russell, J. A., & Barrett, L. F. (1999). Core affect, prototypical emotional episodes,

& other things called emotion: Dissecting the elephant. Journal of Personality and Social Psychology, 76, 805–819.

PART I Cognition and Emotion

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CEOmGboNdIimTIeOnNt anAdNEDmEoMtioOnTKInOoNwledge

CHAPTER 2

Embodiment in the Acquisition and Use of Emotion Knowledge

PAULA M. NIEDENTHAL LAWRENCE W. BARSALOU FRANÇOIS RIC SILVIA KRAUTH-GRUBER

The past 50 years have seen an exponential increase in the number of jour- nal and book pages devoted to reports and discussions of research on emo- tion. Despite the growth of interest in the empirical study of emotion, however, the literature remains largely unintegrated. Researchers have in- dependently studied the processes involved in the perception, interpreta- tion, experience, and use of knowledge about emotion, relying on very dif- ferent theoretical orientations. In addressing such apparently wide-ranging problems, for example, emotion researchers have tested principles of evo- lutionary theory with the use of facial expression recognition data and with the use of autonomic nervous system data; they have pursued cognitive the- ories of emotion and measured reaction times to categorizing words or studied judgments of similarity between words denoting emotional states; and they have evaluated social constructivist theories with the use of lin- guistic analyses and archival data on social customs. In this chapter, we seek to understand the body of knowledge about emotion with a single mechanistic account. Following the pun present in the preceding sentence, in the present chapter, we introduce the notion of embodiment and argue

21

22 COGNITION AND EMOTION

1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

The topic of the chapter is the processing of emotional information and emotion concepts. Our point is that processing emotional information involves a simula- tion of the corresponding emotional state or cue in the perceiver. Consistent with many basic emotion theorists, emotions are defined as short-term, biologi- cally based patterns of perception, subjective experience, physiology, and action (or action tendencies) that constitute responses to specific physical and social problems posed by the environment.

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

By consciousness we mean the object of attention. Once attention has been directed at an embodied emotion, then it can become a subject of advanced representational processes. As noted at the end of the chapter, this will have many consequences for the subjective experience of emotion.

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

We have suggested that although emotions are embodied, this embodiment need not be conscious. It is also possible that some embodied components of emotion, such as the perceptual patterns that define them, can never be con- scious. When conscious attention is directed to the cognitively penetrable

that the acquisition of knowledge about emotion—the perception, recogni- tion, and interpretation of an emotion in the self or other—involves the embodiment of emotional states, and the use of emotion knowledge in- volves the reenactment of these same states. In other words, we think that (1) perceiving emotions involves embodiment, and (2) using emotion knowledge relies on the very same somatosensory and motor states. The implication of this perspective is that perceiving someone else’s emotion, having an emotional response or feeling oneself, and using emotion knowl- edge in conceptual tasks are all fundamentally the same process.

In the sections that follow, we provide evidence for the following four claims: (1) Individuals embody other people’s emotional behavior; (2) embodied emotions produce corresponding subjective emotional states in the individual; (3) imagining other people and events also produces embod- ied emotions and corresponding feelings; and (4) embodied emotions medi- ate cognitive responses. After reviewing this evidence, we discuss how the-

Embodiment and Emotion Knowledge 23

ories of embodied cognition can account for these types of effects (we focus largely on Barsalou’s [1999a] recent theory of embodied cognition). We end by identifying implications of this approach for understanding conscious and unconscious aspects of emotion.

WHAT IS EMBODIMENT?

By embodiment we mean the bodily states that arise (e.g., postures, facial expressions, and uses of the voice [i.e., prosody]) during the perception of an emotional stimulus and the later use of emotional information (in the absence of the emotional stimulus). In the area of emotion the concept of embodiment is associated with the theory of William James (1890/1981), who argued that individuals’ perceptions of the bodily states that occur in the presence of emotional events constitute their emotions (really, their feelings), in the sense of “feeling” somatosensory and motor changes. In essence, James defined emotions as the conscious perception of bodily states. Although our aims are somewhat different—we are concerned with the theoretical grounding for emotion concepts—we come full circle and return to James in this chapter. We propose that the bodily states, or embodiments of emotion, can be, and often are, unconscious, and that the feeling states are conscious. If we consider that embodiments can be unconscious until consciously attended to and manifested as feelings, then the general debate about whether emotion is conscious or unconscious becomes, in our mind, more tenable, and the various disagreements on this point (e.g., see Winkielman, Berridge, & Wilbarger, Chapter 14; Clore, Storbeck, Robinson, & Centerbar, Chapter 16) can be reconciled. It is, above all, necessary to decide whether an emotion is a bodily state, a feeling state, or both.

INDIVIDUALS EMBODY OTHERS’ EMOTIONAL GESTURES AND BEHAVIORS

In this first section we review empirical evidence for the claim that people embody the emotional behaviors of others. These behaviors may include, but are not limited to, facial expressions, postures, and vocal parameters that convey emotion. Here we present evidence concerning the ubiquity of imitation; in the next section we discuss the relations between imitation and subjective emotional state. There is evidence suggesting that such imi- tation is automatic, in that it does not have to be conscious or intentional. However, it is clear that goals, such as the goal to empathize, can enhance or suppress the tendency or the effort put into imitation.

24 COGNITION AND EMOTION

Embodiment of Facial, Postural, and Vocal Expressions of Emotion

Probably the most extensive evidence for the embodiment of others’ emo- tional behavior involves the facial and vocal expressions of emotion. In sev- eral frequently cited studies, Dimberg (1982, 1990) showed that 8-second presentations of slides of angry and happy faces elicited facial electro- myographic (EMG) responses in perceivers that corresponded to the per- ceived expressions. For example, zygomatic activity (which occurs when individuals smile) was higher when participants viewed a happy, com- pared to an angry, face. In addition, corrugator activity (which occurs when individuals frown) was elevated when participants viewed an angry face, and it decreased when participants viewed a happy face. Furthermore, these effects were obtained when the faces were presented subliminally (Dimberg, Thunberg, & Elmehed, 2000).

Vaughan and Lanzetta (1980) used a vicarious conditioning paradigm in which participants viewed the videotaped facial expression of pain dis- played by a confederate (unconditioned stimulus) while working on a paired-association learning task. The pain expression that always followed a target word of the same word category (flower or tree names) produced a similar facial response in the observer during the confederate’s pain expres- sion, as indicated by EMG activity (for related findings, see Bavelas, Black, Lemery, & Mullett, 1987).

Embodiment of positive facial expressions was demonstrated by Bush, Barr, McHugo, and Lanzetta (1989). In their study participants viewed two comedy routines. In one, smiling faces had been spliced into the film concurrent with sound-track laughter. Half of the participants were in- structed to inhibit their facial expressions. The half whose expressions were spontaneous—that is, in whom mimicry was permitted—displayed greater zygomatic and oricularis activity during the spliced segments than during the segments without smiling faces. Research by Leventhal and col- leagues (Leventhal & Mace, 1970; Leventhal & Cupchik, 1975; Cupchik & Leventhal, 1974) similarly showed that exposure to the expressive displays of others produces mimetic responses in observers (and see Chartrand & Bargh, 1999).

McHugo and colleagues studied the embodiment of more complex expressive behaviors (including facial expression, gaze direction, and bodily posture) of political leaders on observers’ facial reactions as a function of their prior attitudes. In one study (McHugo, Lanzetta, Sullivan, Masters, & Englis, 1985), participants watched televised news conferences of then- President Ronald Reagan. Independent of their prior attitudes, participants showed increased brow activity (contraction of the corrugator supercilii

Embodiment and Emotion Knowledge 25

muscle) in response to Reagan’s negative expressions and reduced cheek activity (low zygomatic major activity) during Reagan’s positive expressions. Finally, emotional embodiment has been shown for emotional prosody. In a recent study by Neumann and Strack (2000), participants listened to recorded speeches that were read in either a sad or a happy voice. Under the pretext that the experimenters were interested in whether memory for the content of a speech is improved by the simultaneous reproduction of it by the listener, the participants had to repeat the content of the speech aloud as they listened to it. Thus the participants were focused on the con- tent of the speech that they were instructed to repeat, not on the prosody of the speaker. Different participant-judges later rated the emotional prosody of the initial participants as they repeated the speech. Results showed that participants embodied the prosody of the speakers when shadowing their speech, even though prosody was completely irrelevant to task perfor-

mance, and they were unaware of the influence on their own prosody.
In sum, a large number of studies over the last 30 years has docu- mented the ubiquity of facial, postural, and prosodic embodiment. These studies all show that individuals partly or fully embody the emotional expressions of other people, and some of the results also show that this pro- cess is either very subtle, and likely to occur outside of consciousness, or unmoderated by contextual factors, suggesting that such embodiment is highly automatic in nature. Why would the embodiment of others’ facial, bodily, and vocal expressions of emotion be so automatic and so ubiquitous? In the present view, imitation is the mechanism by which observers come to comprehend the emotions of others. But, of course, this premise would only make sense if the imitation produced a corresponding state in the observer (for a discussion, see Décety & Chaminade, 2003; Zajonc, Adlemann, Murphy, & Niedenthal, 1987). Indeed, much research has

tested this notion, and it is to such work that we turn next.

EMBODIMENT OF OTHERS’ EMOTIONS PRODUCES EMOTIONAL STATES

In some of the studies described in the previous sections, researchers mea- sured not only the embodiment of others’ emotional gestures, but also the occurrence of corresponding emotional states in the perceiver. For exam- ple, in the study by Vaughan and Lanzetta (1980), participants not only imi- tated the confederate’s painful expressions, they also responded to the con- federate’s pain expression as if they were in pain (as indicated by an increase in autonomic arousal). Furthermore, in a follow-up study, Vaughan and Lanzetta (1981) found that the vicarious emotional responses elicited

26 COGNITION AND EMOTION

by observing the confederate’s painful expression could be modified by the opportunity for embodiment, in particular, by the instruction to suppress or amplify facial expression during the confederate’s shock period. Consistent with an embodiment account, participants in the amplify condition who embodied the expressions of pain showed higher autonomic arousal com- pared to both no-instruction participants and participants in the inhibition condition who had to suppress their facial expressions.

Feedback effects of mimicked facial expression on participants’ emo- tional experience were also found in a study by Hsee, Hatfield, Carlson, and Chemtob (1990). Participants were secretly filmed while watching a videotaped interview of a fellow student who described either one of the happiest or one of the saddest events in his or her life, and who displayed the corresponding expressive behavior (i.e., happy or sad facial expressions, gestures, posture, tone of voice). Participants not only embodied the emo- tional expressions of the target person they viewed (evaluated by judges who rated the videotaped facial expressions of the participants), but also their own emotions were affected by the emotional expression they mim- icked.

Finally, neuroscientific evidence that imitated emotion gestures pro- duce emotions was found by Hutchison and colleagues, who examined the activation of pain-related neurons in patients (Hutchison, Davis, Lozano, Tasker, & Dostrovsky, 1999). Importantly, they found that not only were such neurons also activated when a painful stimulus was applied to the patient’s own hand, but the same neurons were also activated when the patient watched the painful stimulus applied to the experimenter’s hand. This finding was interpreted as evidence of an embodied simulation in the perceiver of what was happening to the perceived person (see Gallese, 2003, for summaries of related research).

The studies just reviewed provide correlational evidence that people’s embodiments of others’ emotional gestures are accompanied by congruent emotional states or responses. However, except for a few demonstrations in which mimicry was experimentally inhibited or facilitated, it cannot be concluded from the studies that embodiment causes emotional states. We next review research that suggests that emotion-specific embodied states, such as facial expressions, vocal expressions, and bodily postures, can pro- duce the corresponding emotion or at least modulate the ongoing emo- tional experience.

Effects of Facial Embodiment:
Tests of the Facial Feedback Hypothesis

Most of the research that demonstrates the influence of embodied emotions on emotional state was conducted with the aim of testing the facial feed-

Embodiment and Emotion Knowledge 27

back hypothesis, according to which feedback from facial musculature has direct or moderating effects on emotional state (for a review of findings and mechanistic accounts, see Adelmann & Zajonc, 1989; McIntosh, 1996). In canonical facial feedback studies, participants’ facial expressions were manipulated by the experimenter’s demand to pose (facilitate) or hide (inhibit) their spontaneous emotional expression, by using a muscle-to- muscle instruction that specified the facial muscle to contract, or by nonemotional tasks that allowed the experimenter to guide the production of facial expressions without cueing the emotional meaning of the expres- sion. In many such studies, the opportunity to experience emotion was pre- sented in the form of a variety of emotional stimuli, such as painful electric shocks, pleasant and unpleasant slides and films, odors, or imagery, and the moderation of the emotion by facial expression was assessed. Findings demonstrated that the intensity and quality of the participants’ manipulated facial expression affected the intensity of their self-reported emotional feel- ings as well as their autonomic responses.

For example, in three experiments, Lanzetta, Cartwright-Smith, and Kleck (1976) demonstrated that manipulated facial expression affected the intensity of emotional reactions during the anticipation and reception of electric shocks. In Study 1 participants received an initial set of shocks (baseline sequence) that varied in intensity, and rated the aversiveness of each received shock. Shock intensity was announced by a shock signal slide. For the second set of shocks, participants were instructed to hide their facial display in response to anticipating the shocks announced by the slide. The inhibition instruction caused low- and medium-intensity shocks to be experienced as less painful, but did not decrease the painfulness of high-intensity shocks. In a follow-up study the same basic procedure was used, but this time expression-inhibition as well as expression-exaggeration instructions were given in the manipulation sequence. Participants who were asked to simulate anticipating and receiving no shocks (inhibition in- struction) reported experiencing the shocks as less aversive and painful compared to participants who simulated intense shocks (exaggeration in- struction). Similar results were found in a study by Kopel and Arkowitz (1974).

Kleck, Vaughan, Cartwright-Smith, Vaughan, Colby, and Lanzetta (1976) manipulated participants’ facial expressions by social means. The presence of an observer during the receipt of either no-, low-, or medium- intensity shocks attenuated participants’ facial expressivity (natural inhibi- tion) and produced lower self-rated painfulness of shocks compared to the alone condition. Using pleasant and unpleasant slides as emotion-eliciting stimuli, Lanzetta, Biernat, and Kleck (1982) induced contextual inhibition of facial expression by the means of a mirror installed in front of the partici- pants. The mirror had attenuating effects on both participants’ expressivity

28 COGNITION AND EMOTION

and the self-reported intensity of felt pleasantness–unpleasantness. Similar attenuating as well as facilitating effects of facial expression, manipulated by suppression–exaggeration instructions, were also found with pleasant and unpleasant films (Zuckerman, Klorman, Larrance, & Spiegel, 1981) and odors (Kraut, 1982).

Such modulating effects of facial expressions were also found in stud- ies that used less obvious facial manipulations. In Laird (1974), participants contracted specific facial muscles involved in smile or frown expressions while watching positive and negative slides (Study1) or humorous cartoons (Study 2). “Smiling” participants felt happier while viewing positive slides, whereas “frowning” participants felt angrier while viewing negative slides. Incongruent expressions were shown to attenuate their feelings (see also Rutledge & Hupka, 1985).

Although most of this research demonstrates that facial expressions modulate emotions induced by emotional stimuli, several studies have shown that facial expressions can also initiate corresponding emotional experience in the absence of any emotional stimulus. For instance, using a muscle-to-muscle instruction procedure similar to Laird’s (1974), Duclos et al. (1989) instructed participants to adopt facial expressions of fear, anger, disgust, or sadness while listening to neutral tones. Participants then rated their feelings on several emotion scales. Self-reported fear and sadness were highest in the fear and sadness expression trials, respectively, and higher than in the other three expression trials. Equally high anger and dis- gust ratings were found in the anger and disgust expression trials, which were higher than in the other two expressing trials. Finally, evidence for the emotion-initiating power of facial expressions was found in other studies in which emotion-specific facial expressions, manipulated by muscle-to-mus- cle instructions, resulted in self-reports of the associated emotion (Duncan & Laird, 1977, 1980), especially for participants whose faces best matched the prototypical emotional expression (Ekman, Levenson, & Friesen, 1983; Levenson, Ekman, & Friesen, 1990), and for participants who were more responsive to their inner bodily cues than to external situational cues (Duclos & Laird, 2001; see also Soussignan, 2002).

Effects of Postural Embodiment

Sir Francis Galton (1884) believed that people’s attitudes and feelings are reflected in their bodily postures. In an anecdotal way, he suggested that observing the bodily orientation of people during a party could reveal their attraction or “inclination” to one another. Bull (1951) was one of the first to examine the relation between bodily posture and emotional experience. In one study she induced the emotions of disgust, fear, anger, depression, and joy through hypnosis and found that participants automatically adopted

Embodiment and Emotion Knowledge 29

the corresponding bodily postures. Furthermore, when asked to adopt emotion-specific postures, participants reported experiencing the associ- ated emotions.

Since the work of Bull, several experimental studies have directly explored the impact of bodily posture on emotional experience. For exam- ple, Duclos et al. (1989) studied the impact of emotion-specific bodily pos- tures on participants’ feelings. All participants had to listen to the same series of neutral tones, which were not intended to induce specific emo- tions but were presented as part of a multiple-tasks procedure. In an unob- trusive way, they were also asked to adopt bodily postures associated with anger, fear, or sadness. As expected, posture facilitated the emotional expe- rience of the corresponding emotion. Participants reported feeling sadder in the sad posture, more fearful in the fear posture, and angrier in the angry posture.

In Stepper and Strack (1993) participants’ bodily posture was manipu- lated in an unobtrusive way by either having them adopt a conventional working position or one of two ergonomic positions (upright or slumped posture) when receiving success feedback concerning their performance on an achievement task. Participants who received success feedback in the slumped posture felt less proud and reported being in a worse mood than participants in the upright position and participants in a nonmanipulated control group, who did not differ from one another (see also Riskind & Gotay, 1982).

Flack, Laird, and Cavallaro (1999) examined both separate and com- bined effects of facial expression and bodily posture related to anger, sad- ness, fear, and happiness on corresponding emotional experience. Repli- cating the results of Duclos et al. (1989), they found specific effects of expressive behavior on participants’ self-reported emotional feelings. Par- ticipants always felt the specific emotion they were enacting either with their face or with their body posture. Furthermore, they found that com- bined effects of matching facial and bodily expressions produced stronger corresponding feelings.

Effects of Vocal Embodiment

In a series of experiments Hatfield, Hsee, Costello, Weisman, and Denney (1995) instructed participants to listen to tapes with sound patterns that they then had to reproduce into a telephone. The sounds were designed to convey the characteristics associated with specific emotions (joy, love, fear, sadness, anger, neutral). Participants’ self-reported emotions were affected by the spe- cific sounds they produced. This result demonstrated that emotion-specific tone of voice amplifies the corresponding emotional feeling. Siegman, Ander- son, and Berger (1990), in turn, showed that vocal expression can be used, like

30 COGNITION AND EMOTION

facial or postural expression, to regulate or control one’s emotion. Partici- pants who were instructed to discuss an anger-provoking topic in a slow and soft voice felt less angry and their heart rate slowed. Those who had to speak loudly and rapidly felt angrier and became more physiologically aroused.

Summary

Taken together, the studies reviewed in this section demonstrate that peo- ple’s expressive behavior not only facilitates but can also produce the corre- sponding emotional experience. Facial expressions, bodily posture, and vocal expressions have emotion-specific, facilitative effects on self-reported emotional feelings, as well as effects on other measures of emotional experi- ence. Facial, postural, and vocal embodiments not only modulate ongoing emotional experience but also facilitate the generation of the corresponding emotions. These findings strongly suggest that the embodiment or simula- tion of others’ emotions provides the meaning of the perceived event. Per- haps, then, this is a general rule. Perhaps emotional meaning is the partial or full embodied simulation of an emotion. If this were the case, then simu- lation in the absence of a triggering affective perception or stimulus would involve embodied responses. Furthermore, simulating a particular emotion would affect the ease of processing the symbols associated with affective meanings. It is to the evidence for these two proposals that we turn next.

AFFECTIVE IMAGERY IS ACCOMPANIED BY EMOTION PROCESSES

Numerous studies have used imagery related to simulations of past experi- ences to manipulate emotional states in the laboratory (e.g., Bodenhausen, Kramer, & Süsser, 1994; Schwarz & Clore, 1983; Strack, Schwarz, & Gschneidinger, 1985; Wegener, Petty, & Smith, 1995). However, in these studies, it is not clear whether the required imagery activated emotion pro- cesses or only primed information merely associated with specific emotion words, which then guided subsequent judgments that constituted a depen- dent variable of interest (Innes-Ker & Niedenthal, 2002; Niedenthal, Rohmann, & Dalle, 2003).

Research designed to test just this question has indeed found that physiological changes resulting from imagery parallel those obtained in the presence of the stimuli eliciting the same emotion. For instance, Grossberg and Wilson (1968) asked participants to imagine themselves in various situ- ations. One half of the situations had been evaluated by each participant as fearful, and the other half were rated as neutral. Results indicated that sig-

Embodiment and Emotion Knowledge 31

nificant changes in heart rate and skin conductance between baseline (as measured for each individual at the beginning of the experimental session) and presentation of the situation (read by an experimenter) were similar for neutral and fearful situations. However, the increase in physiological responses between presentation and simulation were more marked for fear- ful situations than for neutral (see also Lang, Kozak, Miller, Levin, & McLean, 1980; Vrana, Cuthbert, & Lang, 1989).

In a related experiment, Gollnisch and Averill (1993) extended these results to other emotions. They asked participants to imagine situations that involve fear, sadness, anger, or joy. Measures included heart rate, electro- dermal activity, and respiration. Mean levels of heart rate were significantly higher during imagery than baseline but did not differ as a function of emo- tion. Mean respiratory rates increased significantly during imagery in com- parison with baseline (as measured in 2-minute pretrial rest period), but only for fear, anger, and joy; sadness produced a decrease in respiratory rates. Skin conductance was unresponsive to the manipulation (Gehricke & Fridlund, 2002; Gehricke & Shapiro, 2000).

Vrana and Rollock (2002; see also Vrana, 1993, 1995) presented partici- pants with emotional imagery scenarios related to joy, anger, fear, or neu- tral. Participants were asked to imagine they were actually in the scene, participating actively in it. As expected, facial expression (as measured by EMG activity at zygomatic and corrugator facial muscles) differed as a function of emotional tonality of the scenario (see also Dimberg, 1990). Corrugator activity was greater during fear and anger simulation than dur- ing neutral and joy scenarios. In contrast, zygomatic activity was greater during joy than during any other scenario.

Differences between imagery of sadness versus joy situations were also found. For instance, Gehricke and Fridlund (2002) found that the simu- lation of joy situations led to greater EMG activity in the cheek region than simulations of sad situations, whereas the reverse was true for EMG activ- ity in the brow region.

Finally, similar results were found when participants were asked to imagine fictitious persons (Vanman, Paul, Ito, & Miller, 1997) or to think about persons whose descriptions were designed to covertly resemble those of significant others participants liked or disliked (Andersen, Reznik, & Manzella, 1996).

In sum, a sizable literature now demonstrates that when emotional events are simulated using imagery, and in the absence of the initial stimu- lus, individuals reenact or relive the emotions, or partial feelings of emo- tion, as indicated by a number of different measures of emotion. If it is the case that the mental processing of past experience can produce embodied emotion, then we can ask whether the process of embodying emotions

32 COGNITION AND EMOTION

interacts with the processing of emotional meaning per se. In the next sec- tion we show that this is indeed the case.

EMBODIED EMOTIONS MEDIATE COGNITIVE RESPONSES

A growing body of research has demonstrated that embodied emotions influence cognitive responses to emotional information. In the following section, we present evidence of such an impact on stimulus identification, stimulus evaluation, and recall.

Stimulus identification

Neumann and Strack (2000, Experiment 1) instructed participants to indi- cate as quickly as possible whether adjectives presented on a computer screen were positive or negative. While performing the task, participants either pressed the palm of their nondominant hand on the top of the table (extension condition) or used their palm to pull up on the underside of the table (flexion condition). These motor movements were manipulated because they are associated with positive affect and approach (arm flexion) and with negative affect and avoidance (arm extension; e.g., Cacioppo, Priester, & Berntson, 1993). Arm flexion facilitated the identification of pos- itive information, whereas arm extension facilitated the identification of negative information. These results suggest that affective movement facili- tates the encoding of affective information of the same valence.

This kind of effect could be the basis of facial expression recognition (Zajonc & Markus, 1984; Zajonc, Pietromonaco, & Bargh, 1982). Indeed, Wallbott (1991) proposed that imitation of facial expression facilitates its recognition. He instructed participants to identify the emotion expressed in a series of face pictures. While performing the task, participants’ faces were covertly videotaped. Two weeks later, each participant was asked to watch the videotape of him- or herself while he or she performed the identifica- tion task, and to guess the identification of the facial expression being judged (which was, of course, not visible). The participants identified the emotion expressed in the pictures above chance level by seeing only their own facial expression while performing the task. These results are compati- ble with the idea that participants had partially simulated others’ facial expression while performing the identification task and that this simulation provided emotional cues for identifying the emotion presented in the pic- ture (see also Niedenthal, Brauer, Halberstadt, & Innes-Ker, 2001; Adolphs, Damasio, & Tranel, 2002; Atkinson & Adophs, Chapter 7, for convergent neuropsychological evidence).

Embodiment and Emotion Knowledge 33

Evaluation

Evaluation responses also seem to be mediated by embodied emotions (but for an alternative view, see Clore et al., Chapter 16). Cacioppo and col- leagues (1993), for example, exposed participants to neutral Chinese ideo- graphs, and participants rated each one on a liking scale. Participants per- formed the task while pressing their palm on the top (arm extension) or pulling it up from the underside (arm flexion) of the table. The ideographs were judged as more pleasant during arm flexion than during arm exten- sion. Subsequent studies demonstrated that participants associated arm flexion with an approach motivational orientation, but only when they per- formed the musculature contraction, not when they merely watched some- one else performing it.

Using a different type of embodiment manipulation, Strack, Martin, and Stepper (1988) found that participants instructed to hold a pencil between their front teeth, thus unobtrusively expressing a smile, evaluated cartoons as funnier, compared with participants asked to hold a pencil between their lips, without touching the pencil with their teeth (which pro- duced a frown expression), or participants instructed to hold the pencil in their nondominant hand (a control condition).

Ohira and Kurono (1993) asked participants to exaggerate their (nega- tive) facial expressions while reading a text presenting a target person as somewhat hostile, under the cover story of transmitting nonverbal informa- tion to a person who was supposedly on the other side of a one-way mirror. These participants later judged the target more negatively than participants who had been asked to conceal their facial expressions or who were not given instructions concerning their facial expressions.

Memory

Laird, Wagener, Halal, and Szegda (1982) asked participants to read pas- sages related either to anger or happiness. After an interpolated task, par- ticipants were instructed to recall as much information as possible about the presented stories while contracting specific facial muscles so that they expressed either a happy or an angry face (importantly, the instructions did not refer to happiness or anger). Participants expressing an angry face recalled more of the angry passages than participants expressing a happy face, whereas the reverse was true for happy passages. A second experi- ment generalized these findings to fear, anger, and sadness, thus ruling out the possibility that frowning leads to better recall of any negative informa- tion.

Moreover, by controlling facial expressions at encoding, Laird et al. were able to rule out another interpretation in terms of state-dependent

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retrieval. That is, a possible account of the Experiment 1 findings is that participants reading, for instance, angry passages had felt anger, and that the manipulation of a facial expression of anger produced the same state, which then served as a retrieval cue (i.e., an example of state-dependent retrieval). In Experiment 2, they found that the facial expression at recall still affected memory performance in an emotion-congruent manner when controlling for the facial expression at encoding; that is, participants main- tained the same emotion expression throughout the experiment.

Schnall and Laird (2003) also demonstrated that such effects could be obtained even when (1) the facial expression is not maintained at time of recall, and (2) when recall implied an autobiographical event that required long-term memory. Consistent with these findings, Riskind (1983) found that participants who expressed smiles were faster at recalling pleasant autobiographical memories and took longer to recall unpleasant memories than participants who expressed a sad face.

Similar results were found when emotional gestures other than facial expressions were manipulated. Förster and Strack (1996) instructed par- ticipants to listen to positive and negative adjectives while performing either horizontal head movements (shaking, associated with negative atti- tude), vertical movements (nodding, associated with agreement), or circular movements (control condition), following a procedure designed by Wells and Petty (1980). They found that recognition of positive words was better when the presentation of these words was associated with vertical move- ments (nodding), whereas recognition of negative words was better when presentation of these words was associated with horizontal movements (head shaking; see Förster & Strack, 1997, 1998, for replications).

We have reviewed existing findings that suggest that individuals embody others’ emotions, that such embodiment causes corresponding emotions in the perceiver, and that embodiment seems to be involved in facilitating and inhibiting the cognitive processing of emotional information more generally. In the next section we describe a recent theory of concep- tual processing that can, we think, account for the ensemble of findings and the way we have linked and interpreted them to this point.

THEORETICAL ACCOUNTS
OF EMBODIED EMOTION EFFECTS

How do we explain the roles of embodiment in emotional phenomena? What implications do these phenomena have for the emotion concepts that people use to interpret emotional experience? The standard answer to such questions is that amodal knowledge structures represent emotion concepts,

Embodiment and Emotion Knowledge 35

and embodied states are peripheral appendages that either trigger or indi- cate the activation of the amodal structures. An alternative account is that embodiments constitute the core conceptual content of emotion concepts. That is, rather than serving as peripheral appendages to emotion concepts, embodiments constitute their core meanings. We address each of these two approaches in turn.

Amodal Accounts of Embodied Emotion Effects

The Transduction Principle

The amodal view of emotion concepts dominates the cognitive sciences and reflects a much wider view of knowledge. The key assumption underlying this view is the transduction principle, namely, the idea that knowledge results from transducing modality-specific states in perception, action, and introspection into amodal data structures that represent knowledge (Barsalou, 1999). To understand how the transduction principle works, first consider the modality-specific states that initiate the transduction process. Such states arise in sensory systems (e.g., vision, audition, taste, smell, touch), the motor system (e.g., action, proprioception), and introspection (i.e., mental states such as emotions, affects, evaluations, motivations, cog- nitive operations, memories).

The representation of these states can be thought of in two ways. First, these states can be viewed as patterns of neural activation in the respective brain systems. Consider the perception of a rose, which might produce pat- terns of neural activation in the visual, olfactory, and somatosensory sys- tems. Reaching to touch the rose might produce neural activation in motor and spatial systems. Introspectively, the rose might produce neural activa- tion in the amygdala. Together, these neural states constitute the brain’s immediate response to the rose. At a second level of representation, some of this neural activation may produce conscious states. Certainly, though, much of the underlying neural processing remains unconscious. For exam- ple, people may be unaware of the low-level processing in vision that extracts shape information, or the low-level processing in action that gener- ates an arm movement. Nevertheless, some aspects of these neural states become realized as conscious images in experience. Two points to be noted, then, are (1) that the modality-specific states activated during a specific experience occur at both neural and experiential levels, and (2) the map- ping between them is not one to one.

According to the transduction principle, knowledge about the world, the body, and the mind result from redescribing the types of modality- specific states, illustrated by the example of the rose, with amodal knowl-

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edge structures. Thus, in such accounts, modality-specific states them- selves do not represent knowledge, but the amodal data structures trans- duced from them do. Knowledge about roses does not consist of the modality-specific states that they produce in perception, action, and intro- spection. Instead, knowledge about roses resides in amodal knowledge structures that describe these states.

Examples of Amodal Representations

Most of the dominant theories in cognitive science represent knowledge in this manner. For example, a list representing features of a rose might look like:

Rose

petals pollen thorns fragrance

Although words represent features in the theoretical notation, a key assumption is that amodal symbols actually represent each word in human memory, where there is a close correspondence between words and their amodal counterparts. For lack of a better notation, theorists generally use words to represent the content of amodal representations. Importantly, however, amodal symbols are assumed to constitute the underlying concep- tual content in memory. During the processing of category members, these symbols are transduced from modality-specific states to represent their fea- tures. Later, when people need to communicate something about the cate- gory, they access the words associated with the symbols to do so.

A second important class of amodal theories integrates various types of conceptual relations with features to produce more complex representa- tions (Barsalou & Hale, 1993). Theories in this category include semantic memory models, predicate-calculus representations of knowledge, frames, and production systems. Not only do such theories represent elemental fea- tures of categories, they also represent a variety of important relations between them. Rather than representing pollen and fragrance as indepen- dent features of roses, these theories might add the following relation between them:

Cause (pollen, fragrance)

Analogous to features, the relations between features are represented amodally. Specifically, as the relations arise in modality-specific states,

Embodiment and Emotion Knowledge 37

amodal symbols for them are transduced, which then become bound to amodal symbols for the features that they integrate.

Finally, some (but certainly not all) connectionist theories implement the transduction principle. Feed-forward network theories offer one exam- ple. In feed-forward networks, a first layer of input units performs percep- tual processing, extracting and representing features on a modality. The fea- ture representations are then transduced into a second representation in the network’s hidden units, which is typically interpreted as a conceptual representation. Conceptual representations are amodal for two reasons. First, random weights are set initially on the connections linking the input and hidden units; this step is necessary for implementing learning. The consequence, though, is a significant degree of arbitrariness between input- and hidden-level representations. Second, the activation patterns on the hidden units redescribe the input patterns, such that the hidden unit patterns have a linear relationship to the output units (in contrast, the input patterns have a nonlinear relationship). For these reasons, the hidden units that represent conceptual knowledge are transductions of perceptual states, much like the transductions that underlie more traditional knowledge structures. However, connectionist architectures that use a common set of units to represent perceptual and conceptual states do not exhibit transduction.

Representing Emotion Concepts Amodally

The dominant approach to representing emotion knowledge similarly rests on the transduction principle (Bower, 1981; Johnson-Laird & Oatley, 1989; Ortony, Clore, & Foss, 1987). According to these theories, various types of amodal knowledge structures are transduced from emotional experience to represent emotion concepts. Furthermore, representing knowledge of an emotion in the absence of experiencing it involves activating the appropri- ate amodal representation. Once this representation is active, it describes various domains of information relevant to the emotion, thereby producing inferences about it.

In general, knowledge about emotion falls into three general domains. First, people have knowledge about the situations that elicit emotions. Thus, seeing a smiling baby produces positive affect, whereas seeing a vomiting baby produces negative affect. Second, people have knowledge about the actions that are relevant when particular emotions are experi- enced. Thus, a smiling baby elicits approach responses, whereas a vomiting baby produces avoidance, at least initially. Third, people have knowledge about the introspective states associated with the “hot” component of emo- tions, including both valence and arousal information (e.g., Barrett, Chap- ter 11; Feldman, 1995). Thus, smiling babies produce warm, mildly aroused

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feelings, whereas vomiting babies produce negative, highly aroused feel- ings. Most importantly, amodal theories of emotion assume that amodal knowledge structures represent all three aspects of emotional experience. When people need to consult their knowledge of emotion, they activate and process such structures.

Embodiment in Amodal Theories

According to amodal theories, embodied states are peripheral appendages linked to amodal knowledge structures. Thus a positive emotion, such as hap- piness, might be linked with embodied states for producing the relevant facial expressions, postures, arm movements, vocal expressions, and so forth. Importantly, however, these embodied states do not constitute core emotion knowledge. Instead, each embodied state is linked to an amodal symbol that represents it. The embodied state of smiling, for example, is linked to an amodal symbol for smiling in the concept of happiness. When knowledge about happiness is processed, the amodal symbol for smiling becomes active, thereby carrying the inference that happiness includes smiling. Notably, however, embodied smiling is not necessary to represent the conceptual rela- tion between smiling and happiness. Instead, actual smiling is only a periph- eral state that can either trigger the concept for happiness or can result from its activation, mediated by the amodal symbol for smiling.

Amodal theories similarly peripheralize all other content in emotion concepts. The perception of another person smiling is represented by the same amodal symbol that represents the action of smiling, not by neural states in the visual system as it perceives smiling—which differ from neural states in the motor system that execute smiling. Similarly, the value and arousal of introspective emotional states are represented by amodal sym- bols, not by the neural states that underlie the modality-specific states. Thus, the modality-specific states that occur in emotion during action, per- ception, and introspection are peripheral appendages linked to core amodal symbols that stand for them. When these appendages are experienced, they can ultimately trigger an emotion concept via the intervening amodal sym- bols. When emotion concepts become active, they can ultimately trigger these appendages, again via the amodal symbols that intervene.

Modal Accounts of Embodied Emotion Effects

The Reenactment Principle

Whereas the transduction principle underlies amodal theories of knowl- edge, the reenactment principle underlies modal theories. According to the reenactment principle, the modality-specific states that arise during per-

Embodiment and Emotion Knowledge 39

ception, action, and introspection are partially captured by the brain’s asso- ciation areas (Damasio, 1989). Again consider the neural activation that arises in the brain’s visual, motor, olfactory, and affective systems when interacting with a rose. While these states are active, association areas par- tially capture them, storing them away for future use. Conjunctive neurons in association areas intercorrelate the active neurons both within and between modalities, such that a partial record of the brain’s processing state becomes established as a memory. Later, when information about the rose is needed, these conjunctive neurons attempt to reactivate the pattern of neural states across the relevant modalities. As a result, the neural state of processing is reenacted to represent the modality-specific states that the brain was in while processing the rose. By no means is the reenactment complete or fully accurate. Indeed, partial reenactment is almost certainly the norm, along with various types of distortion that could reflect base rates, background theories, etc. In this view, no amodal symbols are trans- duced to represent experiences of the world, body, and mind. Instead, reenactments of original processing states perform this representational work. For more detailed accounts of this theory, see Barsalou (1999, 2003a, 2003b, in press), and Simmons and Barsalou (2003).

Representing Emotion Concepts Modally

According to this view, modality-specific states represent the content of concepts, including those for emotion. Consider the three domains of emo- tion knowledge mentioned earlier: triggering situations, resultant actions, and introspective states. Reenactments of modality-specific states repre- sent the conceptual content in these domains, not amodal symbols. Thus reenactments of perceiving smiles visually on other people’s faces belong to the situational knowledge that triggers happiness, as do the motor and somatosensory experiences of smiling oneself. Similarly, reenactments of valence and arousal states represent these introspective aspects of emotion concepts, not amodal symbols representing them (for a similar view, see Barrett, Chapter 11).

In this view, knowledge of the emotion is delivered via actual emo- tional states, some being conscious and some unconscious; knowledge of an emotion concept is not seen as a detached description of the respective emotion. Although these states may not constitute full-blown emotions, they may typically contain enough information about the original states to function as representations of them conceptually. Moreover, these par- tial reenactments constitute the core knowledge of emotional concepts. Embodied states are not merely peripheral events that trigger emotion concepts or that result from the activation of emotion concepts. Instead, embodied states represent the core conceptual content of an emotion.

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Explaining Embodiment Effects in Emotion Research

As we saw earlier, embodiment enters ubiquitously into the processing of emotion. Viewing embodied states as the core elements of emotion con- cepts provides a natural account of these findings. When an embodied emotional response results from perceiving a social stimulus, this embodi- ment plays a central role in representing the emotional concept that becomes active to interpret the stimulus. For example, when the percep- tion of a smiling baby activates embodied responses for smiling, approach, and positive valence in the self, these embodied states represent the emo- tional and affective concepts that become active, such as happiness and lik- ing. Embodied states represent these concepts directly, rather than trigger- ing amodal symbols that stand in for them. A similar account explains the embodiment effects reviewed earlier for visual imagery. As a person is imagining a social stimulus, the emotional categories used to interpret it are represented by the embodied states that become active.

A similar account explains the roles of embodiment in triggering emo- tion concepts and in their subsequent effects on cognitive processing. When a person’s body enters into a particular state, this constitutes a retrieval cue of conceptual knowledge. Because modality-specific states represent knowledge, an active modality-specific state in the body or mind triggers concepts that contain the state as elements of their representation, via the encoding specificity principle (e.g., Tulving & Thomson, 1973). As matches occur, the emotion concept that best fits all current retrieval and contextual cues becomes active and dominates the retrieval com- petition. Furthermore, once an emotion concept dominates, it reenacts other modality-specific aspects of its content on other relevant modalities, thereby producing at least a partial semblance of the emotion. In turn, other cognitive processes, such as categorization, evaluation, and memory, are affected. As an embodied state triggers an emotion concept, and as the emotion becomes active, it biases other cognitive operations toward states consistent with the emotion.

As this brief description illustrates, the embodied approach to emotion offers a plausible and intuitive account of embodiment effects. It is also a productive approach that makes specific predictions, several of which we outline here.

Deep versus Shallow Tasks

The modal account described here predicts that bodily aspects of emotion concepts are simulated only when necessary; that is, in deep, but not in shallow, conceptual tasks. A deep task requires recourse to meaning,

Embodiment and Emotion Knowledge 41

whereas a shallow task can be accomplished by simple associative means. According to a strict reading of the amodal models (e.g., Bower, 1981), there should be no simulation—that is, physiological manifestation of the emotion—in shallow or deep conceptual tasks because individuals can sim- ply “read off” amodal feature lists for both tasks. A generous interpretation of an amodal model might yield the prediction that physiological manifesta- tions will occur in both deep- and shallow-feature generation tasks because thinking about the emotion concept automatically activates the highly asso- ciated nodes that represent the physiological aspects of the emotion. How- ever, a selective prediction that physiological manifestations of emotion are evoked only in deep, but not in shallow, tasks cannot easily be derived from an amodal model. This is because, if anything, physiological nodes are most directly and closely associated with emotion and should be the first to be activated during the use of the emotion concept in a deep or shallow way.

Partial Embodiment

The simulation account predicts that only the needed parts of the bodily representation are simulated (i.e., simulations occur only in the modality required to perform the task). The notion of partial simulation is illustrated by results of recent functional magnetic resonance imaging (fMRI) studies that found a selective activation of relevant parts of the sensory cortex when property verification tasks were performed in different modalities (Kan, Barsalou, Solomon, Minor, & Thompson-Schill, 2003; Kellenbach, Brett, & Patterson, 2001). Again, a strict reading of amodal models does not generate any embodiment predictions, because individuals can simply read off abstract features of emotion concepts. A more generous reading of amodal models would yield the prediction that the processing of emotion concepts should nonspecifically activate the associated sensory basis via top-down links.

Impairment/Facilitation of Sensory–Motor Processing

Finally, the simulation account predicts that manipulations of sensory– motor processing have conceptual consequences. This prediction is sup- ported by studies showing that categorization impairments can result from damage to neural systems representing sensory characteristics of the cate- gory (Farah, 1994; Simmons & Barsalou, 2003). Further, several studies show that recognition and categorization of emotion can be impaired by damage to, or blocking of the mechanisms of, somatosensory feedback. Associative models predict no effects (or, at most, nonspecific effects) of such bottom-up manipulations. In short, amodal accounts see embodiment

42 COGNITION AND EMOTION

as irrelevant for conceptual processing. At best, they see it as a by-product of associations, not as a constitutive element of conceptual processing.

In sum, if these predictions were tested and evidence found in favor of modal models, this evidence would tell us much about the experience and reexperience of emotional states: how individuals ground emotion con- cepts, how emotion processes can be manipulated in the laboratory (or not), and how emotions and feelings can and cannot be regulated by the individ- ual.

CONSCIOUS AND UNCONSCIOUS STATES OF EMOTION

The perspective presented here has a number of implications for conceptu- alizing emotion in general and defining its conscious and unconscious pro- cesses. First, consistent with William James, we have proposed that em- bodied states constitute the fundamental way of representing emotional information. For example, when we see a smiling face, we smile, and this response allows us to know the stimulus (see also Atkinson & Adolphs, Chapter 7; de Gelder, Chapter 6). Although James was criticized for not being able to specify why or when the perception of a given event or object would instigate the bodily state of an emotion in the first place, this is a less worrisome criticism now because good support for the notion of inherent affective “programs” (Tomkins, 1962), or bodily responding to signal stim- uli, has been reported (e.g., Dimberg, 1986, 1990; Dimberg, Hansson, & Thunberg, 1989); although for a critical view, see Barrett, Chapter 11). Thus, as we have shown in our present review of the relevant research, the perception of certain stimuli, including—and perhaps especially— emotional expressions of other people, automatically produces specific bodily states in the perceiver. It is not necessary for such embodied states of emotion to be conscious, as in imitation for example, or even be available to consciousness. The states may be too subtle to gain consciousness, even if attention is directed to them. And potentially conscious embodiments may not become conscious because competing attentional demands simply win out (e.g., Neumann & Strack, 2000). One interesting implication of the notion of unconscious embodiment as stimulus encoding is that individual variability should be relatively low, within obvious morphological con- straints.

When conscious attention is directed to the bodily state, and the bodily state is intense enough be consciously detected, we would suggest, consistent with James, that the individual experiences a feeling state. In the attention to, and interpretation of, a feeling state (e.g., in the service of self-

Embodiment and Emotion Knowledge 43

report), variability and individual differences, including cultural rules of interpretation, can intervene. In an example of such variability, Laird and his colleagues (e.g., Laird & Crosby, 1974) documented stable individual differences in the extent to which expressive behavior influences feeling states per se (e.g., Laird & Bresler, 1992). Laird notes:

The differences in impact of behavior seem to reflect the type of cues on which individuals base their emotional experience. People who attend to their own bodily cues, their appearance, and their instrumental actions are more responsive to so-called “personal” or “self-produced” cues. In contrast, indi- viduals who primarily focus on interpretations of the situation and infer responses from what is appropriate in their situation, are responsive to “situa- tional” cues. (Schnall & Laird, 2003, p. 789; see also Feldman, 1995; Barrett, Chapter 11, for further examples and discussion)

Thus, although unconscious embodiments of incoming stimuli may be quite stable and even universal, as noted, subsequent conscious simulations should be quite variable in content because they rely on the represented feeling states; that is, conscious simulations reenact the biases introduced by directing attention to the bodily state and representing it in conscious- ness as a feeling state. The content of concepts of anger, joy, fear, and so forth, will vary across individuals and situations to the extent that the situa- tion determines selective attention to parts of a represented feeling state or experience and thus helps choose the simulation to be performed.

Distinguishing the bodily state of emotion and the feeling state of emotion is useful in the interpretation of a number of findings that would appear to be inconsistent with the embodiment approach. For example, if biases and individual differences intervene in defining the conscious feel- ing state, and if the bodily states can occur outside of consciousness, then there is no reason why self-report of feeling states should be highly corre- lated with bodily states; and, indeed, they are often not correlated (see Barrett, Chapter 11).

Relatedly, in a series of studies, Rimé, Phillipot, and their colleagues examined people’s knowledge about the bodily states associated with dif- ferent emotions, which they call schemata of peripheral changes in emotion (e.g., Rimé, Philippot, & Cisamolo, 1990). Results showed that such sche- mata, or sets of beliefs, were highly consensual and highly accessible. That is, individuals were in high agreement about the peripheral changes that occur during different emotions. Several studies were then conducted to evaluate the relation between these schemata and actual peripheral changes during an emotional state produced by watching emotionally evo- cative films. Some experimental participants reported their feelings and

44 COGNITION AND EMOTION

peripheral changes during the emotional films, and another set of partici- pants described the contents of their schemata of peripheral changes for the emotions that were said to be evoked by the film (Phillipot, 1997). These two sets of reports were highly correlated, such that reported peripheral changes by one set of individuals were the same as those believed to be produced in the emotional states of interest by another set of individuals. However, further work showed that the reports of peripheral changes by participants who watched the films were less highly correlated with actual peripheral changes. Thus the authors concluded that people tend to report their beliefs about embodied states of emotion rather than an accurate readout of those states. If we separate the notion of bodily states of emotions (as sometimes unconscious) and feeling states (as always the result of conscious attention to the bodily states), we can see that such biases are the norm. The fact that embodied states constitute emotional information processing does not mean that simulations are invariant repro- ductions of those states.

CONCLUSION

We have reviewed a number of studies that suggest that emotion knowl- edge is grounded in the somatosensory and motor states to which emotions give rise. We have suggested that the implication of this work is that per- ceiving someone else’s emotion, having an emotional response or feeling a state oneself, and using emotion knowledge in conceptual tasks all rely on the same fundamental processes. As we then demonstrated, recent theories of embodied cognition, which rely on the notions of modal representation of knowledge and the principle of reenactment, account for this accumu- lated knowledge quite well. Further, such models suggest much about what happens when people process emotional information, and can help gener- ate testable hypotheses about conscious and unconscious states of emotion.

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SCtOudGiNesIoTfItOhNe HAuNmDanEAMmOyTgIdOalNa

CHAPTER 3

The Interaction of Emotion and Cognition

Insights from Studies of the Human Amygdala

ELIZABETH A. PHELPS

Initial investigations of human affective neuroscience emphasized the iden- tification of neural structures that seem to be specialized for emotion pro- cessing (Damasio, 1994; LeDoux, 1996). At the same time, research in cog- nitive neuroscience explored other brain systems identified as primarily important for cognitive functions (Gazzaniga, Ivry, & Mangun, 1998). These initial efforts paralleled the traditional division between psychological study of emotion and cognition. The cognitive revolution and the develop- ment of a subdiscipline of psychology focused on understanding cognition relegated the study of emotion to other domains (Anderson, 1999; Neisser, 1976), particularly social and clinical psychology. Although there have been debates over the years as to the appropriate role of emotion in the study of cognition (Lazarus, 1981; Zajonc, 1980), until recently both psychological and neuroscience research on cognitive function usually failed to consider a role for emotion.

As neuroscience research in human affective processes progresses, however, it has become increasingly apparent that the neural systems of emotion interact extensively with those underlying cognitive processes (see

51

52 COGNITION AND EMOTION

1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

In this chapter, I use the term emotion (in most cases) when referring to the reaction to stimuli that elicit a physiological arousal response, usually due to their aversive nature. The amygdala has primarily been shown to play a role in processing stimuli that are arousing; this role has been shown to extend to arousal in response to positive stimuli (e.g., Anderson, Christoff, Panitz, DeRosa, & Gabrieli, 2002), although most studies use negative stimuli. In addi- tion, the amygdala has been shown to process stimuli that convey fear or threat- related signals (e.g., pictures of fear faces), even if these stimuli do not elicit a detectable physiological response. Although the amygdala is often broadly thought of as a critical structure in emotion processing, there is no clear evi- dence that it plays an important role in other key components of emotion, such as the subjective experience of emotional states (Anderson & Phelps, 2002).

2. Define your terms: conscious, unconscious, awarness. Or say why you do not use these terms.

I use the term awareness throughout my chapter. The primary means used to assess awareness in the studies I report is verbal report; that is, do subjects indicate awareness of an event.

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

I address the conscious–unconcious distinction primarily by referring to indirect (or implicit) and direct (or explicit) means of expression. I address the interac- tion of the two by providing examples of how an acquired conscious awareness and explicit strategies can influence the indirect expression of emotion (primar- ily through physiological measures of arousal). I also indicate how the emotional qualities of a event can influence the likelihood that the subject will be aware

of that event, either during initial stimulus processing or later, during recollec- tion.

also Gray, Schaefer, Braver, & Most, Chapter 4). These interactions have prompted a reconsideration of the appropriate role of emotion in efforts to understand cognition (Gazzaniga, Ivry, & Mangun, 2002). In this chapter, I review recent insights from affective neuroscience into the interaction of emotion and cognition. I focus on the role of the human amygdala, a small structure in the medial temporal lobe thought to be specialized for emo- tion, and its interaction with processes of cognition and awareness.

Studies of the Human Amygdala 53

INDEPENDENT SYSTEMS FOR EMOTION AND COGNITION

The amygdala is an almond-shaped structure in the medial temporal lobe, located just anterior to the hippocampal complex. It was first identified as a brain structure potentially important for emotion when Klüver and Bucy (1939) observed the behavior of monkeys after medial temporal lobe lesions, which included the amygdala, hippocampus, and surrounding cor- tices. These monkeys displayed a pattern of behavior, called “psychic blind- ness,” marked by odd emotional responses, such as approaching objects that would normally elicit a fear response (e.g., snakes). Approximately 20 years later, Weiskrantz (1956) identified the amygdala as the medial tempo- ral lobe structure whose damage is directly responsible for psychic blind- ness. Since that time, it has been widely acknowledged that the amygdala is a brain region whose primary function is linked to emotion.

More recent investigations in nonhuman animals have explored the precise role of the amygdala in emotion processing. These studies have mostly investigated the role of the amygdala in emotional learning, using fear conditioning methods, as a model paradigm. In fear conditioning method, a neutral stimulus (e.g., a tone), the conditioned stimulus (CS) acquires emotional properties by being paired with an aversive event (e.g., a foot shock), the unconditioned stimulus (US). After a few pairings, the animal displays a range of fear responses, such as changes in heart rate, blood pressure, startle reflexes, and freezing, to the previously neutral CS. These learned fear responses are conditioned responses (CRs). Using fear conditioning as a model paradigm, researchers have mapped the pathways of fear learning from stimulus input to response output (e.g., Davis, 2000; Kapp, Whalen, Supple, & Pascoe, 1992; LeDoux, 1996). These elegant ani- mal models have identified the amygdala as a critical structure in the acqui- sition, storage, and expression of fear learning (see LeDoux, 2002, for a review).

Some of the initial efforts to explore the neural systems of emotion pro- cessing in the human brain were inspired by these animal models. Findings from studies of fear conditioning in humans are largely consistent with results from other species. In a typical paradigm in humans, a neutral stim- ulus such as a blue square (the CS) is paired with a mild shock to the wrist (the US). After a few pairings the blue square itself elicits physiologi- cal indications of fear (the CR), such as an increased skin conductance response (SCR; a measure of mild sweating that occurs with autonomic nervous system arousal). Using functional magnetic resonance imaging (fMRI), activation of the amygdala has been observed during fear condi- tioning (LaBar, Gatenby, Gore, Le Doux, & Phelps, 1998; Buchel, Moris,

54 COGNITION AND EMOTION

Dolan, & Friston, 1998). The strength of this activation was correlated with the strength of the CR, as assessed by the SCR (LaBar et al., 1998). In addi- tion, patients with amygdala damage fail to show any evidence of a CR, even though they show a normal response to the US, indicating that the amygdala is critical for the expression of learned fear responses, not the physiological expression of fear itself (Bechara et al., 1995: LaBar, Le Doux, Spencer, & Phelps, 1995).

Although the findings from fear conditioning in humans are consistent with animal models that identify the amygdala as a critical structure in the acquisition and expression of fear learning, there are some differences between humans and nonhumans with amygdala damage. Even though the human amygdala is critical for the expression of the CR, patients with amygdala damage do not display odd emotional responses similar to those observed by Klüver and Bucy (1939) in monkeys (Anderson & Phelps, 2002). In fact, the famous amnesic patient H.M. had a lesion similar to that of the Klüver–Bucy monkeys; however, the effect he experienced was described as primarily a long-term memory deficit with relatively normal social and emotional responses (Milner, Corkin, & Teuber, 1968). A hint of a possible reason for this difference in emotional behavior between humans and nonhumans with amygdala damage came from the initial studies on fear conditioning in humans. These patients with amygdala lesions, who failed to demonstrate any evidence of a CR, as assessed with physiological measures, showed an intact awareness and understanding of the events of fear conditioning (LaBar et al., 1995; Bechara et al., 1995).

For example, patient S.P., who suffers from bilateral damage to the amygdala, was given a fear conditioning paradigm in which a blue square was paired with a mild shock to the wrist. Unlike normal control subjects, she failed to demonstrate a CR to the blue square, as assessed with SCR. She was shown the data indicating a deficit in the normal expression of a CR and asked to comment on what she believed was the significance of these results.

“I knew that there was an anticipation that the blue square, at some particular point in time, would bring on one of the volt shocks. But even though I knew that, and I knew that from the very beginning, except for the very first one where I was surprised. That was my response—I knew it was going to hap- pen. I expected that it was going to happen. So I learned from the very begin- ning that it was going to happen: blue and shock. And it happened. I turned out to be right, it happened!” (in Phelps, 2002, p. 559)

As S.P. indicates in her description of fear conditioning, even though she failed to demonstrate a CR, she had a very good awareness and understand-

Studies of the Human Amygdala 55

ing of the emotional significance of the CS (i.e., the blue square). This awareness most likely would have been sufficient to guide her actions had she been given the option of avoiding the blue square. Studies in patients with hippocampal damage, whose amygdala is intact, show the opposite pattern. That is, they are unable to explicitly report the events of fear condi- tioning, but they show a normal CR, as assessed physiologically with SCR (Bechara et al., 1995). This double dissociation demonstrates the influence of multiple memory systems—an episodic or declarative memory system, dependent on the hippocampal complex, that underlies an awareness and understanding of learned events, and an emotional learning system, depen- dent on the amygdala, that is necessary for learned implicit, physiological expressions of emotional experience. It is possible that patients with amygdala damage display relatively normal emotional responses by relying on episodic representations that result in a cognitive awareness and under- standing of the emotional significance of events.

These initial studies of fear conditioning following amygdala damage in humans suggest that emotional and cognitive learning systems are repre- sented independently in the human brain. The findings appear to support the tradition of investigating cognitive processes independent of emotion’s influence. However, even though this initial research on the human amyg- dala indicates an independence of emotion and cognition, more recent findings highlight the complex interactions between the neural systems of emotion and those of cognition (see also Gray et al., Chapter 4). In the remainder of this chapter, I review recent research suggesting that even though an amygdala/emotion system can operate independently of cogni- tion and awareness, there are also extensive interactions. Cognitive aware- ness can influence amygdala function and emotional expression. At the same time, emotion and amygdala processing can influence awareness and a range of cognitive functions. These interactions are bidirectional and sug- gest a complex relationship between emotion and cognition.

THE INFLUENCE OF COGNITION ON EMOTION

The performance of patients with amygdala damage during fear condition- ing shows that the amygdala is not necessary for an awareness and under- standing of the emotional significance of a CS (LaBar et al., 1995; Bechara, et al., 1995; Phelps, 2002). These patients, who have an intact hippocam- pus, are able to remember and explicitly report that the CS predicts the aversive shock. Fear conditioning in which a neutral CS is paired with an aversive US, resulting in an aversive experience (i.e., pain or discomfort), is only one of the means that can be used to learn about the emotional signifi-

56 COGNITION AND EMOTION

cance of a stimulus. The emotional properties of a stimulus can also be con- veyed through verbal instruction without any direct aversive consequence. This type of symbolic communication is typical in everyday human experi- ence (e.g., see Smith & Neumann, Chapter 12). For example, many com- mon fears, such as a fear of flying, are not usually the result of direct experi- ence but rather are acquired through hearing about potential negative consequences of flying.

Given that patients with amygdala damage are able to remember and verbally report the events of fear conditioning, it is unlikely the amygdala is necessary to acquire an episodic representation and awareness of the emo- tional properties of a stimulus that are conveyed through language. It is unclear if this type of symbolic communication of emotion requires the amygdala at all. This question was addressed using a paradigm of “instructed fear.” As in the fear conditioning paradigm described earlier, a blue square is paired with the possibility of a mild shock to the wrist. How- ever, with instructed fear, subjects are simply told a blue square (the threat stimulus) is potentially linked to a shock. Subjects never actually receive a shock.

Previous studies have shown that instructed fear results in a similar physiological expression of fear (i.e., SCR) as fear conditioning (Hugdahl & Öhman, 1977). Simply being told a stimulus predicts a mild shock is enough to elicit a fear response to that stimulus. fMRI was used to deter- mine if this cognitive, episodic representation of the aversive properties of a stimulus could influence the amygdala. Significant activation of the left amygdala was observed in response to presentation of a blue square ver- bally linked to the possibility of a mild shock (i.e., the threat stimulus) com- pared to a yellow square that was not linked to threat (i.e., the safe stimulus). The strength of the amygdala response to the threat stimulus predicted the magnitude of the physiological expression of fear, as assessed with SCR (Phelps et al., 2001). These results are similar to those observed with fear conditioning in which amygdala activation to a CS predicted the strength of the CR (LaBar et al., 1998).

The finding that instructed fear leads to amygdala activation suggests that an episodic representation and awareness of the emotional significance of the threat stimulus can influence the amygdala. However, these brain- imaging results do not indicate if the amygdala plays any critical role in the expression of instructed fear. To explore the precise role of the amygdala, patients suffering from unilateral (right and left) and bilateral amygdala damage participated in the instructed fear paradigm. Although all the sub- jects remembered and verbally reported that the blue square predicted the possibility of shock, patients with left and bilateral amygdala damage failed to show any physiological expression of fear to the threat stimulus. Patients

Studies of the Human Amygdala 57

with right amygdala damage and normal controls demonstrated physiologi- cal responses consistent with fear to the blue square (Funayama, Grillon, Davis, & Phelps, 2001). These results indicate that awareness of the aver- sive properties of a stimulus, acquired symbolically without direct aversive experience, can influence the amygdala (primarily, the left amygdala), which in turn mediates the physiological expression of fear.

The instructed fear studies demonstrate one method by which cogni- tion and awareness can influence amygdala function. In everyday human life, many of our fears are the result of our interpretation of the significance of events. Whether a specific threat is real and imminent or unrealistic and unlikely, humans can use imagination and interpretation to induce a fear response. The instructed fear studies indicate that symbolically repre- sented fears that are imagined and anticipated, but never experienced, rely on similar neural mechanisms for expression as fears acquired through direct aversive experience.

With instructed fear, cognitive interpretation and imagination result in a fear response. It is also possible to use cognitive control and interpreta- tion to diminish a fear response. This is one of the principles guiding cogni- tive therapies for psychological disorders. For instance, in anxiety disorders a fear response, which may be appropriate in some situations, is expressed in inappropriate or maladaptive circumstances. Cognitive therapy focuses on changing the thought patterns related to the generation of a maladaptive anxiety response in an effort to change this behavior. This type of emotion regulation is important not only in controlling unwanted fear responses but also normal social interaction and emotional function. If the amygdala plays a role in the expression of fears that are learned symbolically and depend on awareness and interpretation for expression, then it is possible the amygdala response is also altered by cognitive strategies that diminish a fear response.

In an effort to examine the effect of emotion regulation strategies on the amygdala, fMRI was used during a study of reappraisal, an emotion regulation technique in which the significance of a potentially ambiguous event is interpreted, or reappraised, to alter its emotional connotation. For instance, if subjects were shown a picture of women crying outside of a church, a possible interpretation would be that the women are at a funeral for a loved one. However, if subjects were instructed to reappraise the scene so that the emotional reaction is less negative, they might imagine instead that the women are at a wedding and their tears are joyful. Previous research has shown that this type of reappraisal instruction can significantly alter the emotional state of the subjects (Gross, 2002). A study by Ochsner, Bunge, Gross, and Gabrielli (2002) asked subjects to reappraise the emo- tional significance of negative scenes during fMRI. Reappraisal not only

58 COGNITION AND EMOTION

significantly diminished the rating of negative affect for the scenes but also reduced the amygdala response, relative to scenes they were instructed to attend to without reappraising them (see also Schaffer, Jackson, Davidson, Kimbers, & Thompson-Schill, 2002). In addition to the amygdala, a region of the left dorsolateral prefrontal cortex (DLPFC) showed greater activa- tion on reappraise versus attend trials. This DLPFC region is similar to that observed during executive control tasks in working memory (Smith & Jonides, 1999), consistent with the notion that reappraisal engages cogni- tive control mechanisms. The amygdala and DLPFC were inversely corre- lated across subjects. That is, those subjects who showed greater DLPFC engagement during reappraisal also showed a greater reduction in amyg- dala activation to the negative scenes.

More recently, a study by Delgado and colleagues (2004) instructed subjects to use an active emotion regulation strategy to diminish condi- tioned fear responses. The emotion regulation strategy diminished the physiological expression of the CR as well as amygdala activation to the CS. Consistent with Ochsner et al. (2002), a similar pattern of activation was observed in the DLPFC (i.e., greater activation to reappraise vs. attend). These results demonstrate that explicit cognitive strategies and control mechanisms can alter the amygdala response during tasks that range from viewing negative scenes to fear conditioning.

The studies of instructed fear and emotion regulation indicate that even if cognitive awareness and understanding of the emotional properties of a CS are not necessary for conditioned fear, there are a number of ways that cognition and awareness can influence the amygdala and emotional responses. Symbolic communication and awareness of the potentially aver- sive properties of an event can result in the expression of an emotional response that is dependent on the amygdala. In addition, cognitive control mechanisms can be used to help execute emotion regulation strategies, which can diminish an amygdala response to an emotional scene or a CS. These findings suggest that the independence of the amygdala function and cognitive awareness observed in fear conditioning may not reflect the importance of cognitive mechanisms of emotional learning or the complex- ity of emotional expressions that are typical in everyday human experience.

THE INFLUENCE OF EMOTION ON COGNITION

The influence of cognitive mechanisms on amygdala function indicates that this subcortical structure can be influenced by symbolic representations, cognitive control, and conscious interpretation. However, the relation between the amygdala and cognitive awareness also goes the other way.

Studies of the Human Amygdala 59

Emotion, through the amygdala, can influence cognitive mechanisms and conscious awareness of events and stimuli. Two primary means have been identified by which the amygdala alters cognitive awareness: (1) The amygdala modulates long-term retention of memory, so that over time we are more likely to be aware of emotional events; and (2) the amygdala influ- ences attention and perception (Lundqvist & Öhman, Chapter 5; de Gelder, Chapter 6; Atkinson & Adolphs, Chapter 7) so that emotional events are more likely to reach awareness.

Memories for emotional events seem to have a vividness and persis- tence that other memories lack. It has been suggested that one adaptive function of emotion is to enhance the storage of episodic memories so that events that are linked to an emotional response, and are potentially more important for survival, are not forgotten (McGaugh, 2000). It is widely acknowledged that emotion enhances episodic memory for events (Christianson, 1992). The result is that over time, we are more likely to remember and be aware of emotional events than neutral events. This mod- ulation of long-term memory and awareness for emotional events is, in part, due to the amygdala’s modulation of the storage of hippocampal-dependent memories.

The hippocampal complex is necessary for initial encoding of episodic or declarative memory. After encoding, there is a period of time during which the disruption of the hippocampus impairs memory retention, sug- gesting that the hippocampal complex is also critical for the long-term stor- age, or consolidation, of memories. Eventually, however, episodic memo- ries can be retrieved independent of the hippocampal function, at which point they are thought to be consolidated (see Squire, Clark, & Bayley, 2004, for a review). In an elegant series of studies in rats, McGaugh and colleagues demonstrated that the release of stress hormones with arousal engages a mechanism by which the amygdala modulates the consolidation, or storage, of hippocampal-dependent memories (see McGaugh, 2000, for a review). The amygdala is not necessary for the normal formation or storage of episodic memories; it simply influences how well these memories are stored when there is an emotional arousal reaction to the event.

A series of lesion, phamacological, and brain-imaging studies in humans supports these animal models, suggesting that the amygdala plays a role in the enhanced retention of hippocampal-dependent episodic memory for emotional events. For example, it has been demonstrated that patients with amygdala damage, in contrast to normal controls, fail to show enhanced memory for arousing events (Cahill, Babinsky, Markowitsch, & McGaugh, 1995). In normal control subjects, the memory advantage for emotional events is more pronounced over time, indicating that emotional events are not forgotten at the same rate as neutral events (Kleinsmith & Kaplan,

60 COGNITION AND EMOTION

1963), consistent with enhanced consolidation or storage of memories with arousal. Patients with amygdala damage, unlike normal controls, show simi- lar forgetting curves for arousing and neutral stimuli (LaBar & Phelps, 1998). When normal control subjects are given beta-blockers, which block the action of stress hormones on the amygdala, these subjects perform simi- larly to patients with amygdala lesions in that they no longer demonstrate a memory advantage for arousing stimuli after a delay (Cahill, Prins, Weber, & McGaugh, 1994). Finally, a number of brain-imaging studies have shown that amygdala activation during the encoding of emotionally arousing events is predictive of the ability to retrieve these events at a later time (Cahill et al., 1996; Canli, Zhao, Brewer, Gabrielli, & Cahill, 2000; Hamann, Ely, Grafton, & Kilts, 1999). These findings, using a range of techniques in humans, support animal models that outline a mechanism by which the amygdala enhances the storage or retention of emotional events with arousal.

By modulating the storage or retention of events with emotion, the amygdala alters the stimuli that are available to awareness over time. Most events encountered in our daily lives are forgotten. For instance, it would be difficult for most people to accurately recollect what they had for dinner a week ago, unless this dinner was significant for some reason. Emotion helps ensure that events are not forgotten. Although there may be other means by which emotion enhances episodic memory that are not amygdala dependent (see Phelps et al., 1998), a wide range of research suggests that the human amygdala is at least partially responsible for the enhanced long- term retention and awareness of events that elicit an arousal response.

In addition to modulating the long-term retention and storage of emo- tional events, the amygdala can also affect memory by altering the initial stage of memory processing—encoding. Findings from a number of studies sug- gest that emotion can change the processing of stimuli when they are first encountered by influencing attention. Emotion has been shown to both cap- ture and facilitate attention. Attention paradigms that require the processing of nonemotional aspects of a stimulus, such as the emotional version of the Stroop task in which subjects report the color of an emotional word (Pratto & John, 1991), often report that emotion impairs performance by making it diffi- cult to disengage from the emotional stimulus (Fox, Russo, Bowles, & Dutton, 2001). However, other studies have shown that in situations with limited attentional resources, emotional stimuli are more likely to reach awareness, suggesting that emotion can also facilitate attention. A classic example of the facilitation of attention with emotion is the cocktail party effect. It is possible to selectively inhibit the processing of irrelevant stimuli (e.g., conversations among others at a cocktail party) unless an emotionally relevant stimulus (e.g., your name) is presented. In this case, the attentional bottleneck is selec-

Studies of the Human Amygdala 61

tively reduced to allow processing and awareness of an emotionally signifi- cant event (see Lachman, Rachman, & Butterfield, 1979, for a review). It has been suggested that this facilitation of attention with emotion may be depen- dent on the amygdala (Whalen, 1998).

To assess if the human amygdala plays a role in the enhanced aware- ness of emotional events in situations with limited attentional resources, the performance of patients with amygdala damage was examined using the attentional blink paradigm (Anderson & Phelps, 2001). This is a rapid serial visual presentation (RSVP) paradigm in which a series of words is pre- sented rapidly. On each trial, 15 words are presented at a rate of approxi- mately 100 milliseconds per word. At this rate, it is very difficult for sub- jects to report the words because they go by so quickly. However, if subjects are instructed to ignore most of the words and focus only on two of the 15 words that are presented in a different-colored ink (i.e., green vs. black ink), they are often able to selectively attend to these words and report them at the end of each trial—although the ability to report the sec- ond word (Target 2) presented in green ink is somewhat dependent on the location of this word in the list. When Target 2 is presented several words after the first target word (Target 1), subjects were usually able to report it. However, if Target 2 is presented only two or three words after Target 1 (called the early lag period), the ability to identify and report Target 2 is diminished. This is the classic attentional blink effect (Chun & Potter, 1995). Noticing and encoding Target 1 creates a temporary refractory period during which it is difficult to notice and encode Target 2. In other words, it is as if attention “blinked.”

Using this attentional blink paradigm, Anderson and Phelps (2001) showed that emotion enhanced the likelihood that Target 2 would be detected in the early lag period. When Target 2 was an emotionally arous- ing word, normal subjects were much less likely to miss it when it was pre- sented in the early lag period. In other words, emotion attenuated the attentional blink effect, indicating a facilitation of attention with emotion. Patients with amygdala damage, however, failed to show the normal attenu- ation of the attentional blink with emotion. Unlike normal controls, these patients were equally likely to miss Target 2 presented in the early lag period when it was emotion or neutral. These results demonstrate that the amygdala plays a critical role in the facilitation of attention with emotion.

The mechanism by which the amygdala might facilitate attention and awareness for emotional events has been suggested by brain-imaging stud- ies in humans and anatomical studies in nonhuman primates. A number of brain-imaging studies have demonstrated enhanced activation of visual processing regions in response to emotional stimuli (Anderson et al., 2003; Kosslyn et al., 1996; Morris, Buchel, & Dolan, 2001; Vuilleumier, Armony,

62 COGNITION AND EMOTION

Driver, & Dolan, 2001). Some of these studies have reported that this mod- ulation of activation in visual regions with emotion is correlated with the amygdala response (Morris et al., 2001) or linked to amygdala function (Vuilleumier et al., 2004). These findings support proposed models that suggest that the amygdala modulates the sensitivity of perceptual process- ing with emotion (Kapp, Supple, & Whalen, 1994; Weinberger, 1995; Whalen, 1998).

Anatomical studies in primates have shown that the amygdala has reciprocal connections with cortical visual areas (Amaral, Behniea, & Kelly, 2003). The amygdala has been shown to respond to the emotional signifi- cance of an event quickly and prior to awareness (LeDoux, 1996; Whalen et al., 1998). It is hypothesized that this early amygdala response may result in feedback to visual-processing regions, which in turn enhances further per- ceptual processing. A number of cortical visual-processing regions has been shown to be enhanced with emotion and modulated by amygdala function, including early visual regions such as the extrastriate cortex (Morris et al., 2001, Vuilleumier et al., 2004). Consistent with the hypothesis that emotion influences even the earliest stages of perception, a recent study found that emotion enhances contrast sensitivity (Ling, Phelps, Holmes, & Carrasco, 2004), a primary visual function known to be coded in the early visual cor- tex. Although there is no direct evidence that the human amygdala alters a specific perceptual process, the findings from a range of imaging, anatomi- cal, and behavioral studies are consistent with the hypothesis that the facili- tation of attention with emotion may be the result of the amygdala’s modu- lation of perception.

The amygdala’s influence on attention and perception suggests that the initial processing of emotional stimuli is enhanced relative to neu- tral stimuli. This enhanced awareness for emotional stimuli with limited attentional resources may also lead to greater memory encoding, resulting in both greater immediate and later awareness with emotion. By altering memory storage, attention, and perception with emotion, the amygdala helps to ensure that emotionally significant events receive priority in cogni- tive processing and awareness.

CONCLUSION

In this chapter I have outlined how some of the neural mechanisms of emo- tion and cognition, which can operate independently, also have complex interactions. A cognitive awareness of the emotional significance of events and conscious application of emotion regulation strategies can influence amygdala function and emotional expression, suggesting two means by

Studies of the Human Amygdala 63

which cognition alters emotion. In addition, the emotion, via the amygdala, influences cognition by mediating the long-term retention and awareness of emotional events, as well as immediate stimulus processing, by modulat- ing attention and perception. Although it is possible to study the behavioral and neural mechanisms of emotion and cognition independently, this research suggests that independent investigations of emotion and cognition may result in an incomplete and inaccurate view of normal emotion and cognitive processes. The neural systems of emotion and cognition are both independent and interdependent. A comprehensive understanding of either emotion or cognition requires a consideration of the complex inter- actions between the two.

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ACfOfeGctNaInTdIOCNognAiNtivDe ECMonOtrTolIODNilemmas

CHAPTER 4

Affect and the Resolution
of Cognitive Control Dilemmas

JEREMY R. GRAY ALEXANDRE SCHAEFER TODD S. BRAVER STEVEN B. MOST

Many people find the topic of emotion–cognition interactions to be intrigu- ing, as if personally relevant and familiar, yet mysterious nonetheless. In some ways this mirrors that of scientific knowledge. The effects of emo- tion on cognition are clearly important but are not fully understood, de- spite clear evidence for a number of important phenomena, including ef- fects on memory, attention, and decision making (Ashby, Isen, & Turken, 1999; Christianson, 1992; Dalgleish & Power, 1999; Dolan, 2002; Eich, Kihlstrom, Bower, Forgas, & Niedenthal, 2000; Forgas, 2001; Isen, 1993; Lane & Nadel, 2000; Lerner, Small, & Loewenstein, 2004; Oatley & Johnson- Laird, 1987; Phelps, Chapter 3; Power & Dalgleish, 1997; Salovey, Mayer, & Caruso, 2002). The aim of this chapter is to articulate an empirically grounded framework for understanding emotion–cognition interactions in mechanistic terms, organized around the concept of control dilemmas.

We focus on affective influences on the exertion of cognitive control and on the direction of selective attention, both of which can be understood in terms of control dilemmas. We do not aim to provide a falsifiable theory so much as a meta-theory: a unified conceptual framework within which to better compare and contrast—and hence potentially understand—re-

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68 COGNITION AND EMOTION

1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

As used in this chapter the term emotion refers to prototypical emotional epi- sodes (Russell & Barrett, 1999): emotion in the heat of the moment, a “complex set of interrelated subevents concerned with a specific object” (Russell & Barrett, 1999, p. 806), accompanied by a subjective feeling (or core affect, Rus- sell & Barrett, 1999) that is at least accessible to awareness, even if not always at the forefront of one’s consciousness. Not everything affective qualifies as emotion, such as preferences and motivationally significant stimuli that need not be subjectively experienced, as well as stimuli that have the potential to evoke emotion (e.g., a photograph of a loved one). Although emotion is often accompanied by facial and other expressions, these are not considered here.

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

Our meta-theory does not deal explicitly with consciousness, so we do not attempt to define it. In part, we argue that emotional states (which tend to be conscious or accessible to consciousness, but need not be; see Winkielman, Berridge, & Wilbarger, Chapter 14) should interact with high-level executive processes (which also tend to be conscious, but also need not be). We also argue that affect can interact with components of selective attention, both endogenous (controlled) and exogenous (automatic). To the extent that con- sciousness is functional, in the sense of having causal consequences, an intrigu- ing candidate for the function of consciousness is to give one part of the system access to global control of the whole system. Each part of the system typically has only limited control of a local subsystem and can provide only a weak bias on the whole system. Informational discrepancies or violations of expectation may be critical as triggering or gating events and, as such, are important for understanding the contents of consciousness (although in themselves, say little about the nature of consciousness; Gray, 1995).

markably varied phenomena. We seek empirical and theoretical constraints on theory building. The meta-theory does not depend on a theory or defini- tion of consciousness.

In diverse subdisciplines of psychology, and increasingly in neurosci- ence and behavioral economics, considerable research has investigated the influences of emotion and related phenomena—both conscious and unconscious—on cognition. Is there a way to refer to and potentially sys-

Affect and Cognitive Control Dilemmas 69

tematize such diverse effects and influences? A promising possibility is to consider people as complex systems, in particular, as complex control sys- tems whose overall function is self-regulation (Carver & Scheier, 1990; Tomarken & Keener, 1998).

A self-regulating system that is complex enough or flexible enough to do more than one thing needs some way of settling on (or otherwise “decid- ing”) what is the best thing to do. Flexibility is useful, but it is a double- edged sword: Being able to do more than one thing opens the door to hav- ing more than a single viable option—and hence to being conflicted about which option is best. Thermostats are paradigmatic control systems that are too simple be conflicted. People can be conceptualized as control systems that, in comparison to a thermostat, are vastly more complex and conflicted (Carver & Scheier, 1990; Dollard & Miller, 1950; Miller, 1944). By a conflict or control dilemma we mean a situation involving inherent tradeoffs in the control of behavior, situations that at the extreme feel subjectively like “damned if you do, damned if you don’t.” By inherent we mean logically or structurally inescapable, such as the speed versus the accuracy of a response, taken in the sense of Marr’s (1982) computational level of analy- sis. That is, conflict is a necessary consequence of optimizing competing goals or constraints. (In the intended sense, conflict is also pervasive in eco- nomic analyses of human behavior; for example, conflict between market equity and market efficiency.) Conflict can occur at many mechanistic lev- els within a control system. Although many control dilemmas can be largely or completely unconscious, they can also be conscious. States of conflict can be subjectively experienced as very unpleasant and even debilitating. Although the affective consequences of conflict are important clinically and theoretically (Carver & Scheier, 1990), they are not central to our interest in the relation between emotion and control dilemmas. Rather, we focus on the role of emotion and affect external to the dilemma as playing a role that can help resolve the dilemma.

In this chapter cognitive control refers to the regulation of thought, feeling, and behavior by actively maintained, internal representations of context information, such as a goal or other information that, when held actively in mind, changes the way in which other information is processed (Braver, Cohen, & Barch, 2002). Active goals can bias processing, leading to changes in thoughts, feeling, and behavior. Cognitive control (also referred to as executive processes or executive attention) is typically deliberate and effortful (Norman & Shallice, 1986; Posner & DiGirolamo, 1998; Posner & Snyder, 1975; Shiffrin & Schneider, 1977; Smith & Jonides, 1999). For example, trying to remember a new phone number just long enough to dial it is effortful and requires cognitive control. In contrast, automatic control is often seemingly effortless or automatic (Bargh, 1994; Shiffrin & Schnei- der, 1977); for example, doing something that is highly practiced, such as

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dialing a phone number one dials every day. Behavior is still controlled by associative links between pressing one digit and the next in the series; it is just not controlled at each step by an actively maintained representation. In short, the process is more ballistic. That is, the cognitive control of thought, feeling, and behavior differs from stimulus-based control of thought, feel- ing, and behavior because it involves actively maintained internal represen- tations. There is no requirement that a goal be conscious, or even accessi- ble to awareness, just that it be actively maintained.

In this chapter we elaborate the idea that a general function of affect is to help resolve control dilemmas. Some control dilemmas involve cognitive control, whereas other do not. Dilemmas can exist between one form of controlled processing and another, between one form of automatic process- ing and another, and between controlled versus automatic processing. Vari- ous theorists have suggested that emotion and affect help assign value or prioritize processing (Dolan, 2002; Oatley & Johnson-Laird, 1987; Simon, 1967; Tomarken & Keener, 1998; Tucker & Williamson, 1984). In behavioral economics risk is increasingly viewed as affective, rather than purely cogni- tive, in nature (Loewenstein & Prelec, 1993; Rottenstreich & Hsee, 2001). Emotion can serve as an interrupt signal that preempts ongoing processing and redirects behavior to more urgent demands (Oatley & Johnson-Laird, 1987; Simon, 1967). And emotion can serve as a signal that one’s progress toward a goal is better than expected (leading to positive affect) or worse than expected (leading to negative affect; Carver & Scheier, 1990). Con- scious emotion, in the form of emotional states, may be a way to convert diverse, fairly abstract contextual cues into an overall assessment of the sit- uation and into an embodied, coordinated response, with the overall con- trol system more optimally tuned to respond as effectively as possible. One function of emotional states may be to modulate cognitive processing in a situation-specific way, setting priorities among conflicting alternatives or tradeoffs. In some sense, emotion serves as a valuation function, regulating the overall mental economy in a way that takes into account both situational (external environment) factors as well as internal constraints on value or subjective importance. A control system dynamically adjusts the behavior of its constituent parts to maintain the integrity, homeostasis, or stability of the whole system, in accord with the internal and external “market forces.” Emotion and cognition are two parts of the overall system. Emotion may influence thought and behavior, in part, by influencing how cognitive parts of the system control thought and behavior. In an integrated system, at some point the distinction between control-by-emotion and control-by- cognition breaks down, and there is just control (Gray, Braver, & Raichle, 2002). Both affective and cognitive forces are at work, exerting control over behavior, yet it is impossible to draw a hard and fast line demarcating

Affect and Cognitive Control Dilemmas 71

where one stops and the other begins. They conjointly control behavior. A subthesis of this chapter is that such integration is especially important dur- ing control dilemmas.

Consider an example. There is often a tension between the short-term and the long-term effects of a given choice or action: “Damned now if you do, damned later if you don’t” (or vice-versa). Such temporal dilemmas are inherent in many real-world situations, such as buying on credit, and in various self-control tasks, including delay of gratification (Mischel, Shoda, & Rodriguez, 1989), distributed choice (Herrnstein, Loewenstein, Prelec, & Vaughan, 1993; Herrnstein, Prelec, & Vaughan, 1986), and other equally fiendish scenarios (e.g., Heatherton, Herman, & Polivy, 1991; Leith & Baumeister, 1996). Emotion might help to resolve the control dilemma in favor of one outcome or another, by helping to tip the balance. When peo- ple are genuinely threatened, they may need to choose what is better in the short term, even if it means incurring a larger long-term cost (Gray, 1999). An emotional state may help people act in what would ordinarily be an impulsive way. Consistent with this logic, threat-related emotional states can bias people to prioritize immediate gains, even at an overall cost, such that they repeatedly chose a smaller–sooner reward over a larger–later one (Gray, 1999). In children, stress tends to impair ability to delay gratification (see Metcalfe & Mischel, 1999), whereas induced positive mood appears to enhance delay of gratification (Fry, 1977). This example is meant to illus- trate a control dilemma (short-term vs. long-term conflict) in which emo- tion provides a way to tip the balance (acting impulsively, delaying gratifi- cation) in ways that could be adaptive. Beyond short-term versus long-term conflicts, there are myriad ways in which people feel conflicted. Emotion might help to resolve some of these dilemmas.

POTENTIALLY CONSCIOUS CONTROL DILEMMAS: EMOTION AND COGNITIVE CONTROL

In this section we first consider a control dilemma that has been extensively considered and investigated, namely, approach–withdrawal conflict, and then turn to other forms of conflict. We do not claim that such conflict is always conscious, but we do consider it likely that such conflict is poten- tially conscious or accessible to awareness.

Approach–Withdrawal Conflict

It is impossible to simultaneously approach and withdraw from something, and yet it is possible to be strongly motivated to do both—creating a state

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of profound conflict. In this section we consider approach–withdrawal conflict, viewing it as a fundamental way for people to be conflicted. Approach–withdrawal emotions are those such as enthusiasm or desire (approach motivated) and fear and anxiety (withdrawal related; Davidson, 1995; Sutton & Davidson, 1997). Many theorists consider approach and withdrawal motivation to be basic or fundamental dimensions, with other aspects of motivation being elaborations of, or otherwise built upon, these two (Carver, Sutton, & Scheier, 2000; Frijda, 1999; Gray, 2002; Lang, Bradley, & Cuthbert, 1990; Miller, 1944).

Approach- and withdrawal-motivated emotions are action oriented or goal directed (Carver et al., 2000; Davidson, 1998). These emotions are subjectively experienced as urgent. Because they are goal directed, these emotions might be expected to influence the cognitive and neural mecha- nisms that support action control and goal-directed behavior, including cognitive control and the lateral prefrontal cortex (Gray, 2001; Gray et al., 2002; Heller, 1990; Tomarken & Keener, 1998). A key idea of the control dilemma perspective is that emotional states can prioritize some (cognitive) functions over others. That is, when there is a conflict over which of two mutually exclusive options to exercise in a given situation (e.g., which of two strategies), only one of which can be implemented at a time, we argue that a given emotion may be able to enhance one of them; enhancing both does not resolve the dilemma. The idea we explore is that emotion helps commit the overall system to a particular, coherent mode of operation (Oatley & Johnson-Laird, 1987). One important source of evidence for this perspective is demonstrations of emotion’s selective effects on cognition, including working memory and cognitive control tasks (Gray, 2001; Gray et al., 2002), frontal lobe tasks (Bartolic, Basso, Schefft, Glauser, & Titanic- Schefft, 1999), and reasoning tasks (Markham & Darke, 1992; Palfai & Salovey, 1993). Selectivity demonstrates that the underlying cognitive and neural architecture is suitable for the overall perspective we propose. Iden- tifying selective effects of emotion does not show that the effects are adaptive—which would require further evidence.

To provide methodologically rigorous evidence for selectivity, we asked participants to watch short videos (to induce an emotional state) and then perform a computerized “three-back” working memory task (to tax cognitive control; Gray, 2001). The three-back task is like a challenging (but not terribly exciting) video game, in which participants need to keep a list of three items in mind. Every few seconds participants have to update their mental list, adding a new item and dropping the oldest, and pressing a but- ton to indicate if the old one matched the new one. Most people find the task very demanding. Working memory, or the active maintenance and manipulation of information in mind, can greatly tax cognitive control,

Affect and Cognitive Control Dilemmas 73

especially when both maintenance and manipulation are required. For methodological reasons, we used both verbal and nonverbal versions of the working memory task. The key prediction was that a given emotional state would influence some tasks but not others, and that the profile of how tasks were influenced would depend on the emotional state. The specific direc- tion of the effect was predicted on the basis of prefrontal hemispheric asymmetries for both approach–withdrawal emotion (e.g., Davidson, 1995; Harmon-Jones & Allen, 1997; Harmon-Jones & Sigelman, 2001; Sutton & Davidson, 1997) and for verbal–nonverbal cognition (e.g., Hellige, 1993; Kelley et al., 1998). The two asymmetries are typically investigated separately, but two untested theoretical positions suggested that emo- tional asymmetries and cognitive asymmetries could interact (Heller, 1990; Tomarken & Keener, 1998). Specifically, approach-related states should activate the left prefrontal cortex (PFC) and enhance processing that depends on that region (e.g., verbal), whereas withdrawal-related states should activate the right PFC and enhance processing that depends on that region (e.g., nonverbal).

We tested this hypothesis in behavioral studies (Gray, 2001) and a functional magnetic resonance imaging (fMRI) study (Gray et al., 2002). The key behavioral effect we found is that an approach-related state (amusement, from 10-minute comedy videos) enhanced verbal working memory performance but impaired spatial working memory performance. In contrast, a withdrawal-related state (anxiety, from 10-minute horror videos) had exactly the opposite effect. That mild anxiety actually enhanced perfor- mance on the spatial task is a counterintuitive finding. Moreover, task- related brain activity was modulated by induced emotions in a manner that was not only consistent with these effects; in addition, the magnitude of the effect of emotion on brain activity predicted the magnitude of the effect on behavior. First, we discuss the behavioral data and then the fMRI data.

A planned analysis of individual differences suggested that the behav- ioral effect was due to induced approach- and withdrawal-related emo- tional states specifically. The more emotionally engaged with the film clips a person became (as indicated by self-reported ratings afterward), the stronger the experienced emotional state and the stronger the effect on per- formance. Critically, individual differences in self-reported personality, and specifically approach and withdrawal disposition as assessed using Behav- ioral Inhibition and Activation scales (BIS–BAS; Carver & White, 1994), predicted which people would experience which effects more strongly. The key result was that individual differences in approach–withdrawal emo- tional reactivity (BIS–BAS) predicted how strongly the emotion induction would influence task performance. That is, the strength of the behavioral effect covaried with individual differences in approach and withdrawal

74 COGNITION AND EMOTION

motivation, and this relation was not explained by performance in a neutral condition. The behavioral effect and the validation using BIS–BAS mea- sures provided a methodologically rigorous test of the idea that induced emotional states have selective effects on cognitive control or executive function, broadly construed.

A further question concerns the specific direction of the observed effect: That is, why should mild anxiety enhance spatial working memory, but mild amusement enhance verbal working memory? The data reveal a selective effect but, of themselves, do not indicate why the effect should be in the direction observed. There are several possible reasons why this par- ticular direction might be adaptive, not simply accidental. We have previ- ously discussed this effect in terms of weak biases on computational effi- ciency, acting in a hemisphere-specific manner (Gray & Braver, 2002b). Several weak biases acting in concert could give rise to an overall, and per- haps even substantial, computational advantage to having different cogni- tive functions lateralized, with emotional enhancement of some, but not other, functions achieved in a hemisphere-specific manner. We briefly dis- cuss two potential types of lateralized cognitive biases that could account for the behavioral data: sustained attention and fine motor control.

Sustained attention and orienting might be more critical in withdrawal- related than approach-related states to facilitate vigilance for a potential threat and rapid orienting to the occurrence of an actual threat. Because nearly all creatures face the threat of predation, there is strong selection pressure to evolve strategies to reduce the danger (Lima & Dill, 1990). Although these forms of attention would be useful in approach-related states, they seem unlikely to be as critical as they are in withdrawal states. Consistent with a hemisphere-based account, neural networks for sus- tained attention and attentional orienting are relatively right lateralized (Cabeza & Nyberg, 2000; Pardo, Fox, & Raichle, 1991). Fine versus gross movement control could be more important in approach versus withdrawal states, respectively. Fine motor control is left lateralized (e.g., left hemi- sphere control of the right hand; Hellige, 1993) and could be more impor- tant in approach-related behaviors (e.g., precise grasping). Coordination of large muscles groups would be more critical for withdrawal (e.g., escaping by running). Several weak biases acting collectively could produce an over- all computational advantage for colateralization of cognitive control func- tions to enable selective regulation by approach–withdrawal states. This account is speculative yet consistent with computational principles and neurobiological evidence about hemispheric specialization, and it makes testable predictions.

Another possible interpretation that we have begun to explore de- pends on the idea that there are two modes of cognitive control: proactive

Affect and Cognitive Control Dilemmas 75

and reactive (Braver, Gray, & Burgess, in press). A proactive mode is what we have described above simply as cognitive control: the active mainte- nance of context information to bias subsequent information processing. In addition, we hypothesize that the cognitive system can exert control through the use of a reactive, rather than a proactive, control strategy. We posit that reactive control occurs following (rather than prior to) the occur- rence of some imperative event. Prior to this event, the system remains rel- atively unbiased and thus relatively free to be driven by bottom-up inputs. Reactive control mechanisms are engaged only as needed, rather than con- sistently, and on a “just-in-time” basis, rather than in advance of their required usage. Finally, when control depends upon the use of context information, the activation of such information by reactive mechanisms occurs transiently rather than in a sustained fashion, and thus decays quickly. As a consequence, in situations when the same context must be accessed repeatedly, full reactivation of the information must occur each time it is needed.

It may be the case that the proactive and reactive systems are fully independent and thus may both be engaged simultaneously. Neverthe- less, there is likely to be a bias favoring one type of control strategy over the other. Such a bias could result from stable individual differences, task demands, or—most relevant for this chapter—induced emotion. Spe- cifically, when participants engage in a verbal working memory task, they may spontaneously adopt a proactive mode, given the relative ease of actively maintaining just a few words. Conversely, when they engage in a nonverbal working memory task, participants may adopt a reactive mode, given the relative difficulty of actively maintaining large amounts of visuospatial information. Approach-related emotional states may bias the system toward a proactive control mode, in part, to sustain a representa- tion of a potential reward actively in mind and guide behavior toward obtaining that reward. Threat-related emotional states may bias the sys- tem toward a reactive mode; threats are typically encountered suddenly rather than slowly, with long anticipation. It seems likely that there is no perfect mapping of the emotional state onto the control mode (e.g., one can envision rumination producing a proactive, sustained anticipatory anxiety). The point for present purposes is that the effect of induced emo- tion on verbal and nonverbal working memory performance (Gray, 2001; Gray et al., 2002) may, we speculate, be explainable in terms of effects on proactive and reactive control, rather than on verbal and nonverbal pro- cessing specifically. Even if this account should eventually fall short, we suggest that it is worth trying to understand emotion–cognition interac- tions in terms of effects on underlying computational processes, and not particular tasks.

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In an fMRI study using the same behavioral paradigm, we provided what is, to our knowledge, the first evidence for selectivity of emotional influences on cognitive control using functional brain imaging (Gray et al., 2002). Although there has been a great deal of work on emotion–cognition interaction (see Phelps, Chapter 3), little or none of it has examined whether emotion can have selective effects on cognitive brain activity. To our knowledge, there are no imaging studies that can be reinterpreted as evidence for such integration, because the minimum experimental design requirements have not been met. Single-task studies (e.g., of emotion and verbal fluency; Baker, Frith, & Dolan, 1997) cannot show selectivity, because showing selectivity requires having at least two tasks, one of which is influenced by emotion and the other is not.

Using the same methods as the behavioral studies, we found that in- duced emotion modulated task-related neural activity within the lateral prefrontal cortex, a region of the brain that is critical for cognitive control (Braver et al., 2002; Miller & Cohen, 2001). The most salient finding was that some brain areas showed a selective effect, with the influence of a particular emotion (amusement, anxiety) depending on the type of cognitive control task (verbal, nonverbal), thereby meeting formal criteria for integration. Moreover, how strongly the emotion induction modulated brain activity was correlated with how strongly the emotion modulated task performance—a finding that is consistent with a causal role of this brain area in influencing behavior. The mere existence of a region with this highly specific profile of activity suggests that emotional states and higher cognition are truly integrat- ed. At some point of processing, functional specialization is lost and emotion and cognition conjointly and equally contribute to the control of thought and behavior. The fMRI data make this point compellingly: Integration occurs not merely somewhere in the brain, but does so specifically in areas that are known from much other work to be critical for cognitive control.

Emotion and Inhibitory Control

When considering how emotion interacts with cognitive control, inhibitory control seems to warrant close attention; yet, to our knowledge, it has been the subject of limited investigation. Because inhibitory control is necessary in situations of conflict between an intended thought, feeling, or behavior and a prepotent or dominant one, effects of emotion on inhibitory control might be particularly relevant to a control dilemma perspective. We note that such high-conflict situations might also involve consciousness, al- though we are agnostic about a necessary role for consciousness. Inhibition may also be a consequence of emotional response—for example, freezing behavior or other behaviors that suppress active motor responses.

Affect and Cognitive Control Dilemmas 77

Inhibitory control is the cognitive capability responsible for deliber- ately suppressing dominant, automatic thoughts or motor responses in order to replace them with responses more adapted to the individual’s cur- rent goals. For clarity, inhibitory control should be distinguished from behavioral inhibition, as used by Gray (1982) to indicate a system charac- terized by a sensitivity to signals of punishment, nonreward, and novelty aimed at avoiding aversive outcomes. Inhibitory control should also be dis- tinguished from Kagan’s (e.g., Kagan, Reznick, & Snidman, 1988) use of the term inhibition to describe socially inhibited (shy) children. This section focuses solely on inhibitory control in the first sense.

A classic example of inhibitory control is instantiated in the Stroop task, in which participants are instructed to name the ink color of color words (MacLeod, 1991; Stroop, 1935). There are typically three conditions in a Stroop task: an incongruent condition in which the subject has to name ink colors that are different from the color word (e.g., the word RED in green ink), a congruent condition (RED in red ink), and a control condition in which the words are not color names or are replaced by non-word symbols. The classic result is slower reaction times in the incongruent condition. The interpretation of this effect is that reading a word is an automatic skill (i.e., highly overlearned). When subjects try to name the color of a word, it is practically impossible for them to avoid reading the word, despite the fact that reading the word interferes with the main task. To respond as instructed, participants have to inhibit the automatic word reading in order to successfully accomplish the task (Hughdahl & Stormark, 2002; MacLeod, 1991). Thus there is a control dilemma: a direct conflict between automatic processing (reading the word) and controlled processing (naming the color). The effect is so strong that the unintended slowing can be readily perceived by the participant.

Inhibition appears to be a basic, core aspect of executive control that is involved in most executive tasks (Miyake et al., 2000; Zacks & Hasher, 1994) and is an important function of the prefrontal cortex (Diamond & Goldman-Rakic, 1989; Fuster, 1997). Top-down inhibitory control of domi- nant responses is an omnipresent process during the self-regulation of emo- tion, when involuntary emotional responses have to be suppressed and overridden by controlled responses more adapted to the individual’s goals (Ochsner, Bunge, Gross, & Gabrieli, 2002; Schaefer et al., 2003).

Most everyday life situations in which inhibitory control is required involve emotions, to a certain extent. Indeed, inhibitory control is enacted in situations in which a choice has to be made between at least two conflict- ing responses. Inhibitory control processes suppress the response that is incongruent with the individual’s current goals and prioritize the congru- ent response. This implies that the utilization of inhibitory control is a nec-

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essary consequence of the appraisal of the goal—(in)congruency of a given situation. Goal incongruency is a strong potential cause of emotional activa- tion (Carver & Scheier, 1990; Frijda, 1986; Higgins, 1987; Johnson & Multhaup, 1992; Lazarus, 1991; Power & Dalgleish, 1997; Scherer, 2001). (Note that goal incongruency or expectation mismatch may trigger more elaborate processing and conscious awareness (Gray, 1995). Therefore, inhibitory processes are likely to be activated conjointly with an emotional activation in natural situations, thereby increasing the need to understand their potential interactions.

There are at least three main sources of empirical contributions to the understanding of the interactions between emotion and inhibitory control. First, several studies have tried to assess the inhibition of emotional con- tents, mostly using the emotional Stroop task. Second, several studies assessed the performance of emotionally disordered patients in inhibitory control tasks. Third, at least two studies have investigated how affective manipulations influence performance on cognitive control tasks that re- quire inhibition.

In the emotional Stroop paradigm, participants are asked to name the ink color of emotional words compared to neutral words (for an excellent review, see Williams, Mathews, & MacLeod, 1996). The prototypical result is that the time needed to name negative or positive words is increased in comparison to neutral words, though the effect is more reliable if the words used refer to a personal concern of the subjects (Hughdahl & Stormark, 2002). However—and importantly—it is not clear that inhibitory control processes are the critical factor in the emotional Stroop effects. Indeed, there are no clear incongruent or congruent conditions in this paradigm, because the words are not color words. Hence it can be argued that there is no conflict between two competing responses of the same category. The emotional Stroop results might be best understood as the results of an attentional bias toward emotional information (Hughdahl & Stormark, 2002).

Another method of investigating the interaction between emotion and inhibitory control is to assess the impact of long-term emotional states and dispositions on inhibitory performance. Disposition can be investigated by examining performance of either normal participants or emotionally disor- dered patients on inhibitory tasks. Several studies tried to assess the perfor- mance of patients with emotional disorders on inhibition tasks. A reliable finding seems to be the impairment of inhibitory control in depressed patients. For instance, Lemelin and colleagues (Lemelin, Baruch, Vincent, Everett, & Vincent, 1997; Lemelin et al., 1996) found that depressed patients were impaired in the standard Stroop task and in a visuospatial interference test, suggesting that these patients had impaired inhibitory control. Similar results have been reported for bipolar depressed patients

Affect and Cognitive Control Dilemmas 79

in their depressive phase (Ali et al., 2000; Jones, Duncan, Mirsky, Post, & Theodore, 1994). Further, Murphy and colleagues (1999) found that the reaction times of depressed patients were slower when attempting to inhibit a response in a go/no-go task, which requires withholding a re- sponse.

An impairment of inhibitory control also seems to be a consistent find- ing in patients with obsessive–compulsive disorder (OCD), a debilitating anxiety disorder. For instance, Hartston and Swertlow (1999) found that patients with OCD were impaired in their performance on the Stroop task. Bannon, Gonsalvez, Croft, and Boyce (2002) found the same result using a Stroop task and a go/no-go task; Rosenberg, Dick, O’Hearn, and Sweeney (1997) found an impairment of response inhibition in patients with OCD, using an antisaccade task. Interestingly, the impairment of response inhibi- tion in patients with OCD remained significant even after controlling for schizotypal and depressive symptoms (Aycicegi, Dinn, Harris, & Erkmen, 2003).

Other emotional disorders also seem to be associated with a dysfunc- tion of inhibitory control. For instance, Wood, Mathews, and Dalgleish (2001) found that high-trait-anxious individuals were impaired in their ability to inhibit the inappropriate meaning of a homograph. Further, Stein, Kennedy, and Twamley (2002) found that women suffering from posttraumatic stress disorder (PTSD) were impaired in their performance on the Stroop Color–Word Test and in a set-shifting task. Moreover, Murphy and colleagues (1999) found that manic patients committed more errors than depressed and controls in a go/no-go task.

Overall, the data seem to indicate that emotional disorders are associ- ated with impairments of inhibitory control. However, it is not yet clear which processes are responsible for this pattern of results. Indeed, at least two main alternative explanations can account for the association between emotional disorders and inhibitory impairment. The first account empha- sizes an impairment of inhibition as causing the emotional disorders by impairing capacities that regulate emotion. The second account emphasizes that depressed or anxious moods are associated with more rumination (neg- ative repetitive thoughts) that creates a working memory load and depletes attentional resources (Watkins & Brown, 2002).

A direct test of the interaction between affect and inhibitory control would consist of assessing the performance of normal subjects in an inhibi- tion test just after the induction of an emotional state. To our knowledge, only two studies have explicitly adopted this procedure, and they obtained contradictory results. First, Kuhl and Kazen (1999) assessed standard Stroop color naming after a brief exposure to affectively valenced words. They found that the color–word interference disappeared after exposure to positive words, compared to neutral and negative words, with no differ-

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ences between neutral and negative words. This is a remarkable result, although it is not clear whether the effect is caused by an actual emotional state or the priming of emotional semantic categories that have been acti- vated by the emotional words. Even still, exposure to positive affective stimuli enhanced performance. Second, Phillips, Bull, Adams, and Fraser (2002) assessed Stroop performance after a mood induction procedure by recollection of positive versus neutral memories. They found that the recol- lection of positive memories impaired Stroop performance in a standard version of the task (naming the ink color of incongruent color words), and that this impairment was more pronounced when the subjects had to alter- nate between word and color naming. Hence this study’s results argue for a deleterious effect of positive emotion on inhibitory control. One of the main differences between these two studies is the mood induction proce- dure (MIP) used. Although memory recollection might have been more effective than using affectively valenced words to elicit an actual emotional state, the task of recollecting an emotional autobiographical memory may have increased the occurrence of thoughts related to the remembered event or mood-related thoughts, thereby depleting the working memory resources necessary to successfully achieve the Stroop task.

More generally, to understand emotional modulation of inhibitory con- trol, several conceptual and methodological issues need to be better under- stood. For instance, direct tests of the emotional modulation of inhibitory control should take into account the different processing characteristics of MIP and their possible effects on the inhibition task. In addition, it would be worthwhile to explore the effects of other emotional properties than valence (e.g., emotional arousal, specific emotional appraisals) on inhibitory control. Future studies should also consider the possibility that cognitive control encompasses several dissociable processing components that play different roles in inhibitory control processes, and that may be differen- tially affected by emotion. Indeed, some distinctions have been proposed in the literature between conflict detection and maintenance processes (Botvinick, Braver, Barch, Carter, & Cohen, 2001; Braver & Cohen, 2000; Kerns et al., 2004), and between reactive and proactive control (see previ- ous section; Braver et al., in press).

POTENTIALLY UNCONSCIOUS CONTROL DILEMMAS: AFFECTIVE INFLUENCES ON SELECTIVE ATTENTION

In this section we shift from considering emotion as a quasi-executive form of control that shapes cognition, to considering affective influences on selective attention. We do not claim that such influences are always uncon-

Affect and Cognitive Control Dilemmas 81

scious, but we do consider it likely that they are often unconscious or not accessible to awareness. Selective attention has multiple components, including some that are controlled and some that are automatic, and for this reason is potentially a very interesting paradigm in which to examine rela- tions among emotion, control, and consciousness.

Although the word control implies the operation of explicit, goal- driven mechanisms, control dilemmas themselves can occur whenever the cognitive system must “choose” between two or more comparable options. In such cases, selective attention can shift the weight allotted to certain signals, biasing the paths taken in the course of cognitive processing (Desimone & Duncan, 1995). Notably, selective attention is not always under deliberate or effortful control; just as people can often direct atten- tion voluntarily, attention can also be captured without a person’s volition (Yantis & Jonides, 1984). The former type of attentional allocation is often referred to as endogenous, voluntary, or top-down; the latter is often referred to as exogenous, automatic, or bottom-up. Evidence from a number of studies suggests that differences in manner of allocation reflect the oper- ation of separable components of attention. For example, relatively auto- matic attentional shifts tend to be linked with a transient time-course, in which maximum facilitation of processing at the attended location is reached within about 150 milliseconds, but declines soon thereafter. In contrast, voluntary shifts can be sustained: Maximum facilitation is reached after about 300 milliseconds and can be maintained for extended periods of time (Müller & Rabbitt, 1989; Nakayama & Mackeben, 1989). In addition, different neural networks are implicated in the different types of attention shifts, with automatic shifts associated with heightened right-lateralized activity in the temporoparietal and inferior frontal cortices, and voluntary shifts associated more with activity in the intraparietal and superior frontal cortices (Corbetta & Shulman, 2002). Finally, it has been suggested that exogenously and endogenously allocated attention might have different consequences for the binding of visual features (Briand & Klein, 1987) as well as for conscious awareness of a stimulus (Most, Scholl, Clifford, & Simons, 2005).

Regardless of distinctions between different components, attention by its very nature involves the resolution of competing demands. The distinc- tion between relatively automatic and voluntary attentional shifting, plus a growing literature on individual differences and attentional biases to emo- tional information, make an examination of selective attention potentially fruitful for exploring control dilemmas at multiple levels of cognitive pro- cessing.

Evolutionary arguments have highlighted the adaptive nature of biases to attend to emotional information (e.g., Lundqvist & Öhman, Chapter 5;

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Öhman & Mineka, 2001). When unexpected sources of danger or self- relevance appear, it is almost always in one’s best interest to attend to them right away (cf. Simon, 1967). Consistent with this hypothesis, several stud- ies have demonstrated that potentially threatening stimuli capture atten- tion more readily than nonthreatening stimuli. For example, it is easier to detect a discrepant angry face among happy faces than vice versa (Öhman, Lundqvist, & Esteves, 2001; Lundqvist & Öhman, Chapter 5). Further- more, such effects can be very specific; stimuli that are evocative to one person can seem bland to another—and attentional biases often reflect such idiosyncrasies. In one study, patients with specific phobias were asked to engage in a visual search for pictures of snakes, spiders, or flowers and mushrooms in a computer display (Öhman, Flykt, & Esteves, 2001). In this paradigm, the time it takes to locate a target typically varies as a function of the number of distracters in the display: The greater the number of distracters, the longer the search time. Attentional biases to a stimulus are inferred when people consistently direct attention to that stimulus first, in which case search time is generally unaffected by the number of distracters present (Treisman & Gelade, 1980). When participants searched for spider or snake targets among flower and mushroom distractors, not only were they faster to find the target than when searching for flowers or mushrooms among snakes and spiders, but this was especially true when the target was specific to the participant’s phobia (i.e., a snake for people with snake pho- bia or a spider for those with spider phobia). Importantly, the speed of find- ing the fear-relevant targets (but not the fear-irrelevant targets) was rela- tively unaffected by the number of distractors in the display—a pattern that suggests strong attentional biases for fear-relevant stimuli (Öhman, Flykt, et al., 2001).

Given that people appear predisposed to attend to emotional stimuli, emotional or mood states and chronic affective styles might help to mediate such attentional biases. Some of the strongest evidence in support of this possibility comes from research on emotional disorders (McNally, 1996). For example, in a dot-probe task, clinically anxious individuals were faster than both healthy controls and clinically depressed individuals to respond to probes, when the probes appeared at locations previously occupied by threat cues rather than locations previously occupied by neutral cues (MacLeod, Mathews, & Tata, 1986). Similarly, people with PTSD, as well as particular phobias and anxieties, have difficulty ignoring information rele- vant to their disorders, as demonstrated by interference in the emotional Stroop paradigm. In this task, people were slower to name the colors of words when the words themselves were emotional rather than neutral. Again, these effects can be quite specific. Thus war veterans with PTSD were especially slow in response to words such as body-bags (McNally,

Affect and Cognitive Control Dilemmas 83

Kaspi, Riemann, & Zeitlin, 1990), whereas socially anxious individuals were selectively slower in response to socially relevant words such as party (Hope, Rapee, Heimberg, & Dombeck, 1990; McNally et al., 1990).

Notably, in both the emotional Stroop and dot-probe paradigms, the emotional nature of the stimuli is irrelevant to the assigned task. This stands in contrast with the search paradigm (e.g., Lundqvist & Öhman, Chapter 5; Öhman, Flykt, et al., 2001), in which subjects actively search for a target that differs from the surrounding stimuli along an emotion-relevant dimension. By emphasizing distinctions between paradigms in which peo- ple actively search for an emotional stimulus and those in which subjects must suppress emotional information, researchers might begin to delineate levels of attentional control that are most affected by emotion-related states or traits. Potentially, these levels could map onto distinctions between rela- tively automatic and voluntary components of attention—and, if only loosely, onto unconscious and conscious processes (cf. Bishop, Duncan, Brett, & Lawrence, 2004).

As insights from the clinical and psychophysical literatures continue to converge, our understanding of how affect influences attentional control is likely to grow more precise. For example, although the emotional Stroop and dot-probe paradigms initially revealed attentional biases broadly de- fined, more recent experiments have sought to pinpoint the mechanisms underlying these biases. Indeed, the simple act of orienting attention can be broken down into at least three components: disengaging from one stim- ulus, shifting attention, and engaging with a new stimulus (Posner & Petersen, 1990). Recent studies have suggested that the biases revealed via the dot-probe (and perhaps the emotional Stroop) might reflect difficulty in disengaging from emotional information rather than biases to shift attention to such information in the first place (Fox, Russo, Bowles, & Dutton, 2001). In these experiments, threatening and nonthreatening faces or words were used as cues indicating the likely location of a target. All cues appeared before the target in one of two potential target locations. Valid cues cor- rectly indicated the target location; invalid cues incorrectly indicated the target location. High-anxious subjects were slower to respond to the target if the cue was invalid but threatening. However, the emotionality of the cues did not seem to affect response time when the cues were valid. This pattern of results suggests that the differences in response times reflected difficulty disengaging from the threatening cues rather than faster alloca- tion of attention to them. Interestingly, these effects were seen only in high-anxious, not low-anxious, subjects (Fox et al., 2001). Such findings contribute to our understanding of which particular components of atten- tion are likely to be especially influenced by emotion. Further understand- ing of the rich interactions between attention and emotion can give us not

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only insight into the organizational structure of emotion-based attentional biases but also serve as a model for understanding how emotional systems can help organize the functioning of other cognitive domains as well.

LOOKING TO THE FUTURE (WITH ANTICIPATION!)

By elaborating several examples, our aim has been to articulate more broadly a meta-theoretical perspective on the function of emotion and affect. We propose that a very general function of affect is to help resolve control dilemmas inherent in being an autonomous (yet highly social), self- regulating control system—er, that is, a human being. We are cautiously optimistic that a control dilemma perspective might be useful beyond the examples given here, by providing coherence to a field poised to make major advances. There are many other ways in which people—and self- regulating systems, more generally—can be conflicted. Some types of men- tal conflict may be severe enough that the conflict becomes conscious or otherwise initiates processing that strongly influences the contents of con- sciousness. Yet other conflicts may be resolved without so much as raising a metaphorical ripple on the surface of the mind, and these may be more the norm than the exception, given that a large proportion of the control of human behavior operates expertly without consciousness.

To hint at the broader relevance of a control dilemma perspective, beyond the examples considered above, we note several tradeoffs that have been suggested to be influenced by emotion and affect. First, a substantial literature converges on the idea that negative moods promote more system- atic processing and positive moods promote heuristic processing (e.g., Bless & Schwarz, 1999; Bolte, Goschke, & Kuhl, 2003; Palfai & Salovey, 1993). The conflict appears to be between whether to engage cognitive control mechanisms (analytic processing) or not (heuristic processing). Heuristic and analytic processing may often preclude each other, leading to control conflict, although it has been suggested that they need not always conflict (Isen, 1993).

Second, a related distinction and possible control dilemma is between global and local attentional focus. One can typically attend either to the “forest” or the “trees” in a given situation—so how does one’s inner homunculus decide to which to attend? An early theoretical account sug- gested that emotion narrows the range or scope of attention (Easterbrook, 1959). Recent work on strategic memory encoding in OCD has suggested a bias toward seeing the details (“trees”) rather than the gestalt (“forest”; Sav- age et al., 1999; Savage et al., 2000). Conversely, positive affect appears to result in a bias toward a global attentional focus (Gasper & Clore, 2002).

Affect and Cognitive Control Dilemmas 85

Third, a computational tradeoff between distractibility and persever- ation (Braver & Cohen, 2000) has been suggested to be influenced by affect (Dreisbach & Goschke, 2004). Specifically, a brief presentation of positive images during a task-switching paradigm led to increased switch costs (perseveration) compared to when the images were affectively neutral, and to decreased switch-costs (distractibility) when the images were affectively positive.

Fourth, anxiety can influence speed versus accuracy (Leon & Revelle, 1985). Specifically, high-trait-anxious participants performing a difficult geometric analogies task under time-stress did not simply perform worse on the task than low-trait-anxious control participants. Instead, a detailed analysis revealed that the trait-anxious participants performed faster, but less accurately, than the controls.

Fifth, effects of emotion on risk taking have been explored (e.g., Isen, Nygren, & Ashby, 1988; Johnson & Tversky, 1983), and these effects are likely amenable to a conflict analysis in terms of risk–reward tradeoffs.

And sixth, consistent with the idea that emotions are not merely per- sonal phenomena but are also strongly social in nature (e.g., Frijda, 1999), a major function of emotion might be to help reduce social conflicts, for example, self-interest versus group (prosocial or collective) interest (Isen, 1970; Isen & Levin, 1972). In the prisoner’s dilemma task, an experimental situation that explicitly presents participants with a conflict between per- sonal and group interest, aspects of emotion and mood could help sustain a bias toward cooperation (Gray & Braver, 2002a; Rilling et al., 2002).

Finally, although we are advocating a general perspective, we empha- size (strongly!) that it is important to make distinctions among affective phenomena. One cannot safely assume that effects of emotion proper on cognition are the same as effects of mood, stress, pain, and various emo- tional psychopathologies. Risk, motivation, reward, and punishment are also categorically different constructs and cannot safely be lumped together or with emotional states in an “emotion-related” conceptual bin. In addi- tion, as many theorists and investigators have emphasized, emotional and mood states are likely to depend in important ways on individual differ- ences, including variation within a normal range and to extremes that are pathological (e.g., Barrett, Chapter 11; Costa & McCrae, 1980; Davidson, 1998; Larsen & Ketelaar, 1991). The states may differ not simply in inten- sity (e.g., depressed mood vs. sadness) but possibly in qualitatively and mechanistically different ways.

In sum, many effects of emotion on various tradeoffs have been explored and documented. The larger computational perspective—of emo- tion as helping to resolve control dilemmas—is more general and, to our knowledge, has not been explored previously as a unifying framework. We

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are cautiously optimistic that a control dilemma perspective can help us better understand effects of emotion, mood, and affective stimuli on cogni- tion. It will be particularly exciting to further investigate such a perspective in relation to conscious and unconscious processes. Consciousness is intriguing but does not lend itself readily to empirical investigation. Poten- tial relationships among consciousness, emotion, and cognitive control are anything but simple. And yet these relationships are profoundly relevant to human nature and human experience. Consciousness, emotion, and cogni- tive control may covary to a significant extent. Moreover, they may covary for functionally adaptive reasons related to enhancing global control and, if the present argument is on the right track, to the resolution of control dilemmas.

ACKNOWLEDGMENTS

Some of the research described in this chapter was supported by a grant from the National Science Foundation, and preparation of the chapter was supported by a grant from the National Institute of Mental Health.

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PART II

Unconscious Emotional

Processing

Perception of Visual Stimuli

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CUaNuCghOtNbSyCthIeOEUvSilAENyDe EMOTIONAL PROCESSING

CHAPTER 5
Caught by the Evil Eye

Nonconscious Information Processing, Emotion, and Attention to Facial Stimuli

DANIEL LUNDQVIST ARNE ÖHMAN

A BIOLOGICAL PERSPECTIVE ON THE HUMAN FACE

The Face as an Evolved Structure

The mind’s primary façade to the world, the face, is an amazingly complex biological structure. Functionally critical openings for breathing, ingestion of food and fluid, and emission of sounds, as well as more or less hidden sensory surfaces, are embedded in a multitude of muscles and richly wrin- kled skin tissue. In spite of the constraints (two eyes placed above a nose, which is placed above the mouth, and so forth), there are nonetheless strik- ing individual differences in the way we look. As a result, the face is the pri- mary vehicle for visual recognition of individuals. In addition, it provides information about factors such as age, sex, attractiveness, and health (Bruce & Young, 1986; Cole, 1998). However, beyond these relatively static sources of information, the intricate musculature of the face provides rich dynamic information of primary psychological significance.

Facial Muscles and Their Neural Control

There are two layers of facial muscles (see, e.g., Fridlund, 1994, for a review). The inner layer contains very strong muscles of obvious biological significance, such as the masseter and the temporalis, which move the jaw-

97

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1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

The account presented in this chapter addresses the face as an emotional stimu- lus. The basic premise is that humans are evolutionarily prepared to respond to and produce emotional facial gestures. This means that we respond automati- cally to emotional faces even if their expressions are masked from conscious recognition. Furthermore, threatening faces attract attention when presented among neutral or emotional distractor faces.

From the evolutionary perspective, emotions are viewed as dispositional states that give attentional priority to particular stimuli and prime responses that, in the long run, promote the transfer of genes between generations. A pri- mary task of emotions is to evaluate which stimuli are good and bad in the sense that they should be approached or avoided. Emotions are action sets that prioritize particular classes of functional responses. They are complex responses incorporating diverse and partly independent components, such as expressive behavior (e.g., facial expressions), action tendencies (e.g., avoidance), attentional priorities, and autonomic responses (e.g., skin conductance, heart rate) that pro- vide metabolic support for action and feelings (e.g., an urge to get out of the sit- uation).

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

Un- (or non)conscious and conscious in this chapter simply mean nonreportable and reportable, respectively. To be aware of an event is to be able to report and comment on it.

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

The basic emotion systems are evolutionary old. Because they evolved in primi- tive brains, they rely on ancient systems deep in the human brain that are not readily available to more recently evolved structures such as the cerebral
cortex. Therefore, emotions can be activated automatically and nonconsciously, independently of conscious access to the eliciting stimulus. The validity of this proposal is best documented for the emotion of fear. Because emotion is rapidly activated before the perceptual analysis of the emotional stimulus is complete, it is based on a crude sensory analysis likely to rely on critical features rather than on sophisticated configural analysis.

The rapid recruitment of subcortical emotional networks is consistent with a Jamesian view on emotion, according to which the feeling comes late and includes conscious appreciation of the bodily response in relation to the elicit- ing stimulus.

Caught by the Evil Eye 99

bone. In contrast, the function of the outer layer may appear somewhat obscure. It is composed of numerous small muscles that primarily move facial skin tissue rather than, like most other striped muscles, body limbs. The sphincter muscle encircling the eye, the orbicularis oculi, which medi- ates involuntary eyeblinks, and the corrugator supercilii, which lowers the medial part of the eyebrows, both serve obvious functions in protecting the eye. However, they are also used voluntarily in what appear to be biologi- cally more arbitrary activities such as flirting or to emit “eyebrow flashes,” a universal gesture of friendly greeting (Eibl-Eibesfeldt, 1970). Similarly, the zygomaticus major connects the corner of the mouth to the cheekbone, not to expose the canines but to produce the most universally recognized facial gesture, the smile (e.g., Russell, 1994).

The facial muscles are innervated from two quite distinct neural sys- tems of different evolutionary origin. The evolutionarily older system origi- nates in the striatum, the top level of what was once the reptilian brain, that controls reflexive behavior related to basic biological functions such as consumatory behavior, attack, and defense. This system exerts involuntary, symmetric, and bilateral control of the facial musculature (Fridlund, 1994). The other system, of much later evolutionary history, has the typical contralateral origin of voluntarily controlled muscles, with neurons starting in the face area of the motor cortex to provide fine-tuned control of muscles primarily around the mouth for sound articulation (Gazzaniga & Smylie, 1990). Its evolution was part of the emergence of the most human of all characteristics, language. However, the resulting fine-tuned control of the lower face not only benefited the repertoire of speech sounds but also sup- ported voluntary facial actions that could be used for visual rather than vocal communication. Thus this control could override and partly conceal the facial responses evoked by the more reflexive older system originating in the striatum. Accordingly, intentional social smiles that do not necessar- ily mediate felt happiness primarily involves the mouth, whereas a felt “Duchenne smile” also incorporates the muscles around the eyes (e.g., Ekman, 2003).

Thus part of facial muscle control is likely to have coevolved with lan- guage, but the primary evolutionary contingencies for facial muscles de- rived from their role in social communication, as first recognized by Dar- win (1872/1998). He pointed to similarities between human facial displays and those of other primates, and subsequent research has generated quite convincing evolutionary histories for some expressions, such as, for exam- ple, the smile (van Hooff, 1972). Indeed, modern evolutionary theory’s emphasis on the importance of the social interaction in the shaping of humans (e.g., Alexander, 1974; Humphrey, 1983; Trivers, 1985; Wilson, 1976) gives the face a central role in human evolution.

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The human face has a more complex facial musculature than that of other primates. It appears that the proliferation and diversification of facial muscles, as well as the enhanced versatility of their neural control, coin- cided with the rapid enlargement of the hominid brain volume during the past million years (Chevalier-Skolnikoff, 1973). Thus the capacity for com- plex facial displays is likely to have coevolved with enhanced potential for complex behavior and complex inner states (Cole, 1998).

The Role of the Face in Human Evolution

When exchanging life in the rain forest for that on the savanna, early homi- nids were exposed to new sets of survival contingencies. Such contingen- cies included not only an advantage for upright, two-legged locomotion, but also for living in larger, more stably organized groups. Living in large groups provided better protection from the big predators of the savanna and assisted group members in scavenging on their kills in competition with other scavengers. It also facilitated organized hunting of large prey. But living in large groups also posed its own set of critical selection contin- gencies. It necessitated the recognition of, and memory for, a large number of individuals and skillful navigation in a multitude of social relationships. Those successful in this endeavor had to be “natural psychologists” in order to understand, predict, and make use of fellow human beings to their own advantage (Humphrey, 1983). In short, “mind reading” was an important asset. For reading the minds of others, the face is a rich source of informa- tion because facial gestures convey clues to intentions as well as to emo- tional and motivational states. In the context of social interaction, skills in decoding the social signals emitted by another person are amplified when combined with some degree of volitional control of one’s own signals. As every poker player knows, an expressionless face coupled with astute rec- ognition of emotion in others is a key to success. But a gambler also knows that recognizing and trusting “gut feelings” are important preludes to man- aging one’s own expressive behavior. As noted above, gaining voluntary control of facial muscles benefited both language articulation and control of facial gestures. Thus versatile control of the face muscles was a central component of the social intelligence that many theorists postulate as the critical driving force behind the rapid expansion of human brain size dur- ing the last few hundred thousand years (e.g., Dunbar, 1996; Humphrey, 1983). Often dubbed “Machiavellian intelligence” because the essence of this control was taken to be the ability to exploit social skills and insights in pursuing the interest of one’s own genes (Whiten & Byrne, 1997), the pos- sibility of concealing instinctive expression behind voluntarily controllable ones was a handy tool from this perspective.

Caught by the Evil Eye 101

Production and decoding of facial gestures are likely to have been shaped by mutually dependent evolutionary forces. The ability to produce distinctive displays (e.g., conveying threat) is clearly advantageous from an evolutionary perspective, whether the display communicates an aggressive intention or merely serves as a cue for impending negative consequences (Owren, Rendell, & Bachorowski, Chapter 8). But individuals who more efficiently read their opponents’ threatening stance also have advantages in the next step of the interaction. In short, “displays co-evolve with vigilance for them” (Fridlund, 1997, p. 105). Thus social signaling and the under- standing of social signals coevolve in a process where the “sender’s” signal (signal meaning and signal behavior) and the “receiver’s” neural responses to the signal influence each other to form an integrated social signaling sys- tem for the members of a species (e.g., Endler, 1992; Krebs, & Davies, 1993; Fridlund, 1997; Enquist & Arak, 1998; for an alternative view, see Owren et al., Chapter 8). Accordingly, research on human facial expression indicates that facial expressions comprise both stereotypic signals and sig- naling behavior (the looks and use of facial expressions of anger, happiness, fear, disgust, sorrow, and surprise; see, e.g., Ekman, 2003; for a critical view, see Barrett, Chapter 11), as well as specialized neural structures for recognition of facial emotion and facial identity.

Specialized Neural Structures for Facial Information

If this evolutionary scenario is valid, then one would expect there to be spe- cific neural circuits in the human brain for recognizing the identity of a face as well as the emotions expressed by the face. This expectancy appears to receive support from the data. Processing of faces—in particular, process- ing of facial identity—has been found to involve the fusiform gyrus in the inferior temporal lobe, an area subsequently called the fusiform face area (FFA; e.g., Kanwisher, McDermott, & Chun, 1997; Bruce & Young, 1996; Bruce, Green, & Georgeson, 1996; Adolphs, 2002). Recognition of dynamic facial attributes such as gaze direction and emotional expression, on the other hand, is believed to rely mainly on structures in the superior tempo- ral sulcus (STS)1 (Haxby, Hoffman, & Gobbini, 2000), which has been pro- posed to constitute a system for social cognition in concert with the amygdala and the orbitofrontal cortex (Allison, Puce, & McCarthy, 2000). The notion that faces are processed by specific neural structures has also been supported by several reports of lost ability to recognize faces follow- ing brain damage. Thus damage to the ventromedial regions of the oc- cipitotemporal cortex (including the FFA) typically cause prosopagnosia, a loss of face recognition ability (e.g., Sergent & Signoret, 1992; see also Marotta, Genovese, & Behrmann, 2001). Some patients with prosopagno-

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sia, however, show unimpaired recognition of facial expressions of emotion (Tranel, Damasio, & Damasio, 1988), which supports the notion that facial identity and expression are processed in different areas.

Psychophysiological Responses to Facial Stimuli

Facial Muscle Responses

An evolutionary origin of facial signals implies that humans should possess efficient routines for automatically responding to facial signals. This hy- pothesis has been examined extensively by Dimberg (1982; see reviews by Dimberg, 1990; Dimberg & Öhman, 1996), who used electromyography (EMG) to record responses of facial muscles to facial stimuli. In this way, subtle responses from well-defined facial muscles, not necessarily detect- able by the naked eye, could be accurately quantified. By measuring EMG from the corrugator and the zygomatic major muscles, Dimberg (1982) assessed activity in key muscles for displays of anger and happiness, respectively. The corrugator pulls the eyebrows together to produce the deep furrow in the forehead that signals discontent, anger, or threat, and the zygomatic major pulls the corner of the mouth toward the ear to help produce the universally recognized smile. Dimberg (1982) reported that research participants exposed to an angry face showed increased activity in the corrugator and little change in the zygomatic, whereas a happy face induced the opposite pattern: increased zygomatic activity, with little change in the corrugator. Thus these data suggested that emotional faces induced their mirror images in observers. A happy face activated key mus- cles in a happy display, and an angry face activated key muscles in an angry display. Lundquist and Dimberg (1995) extended this conclusion to a broader set of emotions (anger, happiness, fear, sadness, disgust, and sur- prise) by recording EMG from a larger set of muscles.

The responses in the corrugator and the zygomatic muscles to facial stimuli are rapid, demonstrating differential responses to angry and happy faces within 400 milliseconds after stimulus onset, and reaching peaks of activity within the first second of stimulation (Dimberg & Thunberg, 1998). The rapid activation in these facial muscles is consistent with the hypothe- sis that facial muscles respond automatically and nonconsciously to facial stimuli. This hypothesis was directly tested by Dimberg, Elmehed, and Thunberg (2000) using a backward masking technique (see Esteves & Öhman, 1993). Different groups of participants were exposed to briefly (30 milliseconds) presented angry, neutral, and happy faces that were immedi- ately followed by a much longer (5 seconds) presentation of a neutral mask- ing stimulus. With this arrangement of the stimuli, the participants could consciously perceive only the second, masking stimulus; they could not

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see the preceding target stimulus. Nevertheless, participants exposed to masked happy faces showed larger zygomatic responses than those exposed to masked neutral and angry faces, and those exposed to masked angry faces showed larger corrugator responses than those exposed to masked neutral and happy faces. In other words, the participants’ facial muscles appeared to know more about the stimulus than what the participants were able to perceive consciously. This is a theoretically significant conclusion that is consistent with the facial feedback hypothesis of emotion (e.g., Izard, 1977). Thus, through fast feedback circuits to the brain, the automatically activated facial muscles could add a context that influences the interpreta- tion of a stimulus as emotionally relevant (e.g., James, 1884/1976).

Autonomic Responses

Further support for the notion of automatic decoding of facial signals comes from experiments focusing on the emotional effect of angry faces. Öhman and Dimberg (1978) used facial expressions as stimuli in a Pavlovian condi- tioning experiment with humans, with skin conductance responses (SCRs) as their dependent variable. Different groups of subjects were trained to differentiate between two happy, two neutral, and two angry faces by hav- ing one of them followed by a mild electric shock to the fingers. All three groups acquired differential SCRs to the shock-associated and non-shock- associated face, but only those conditioned to angry faces showed lasting resistance to extinction when the shock was omitted. This basic finding, which has been replicated in several laboratories (see review by Dimberg & Öhman, 1996), has been taken as support for the hypothesis that evolu- tion has prepared humans to persistently associate fear to evolutionarily relevant threat stimuli (Seligman, 1970; Öhman & Dimberg, 1984; Öhman & Mineka, 2001).

The Pavlovian face-conditioning paradigm has been exploited to ana- lyze the nonconscious activation of autonomic responses. After undergoing conditioning to angry or happy faces presented in full view, research partic- ipants presented with masked versions of such stimuli continued to show elevated responses to conditioned angry faces, even though there was no sign of conscious recognition of the emotional expression of the stimulus (Esteves, Dimberg, & Öhman, 1994; Parra, Esteves, Flykt, & Öhman, 1997). Furthermore, Esteves, Parra, et al. (1994) demonstrated that en- hanced SCRs can be conditioned to masked angry, but not to masked happy, faces. Thus not only can responses be elicited by emotionally pro- vocative facial stimuli (with or without previous conditioning), but new responses can also be associated to masked, nonconsciously presented stimuli. Applied to face-to-face situations of social encounters, these data suggest that barely perceivable facial gestures can result in nonconsicous

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Pavlovian conditioning of fear responses to a sender who induces aversive emotional states in the receiver.

Brain Responses to Masked Facial Stimuli

There is an extensive literature suggesting that the amygdala, a collection of neural nuclei in the anterior medial temporal lobe, is sensitive to visual information as it pertains to social interaction; a primary source for such information, of course, is the face (see reviews by, e.g., Adolphs, 2002; Öhman, 2002). Morris, Öhman, and Dolan (1998) examined amygdala responses to nonconsciously and consciously presented facial stimuli. They used a Pavlovian face-conditioning paradigm to induce enhanced emo- tional responding to an angry face by pairing it with an aversive noise. These conditioning trials were presented among other trials involving either of two neutral faces or another angry face, with none of these faces followed by the noise stimulus. Participants were then placed in a positron emission tomography (PET) scanner to assess regional changes in cerebral blood flow to facial stimuli presented under different conditions of aware- ness. The participants were exposed to scans involving repeated pair-wise presentations of the facial stimuli in different sequences. In different scans, the conditioned angry face was masked by one of the neutral faces, and the nonconditioned angry face was masked by the other neutral face. Partici- pants could only perceive the neutral faces consciously and remained unaware of the preceding angry face. In this way, changes in regional cere- bral blood flow could be contrasted between conditions involving two masked angry faces, one of which had been given enhanced emotional impact through conditioning.

Morris et al. (1998) reported reliable and specific activation of the right amygdala to the masked conditioned angry face, thus demonstrating that conscious perception of the emotional nature of the stimulus was not neces- sary for activation of the amygdala. Following up on these data, Morris, Öhman, and Dolan (1999) tried to delineate the network of structures that occasioned nonconscious activation of the amygdala to masked, emotion- ally provocative stimuli. They examined covariations between blood flow changes in the amygdala and changes in other brain areas. Morris et al. (1999) reported that two structures, the superior colliculus of the midbrain and the right pulvinar of the thalamus, were statistically tied to non- conscious activation of the right amygdala.

These results were replicated on a patient with blindsight (see Weiskrantz, 1985), who had blind areas in the visual field because of damage to the primary visual cortex (Morris, de Gelder, Weiskrantz & Dolan, 2001). The amygdala was activated by nonperceived faces presented in the blind

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areas of the visual field, and connectivity analyses tied this effect to the supe- rior colliculi and the pulvinar. The superior colliculus and the pulvinar are closely linked to attentional systems of the brain that control eye movements and the selection of salient visual objects (Posner & Peterson, 1990; Robinson & Peterson, 1992; see also LaBerge, 1998; Wright, & Ward, 1998). These “magnocellular” pathways are served by large, rapidly conducting neurons that mediate low-frequency information and provide a rough outline of a scene, whereas more detailed high-frequency information is conveyed by a separate “parvocellular” system served by smaller neurons that provide information about color and objects. Vuilleumier, Armony, Driver, and Dolan (2003) filtered visual information to separately activate these two systems in response to facial stimuli. They showed that only low-frequency information activated the amygdala, supporting the hypothesis that the effect was medi- ated by the pathways that pass through the superior colliculi. Thus the results of Morris et al. (1998, 1999, 2001) and Vuilleumier et al. (2003) are consistent with LeDoux’s (1996, 2000) model of fear activation, which proposes that the amygdala can be nonconsciously accessed from subcortical sites to rapidly redirect attention and to set emotion in progress, even before the eliciting stimulus has been registered in consciousness.

Conclusion: Biology and the Nonconscious Recognition of Emotional Facial Stimuli

The research reviewed in this section shows that faces presented under conditions that prevent their representation in conscious awareness never- theless evoked psychophysiological responses that reflect nonspecific emo- tional activation. Furthermore, the data suggest that the perceptual pro- cessing required for these effects have a subcortical origin, relying on a network that includes the superior colliculi, the pulvinar, and the amygdala (for a similar view, see de Gelder, Chapter 6, and Atkinson & Adolphs, Chapter 7). This system is an evolutionarily ancient one (e.g., Allman, 1999), and the perceptual analysis it can accomplish is necessarily crude. It is temporally prior to the cortical processing of facial features (inferior occipital gyrus) and full faces (involving the FFA, the superior temporal sulcus, and the inferior temporal cortex). Because of the rich efferent con- nections between the amygdala and cortical areas involved in visual pro- cessing in primates (Amaral, Price, Pitkänen, & Carmichael, 1992), the subcortical system could serve to tune subsequent cortical processing of the stimuli.

The observations suggesting that threatening and friendly faces are seg- regated for differential processing at an early, subcortical level of visual pro- cessing could be taken to imply that the system is tuned to critical features in

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these faces that decide whether they should be interpreted as threatening or friendly. Because the superior colliculus provides the most advanced visual information in the brains of reptiles and birds, evolutionary considerations, as well as the previously reviewed data, suggest that functionally significant information can be extracted at this nonconscious level of information pro- cessing. Furthermore, the remaining vision that is seen in blindsight patients may be accounted for by the processing of visual information in the superior colliculus and the pulvinar nucleus in the thalamus (de Gelder, Chapter 6; Weiskrantz, 1985). However, it is unlikely that faces are recognized as faces at this preliminary level. As a result, individual features should have a greater impact on producing differential nonconscious effects on emotional activa- tion. Finally, the functional advantage of this organization, which is presum- ably tuned to invariant features signaling one or the other facial emotion, is that the system can respond very quickly, alarming the amygdala to tune areas that perform further analysis of the input.

FACIAL FEATURES AND THEIR ROLE IN ATTENTION AND RECOGNITION

Critical Features for Recognition of Facial Emotion

Aronoff and coworkers (Aronoff, Barclay, & Stevenson, 1988; Aronoff, Woike, & Hyman, 1992) argued that there are general geometric properties in visual displays that carry critical information to determine the emotional valence of faces. For example, Aronoff et al. (1988) demonstrated that diag- onal lines were perceived as more negative than horizontal or vertical lines, as were lines with sharp angles rather than smoothly curved shapes, and oval shapes were perceived as more energetic than circular ones. They also demonstrated that ceremonial masks that were regarded as threatening and evil in different cultures contained a multitude of features that were per- ceived as negative when presented in isolation.

Inspired by the results reported by Aronoff et al. (1988), Lundqvist, Esteves, and Öhman (1999, 2004) constructed schematic faces that were used to systematically examine the role of eyebrows, eyes, and mouths in conveying threatening and friendly impressions of faces. Participants rated their emotional impression of each stimulus face by means of 11 semantic differential scales that were factor analytically grouped into dimensions of evaluation (here, negative evaluation), potency, and activity before being subjected to analyses of variance (ANOVAs).

Eyebrows emerged as the most important and influential facial feature for conveying threat. Whether presented in isolation, in basic configura- tions with only a mouth, or in complete facial configurations that included

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eyes and mouth, the shape of the eyebrows had a strong impact on emo- tional impression. ∨-shaped eyebrows conveyed a negative and threatening impression, whereas ∧-shaped brows provided a positive, friendly impres- sion. Data also showed that eyebrows presented outside a facial context can convey an emotional impression independent of a facial context (Lundqvist et al., 2004; cf. Aronoff et al., 1988, 1992). However, the effect of individual features was smaller when the feature was presented in isolation, and the effect of a feature was subordinate to the effect of the configuration. Thus eyebrows had basically no effect when placed under a mouth instead of above it. The upright basic eyebrows–mouth configurations (in the absence of eyes) conveyed threat as effectively as complete faces and predicted the emotional impression of complete faces.

Even though all examined facial features affected emotional impres- sion to some degree, the weight of their effects differed. Eyebrows had the most profound effect on emotional impression, followed in order by mouth and eyes. Figure 5.1 illustrates these findings using a two-dimensional emotional space defined by negative evaluation and activity. This space was subdivided into areas of threat and nonthreat by the shape of the eyebrows. These areas, in turn, were segregated into “scheming” and friendly areas on the basis of the mouth, and these areas were further subdivided by the shape of the eyes. In this way, faces with consistently threatening or friendly features were placed at opposite poles of the emotional space. These results are consistent with face-processing theories that postulate a sequential, hierarchical processing of facial features (Marr, 1982; Bruce & Young, 1986; Haxby et al., 2000). Even though isolated features (especially ∨-shaped eyebrows and ∪-shaped mouth) have some ability to convey emotional impressions outside a facial context, the placement of features in a configuration with other features in a face-like structure is decisive both for the quality and strength of the emotional impression of the face. Con- versely, placing features in a configuration deviating from normal faces (e.g., mouth above eyebrows) blocks the effect of the individual features.

The central role of ∨-shaped eyebrows in threatening faces and a ∪- shaped mouth in happy faces is further supported by data from image anal- yses of neutral, happy, and angry faces (Lundqvist, & Litton, 2004). Using the averaged Karolinska directed emotional faces (AKDEF; Lundqvist, & Litton, 1998) to analyze differences between emotional and neutral faces, the largest difference was found in the eyebrows/eyes area for angry faces, and in the mouth area for happy faces. Consistent with these image analy- ses, eye-tracking data from participants who freely viewed schematic threatening and friendly faces (unpublished data) showed that fixations were mainly directed to eyebrows and eyes for threatening faces, and to the mouth area for happy faces (see Figure 5.2).

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FIGURE5.1. Thetwo-dimensionalplotoveractivityandnegativeevaluationfortherat- ings of schematic facial stimuli shows how the stimuli form a hierarchy of clusters around different facial features. First, faces are subdivided according to the different shapes of eyebrows. Second, faces form subclusters around the different shapes of mouth. Finally, within these subclusters, there are formations of faces around the differ- ent shapes of eyes.

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FIGURE 5.2. Image analysis of pictorial facial stimuli highlights the importance of eye- brows for threatening faces and the importance of mouth for friendly faces. Eye-track- ing data show that visual attention is drawn to the eyebrow area on threatening faces, and to the mouth area on friendly faces.

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Searching for Threat among Schematic Faces

Because threatening animal stimuli have been demonstrated to recruit atten- tion very effectively in visual search tasks (Öhman, Flykt, & Esteves, 2001), visual search paradigms are good candidates for documenting behavioral effects of threat as conveyed by schematic faces. The first experiment used perceptually well-controlled schematic faces, based on the results reported by Lundqvist et al. (1999, 2004) to replicate a visual search experiment with real faces reported by Hansen and Hansen (1988; Öhman, Lundqvist, & Esteves, 2001). If a threat advantage could be demonstrated with these stim- uli, the next aim would be to determine if the critical facial features for threat delineated in the rating studies (Lundqvist et al., 1999, 2004) also would be effective in recruiting attention (Lundqvist & Öhman, 2005). Thus Öhman, Lundqvist, et al. (2001) used schematic threatening, friendly, and neutral faces to test the hypothesis that humans preferentially orient their attention toward threat. The design of threatening and friendly faces incorporated the most threatening and the friendliest versions of the facial features (eyebrows, mouth, and eyes) into threatening and friendly faces, respectively, that were presented as targets among neutral or emotional (e.g., friendly faces for threatening targets) distractor faces (see Figure 5.3).

Across a number of experiments, threatening faces were detected reli- ably faster and more accurately than friendly faces, irrespective of whether the target faces were presented among neutral or emotional faces. However, when all faces in a matrix were identical, the time and accuracy to decide that a target stimulus was not present did not differ between matrices of threaten- ing and friendly faces. The detection difference between threatening and friendly target faces was reliable across crowd sizes ranging from 4 to 25 faces (Öhman, Lundqvist, et al., 2001). Also, measurement of eye movements (Lundqvist & Öhman, 2004) showed that the eyes moved more directly, with shorter scan path and fewer fixations, toward a threatening than toward a friendly target among neutral distractors—which suggests that the former recruited attention more efficiently than the latter. Threatening angry faces were also detected faster and more accurately than other negative (scheming or sad) faces (Öhman, Lundqvist, et al., 2001), suggesting that the threat advantage can be attributed to the emotional impression of the face rather than to the differences in negative valence, uncommonness, or novelty among the different faces (cf. Whalen, 1998). The results show that, de- spite the basic physical–geometrical equality of schematic threatening and friendly faces, these facial stimuli affect attention differently. Whereas both types of faces were searched with equal efficiency in displays without a tar- get, threatening faces guided attention faster and more accurately than friendly faces when they were presented as targets.

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FIGURE 5.3. Visual search data reveal superior detection of a threatening target face, but equally efficient search of threatening and friendly crowds that are presented with- out any target.

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The Relation between Facial Emotion and Visual Attention

Lundqvist and Öhman (2005) used visual search tasks to examine which emotional facial features and configurations were necessary and sufficient to produce the observed advantage in target detection. Participants were exposed to visual search tasks in which target faces had one, two, or three features (eyebrows, eyes, mouth) that provided differential emotional infor- mation (threatening, friendly) in relation to neutral background faces. After the visual search task, participants were asked to rate the stimuli as a way to examine the relationship between the emotional impression of a face and the visual search performance.

Somewhat surprisingly (particularly from the perspective of the rating data reported by Lundqvist et al., 2004), the results showed that emotional eyebrows alone (with neutral eyes and mouth) did not produce a consistent threat advantage with neutral distractors, but that the mouth alone (with neutral eyebrows and eyes) did (Lundqvist & Öhman, 2005, Experiments 3 and 4). However, for conditions in which the eyebrows varied (i.e., carried emotional information), the overall detection times were considerably shorter and the hit rate was close to ceiling, suggesting that eyebrows had processing priority. Perhaps because of floor (detection latency) and ceiling (hit rate) effects, the efficient performance when eyebrows varied tended to give smaller threat advantages. If a threatening target face could be dis- criminated from the distractors via eyebrows, it was detected very effi- ciently with short response latencies (mean 660 milliseconds for all condi- tions involving changes in eyebrows) and high hit rates (98%). When the mouth was used to discriminate between target and distractor faces, targets were detected less efficiently with intermediate detection latencies (803 milliseconds) and hit rates (91%). Finally, if the discrimination could be made only via the shape of the eyes, the detection of targets was compara- tively inefficient, with slow detection latencies (839 milliseconds) and rela- tively low hit rates (86%).

Finally, a correlation analysis revealed a close relationship between emotion and attention measures. First, there were strong inverse relation- ships between detection latency and ratings of negative evaluation, activ- ity, and potency for threatening, but not for friendly, facial configurations (Lundqvist & Öhman, 2005). Second, the attentional threat advantage (i.e., the difference in detection latency between threatening and friendly faces in a given stimulus pair) correlated closely with the contrast be- tween these faces in emotion measures (see Figure 5.4). Thus a large dif- ference in emotion scores for a contrasted pair of threatening and friendly faces was associated with a large difference between these faces in atten- tion measures.

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FIGURE 5.4. Differences between threatening and friendly faces on attention measures follow the differences in the same faces on emotion measures. The code under each set of stimuli signifies which feature(s) conveyed the facial emotion: EB, eyebrows; EY, eyes; MO, mouth. RTs, response latencies.

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Taken together, the results from these experiments are consistent with the notion of a feature hierarchy that was initially observed in the rating studies. Furthermore, the results revealed a very close relation between emotion and attention measures, indicating that a threat advantage effect is closely linked to the emotional contrast between the compared stimuli.

The Role of Facial Features for Search of Faces

The apparent hierarchical relationship between eyebrows, mouth, and eyes may reflect the structural description (or feature detectors) underlying the recognition of facial emotion. In this case, the rank order effects of different features might be a consequence of the order with which features are matched to the specific structural description of a threatening/angry or friendly/happy face. Such an account would make a feature hierarchy an intrinsic part of the face-processing system. Alternatively, facial features might be differentially weighted according to how useful they are for dis- criminating emotions. Such a notion would locate the hierarchical feature effect in the stimulus itself. This notion was supported by the image analy- sis of pictorial emotional stimuli, which showed that the main change of information between a neutral and threatening face was found in the eye- brow region, and between a neutral and a friendly face in the mouth region (Figure 5.3). The priority of threatening faces would then result from the fact that a threatening face is more urgent to deal with than a friendly one.

The magnitude of the perceptual difference between an emotionally shaped feature (eyebrows, eyes, mouth) and the neutral control shape could be due to a nonemotional factor. However, even though target–distractor discriminability determines how faces are searched and discriminated (cf. Duncan & Humphrey, 1989), the close relation between attention and emo- tion suggests that the superior effect of threatening faces on attention is linked to the emotional rather than the perceptual properties of the facial stimuli.

Facial Emotion and Visual Attention: A Neural Model

The visual search data (Lundqvist & Öhman, 2005; Öhman, Lundqvist, et al., 2001) documented a strong association between emotional impression (e.g., high scores on negative evaluation) and efficient detection (short detection latencies and high hit rates). Moreover, the data indicated that the superior detection of threatening faces was closely related to the emo- tional contrast between the threatening and friendly configurations (Figure 5.4). These data indicate that the emotional impression of a facial stimulus regulates how that face affects attention. Such effects of emotion on visual

Caught by the Evil Eye 115

attention imply that the facial emotion of the schematic stimuli was recog- nized preattentively (for a similar view see de Gelder, Chapter 6; Atkinson & Adolphs, Chapter 7), and that the recognized emotional properties of a particular face determined how attention was directed to that face.

The emotion literature contains related evidence showing clear rela- tionships between the emotional significance of a stimulus and different psychophysiological response systems. Lang, Bradley, and Cuthbert (1997) showed that negative evaluation and activity reflect central motivational systems and signify a fundamental dimensionality that underlies human emotion. Their data showed strong positive relations between negative evaluation and EMG responses in the corrugator supercilii (the facial mus- cle mediating the eyebrow frown) and between negative evaluation and the magnitude of the startle reflex (measured by eye-blink responses to loud noises). Their data also revealed strong positive relations between activity (arousal) and skin conductance responses (Lang et al., 1997).

From this psychophysiological perspective, the more efficient at- tention to threatening compared to friendly configurations in our data (Lundqvist & Öhman, 2005; Öhman, Lundqvist, et al., 2001) may be inter- preted as reflecting a similar modulation of neural activity as that shown by the data of Lang et al. (1997). In theory, the neural representation of each facial configuration would thus be nonconsciously modulated according to that face’s emotional properties. Hence, a face conveying a threatening impression (e.g., high negative evaluation) would be modulated for en- hanced processing and thereby stand out more from the background and be easier to detect. Conversely, a friendly configuration (e.g., low negative evaluation) would be modulated to a lower, possibly even inhibited, level and thus stand out comparatively less from background information.

Figure 5.5 illustrates how the neural representations of threatening and friendly faces may be modulated according to their emotional signifi- cance. The figure describes data from the visual search studies (Lundqvist & Öhman, 2005; Öhman, Lundqvist, et al., 2001) and is based on models of visual perception (e.g., Marr, 1982; Gegenfurtner & Sharpe, 1999), face processing (Bruce & Young, 1986; Haxby et al., 2000), and visual attention (Wright & Ward, 1998; LaBerge, 1998, 2002). According to the models of Bruce and Young (1986) and Haxby et al. (2000), face processing works sequentially, with increasing complexity over serial, modular levels. First, a basic component analysis of facial information is performed, the outcome of which is used for any subsequent specialized facial processes, such as iden- tity and expression recognition. This core system then involves other neural structures, depending on task demands. Haxby et al. (2000) suggest that the basic, multipurpose extraction of facial information is carried out in the inferior occipital gyrus. The subsequent handling of facial emotional con-

FIGURE 5.5. A model of how emotion modulates attention. The model illustrates how attention initially is directed to the pretrial fixation cross (1). When an array of faces is presented (2), the faces are processed sequentially (3). After a basic, multipurpose extraction of facial features and properties (3a), the shape and position of facial features is matched to facial structural descriptions (3b), the outcome of which links the configu- ration to its emotional properties (3c). Emotion modulates the neural firing rates, repre- senting threatening and friendly configurations differently (4), resulting in quicker and more accurate detection of threatening configurations (4a) compared to friendly ones (4b).

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figurations is performed in the superior temporal sulcus. Finally, connec- tions between the superior temporal sulcus and the limbic system, foremost the amygdala, then link emotional properties to the facial configura- tion. However, the concept of a “low” subcortical route to the amygdala (LeDoux, 1996), the evidence for which was discussed earlier in this chap- ter (pp. 104–105), proposes that the amygdala is accessed even before, and can modulate initial processing in the visual cortex (this route is not illus- trated in Figure 5.5).

The involvement of the amygdala in recognizing emotion in facial stimuli, such as the schematic faces used here, is also supported by an fMRI experiment by Wright, Martis, Shin, Fischer, and Rauch (2002). They exposed participants to blocks of threatening, friendly, and neutral sche- matic faces and reported a significant increase in the activation of the left amygdala for both threatening and friendly faces, compared to a neutral face. There was also a significant difference in activation in the left occipitotemporal cortex (OTC) for threatening and friendly faces. These data imply that the speculated activity modulation of threatening and friendly faces takes place in the inferior occipital cortex (IOC) in the OTC. The fact that the significant difference in activity is found in the OTC (Wright et al., 2002) does not necessarily mean that the difference in neural activity is caused by that area, only that it is expressed there.

CONCLUDING COMMENTS

Evolution has equipped humans with an expressive face that is useful for producing a versatile repertoire of social signals. The development of this repertoire is predicated on the ability of conspecifics to quickly recognize and react appropriately to each signal.

The data reviewed in this chapter argue quite persuasively that humans possess a highly efficient system for recognition of emotional faces. This system allows humans to recognize and react to facial stimuli without conscious experience of the stimuli and prior to a conscious awareness of the stimuli. In the first section of the chapter (A Biological Perspective on the Human Face), we reviewed data that illustrate how emotional facial stimuli can be decoded and responded to even during experimental condi- tions that bypass conscious awareness, because conscious recognition is blocked by backward masking. In the second section of the chapter (Facial Features and Their Role in Attention and Recognition), we reviewed data that suggest that the direction of visual attention to emotional facial stimuli is regulated by a preconscious recognition of the emotional properties of the faces.

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These behavioral results can be accommodated by recent neural mod- els of perception and attention, in which the amygdala is added as a central structure for emotional evaluations. The argument presented in this chap- ter provides a psychobiological starting point for understanding the pro- cessing of emotional information in the face. The existing data are largely limited to facial signals of threat. There are also some interesting results suggesting that happy faces can have nonconscious effects on motiva- tion (Berridge & Winkielman, 2003; also see Winkielman, Berridge, & Wilbarger, Chapter 14), and that the recognition of happy faces is facilitated by a positive and impeded by a negative context, as provided by olfactory stimulation (Leppänen & Hietanen, 2003).

ACKNOWLEDGMENTS

This chapter is based on a doctoral dissertation (Lundqvist, 2003) presented to the Karolinska Institute by Daniel Lundqvist under supervision by Arne Öhman. The research was supported by grants from the Bank of Sweden Tercentennial Founda- tion to Arne Öhman.

NOTE

1. The differential involvement of the inferior temporal lobe and the STS in the processing of identity and expressions has also been demonstrated for the macaque monkey (see, e.g., Hasselmo, Rolls, & Baylis, 1989).

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UN No n C c Oo n N s c S i C o u I s O E U m S o A t i N o n D s E M O T I O N A L P R O C E S S I N G

CHAPTER 6 Nonconscious Emotions

New Findings and Perspectives on Nonconscious Facial Expression Recognition and Its Voice and Whole-Body Contexts

BEATRICE DE GELDER

In the early days of scientific psychology, the notion of unconscious infor- mation processing was much debated and controversial. The idea that our thoughts result from deliberations we are not aware of is no longer provoca- tive. But emotional information processing may still occupy a special niche in this changed and broadened intellectual landscape. The notion that our brain processes crucial emotional information outside of awareness seems to present a challenge for traditional Western notions of autonomy, the self, and free will. Not only are emotions even more personal and related to first-person authority than are cognitions, but emotion also has a special link with adaptive behavior and action. As a consequence, the very idea of unconscious emotional information leading straight to action may be a cause for concern.

The last decade has seen significant progress in the scientific under- standing of how emotional information is processed. By far, most research has focused on the recognition of facial expressions. There is now a growing consensus that facial expressions of emotion can be processed outside awareness. There is also increasing insight into the neural underpinnings of conscious and nonconscious recognition of facial expressions. Functional neuroimaging studies in both healthy subjects and brain-damaged patients

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1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

All the research reported and discussed in the chapter deals with perceptual processes, whether conscious or unconscious.

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

In distinguishing conscious and nonconscious emotions, we usually adopt a methodological criterion that defines what counts as purely perceptual process. This distinction between conscious and nonconscious is not important. Whether or not the observer is aware of the stimulus does not matter for the stage of processing in which we are interested. The obvious exception is, of course, affective blindsight. But this phenomenon is important because it has the power to reveal alternative processing routes.

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

From the methodological perspective just described, this distinction is not criti- cal. What counts is whether or not a perceptual process leads automatically and in a mandatory way to a representation. Subsequent perceptual elaboration often depends on consciousness, but our research is not about those later postperceptual cognitive processes.

converge to indicate that amygdala and orbitofrontal areas are activated by emotional faces, independently of voluntary attention and even without any awareness of the stimuli presented (Adolphs, 2002b; Breiter et al., 1996; Morris et al., 1996). Presumably, this primitive emotion system operates in- dependently of awareness and higher cognition; indeed, it is often referred to as the fast and automatic emotional processing route. The amygdala plays a central role in this basic emotional system. In addition to receiving input from various sensory systems, the amygdala may directly modulate the fusiform cortex to enhance the processing of salient face stimuli. A more controversial and challenging idea is that amygdala responses to emotional stimuli could be driven by subcortical inputs that are independent of pre- liminary analysis in the striate cortex and more anterior visual areas (Mor- ris, Friston, et al., 1998; de Gelder, 1999). This “low” route (as it is some- times called) conveys rather crude information based on a coarse parsing of a face stimulus; this crude information, in itself, is sufficient to trigger an emotional response. If conscious and unconscious processes have their own neural networks (LeDoux, 1992, 2000; see Edelman & Tononi, 2000, for a

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review), then it is theoretically possible that both routes interact and that conflicts can arise between conscious and unconscious processes. Such conflicts, in turn, can be seen against the background of the larger question regarding the role nonconscious emotional processes play in daily life.

The first part of this chapter reviews recent research on nonconscious recognition of facial expressions and discusses the most far-reaching con- ception of nonconscious emotion perception and its neural underpinnings. The second half is devoted to research that moves beyond the face and con- centrates on two contexts in which faces routinely appear in everyday life: the voice (expressions of emotion in the tone of voice) and the whole body (bodily expressions of emotion). This extended perspective draws attention to synergies between different emotional subsystems, with one subsystem specific for fear. It moves scientists away from a picture of nonconscious emotion as dominated solely by vision toward a more embodied notion of emotion processing and cognition, which could be integrated with the research on emotional experience, not discussed here. In this sense, my final conclusions about the importance of action and simulation in emotion processing are consistent with those suggested by several contributors to this volume (e.g., Niedenthal, Barsalou, Ric, & Krauth-Gruber, Chapter 2; Barrett, Chapter 11; Prinz, Chapter 15).

Within the limits of the chapter we cannot address fundamental ques- tions on the nature of emotion and consciousness. When relevant, specific implications of the research for the big issues of emotion and consciousness will be noted. Instead, I will build a case for the hypothesis that emotional information, like any other kind of information that impinges on the sen- sory systems, is processed at the perceptual level in an automatic and man- datory way. In this chapter I do not use the term emotion to refer to a spe- cific type of response, such as a behavior or a coordinated packet of behaviors, feeling, facial movements, physiology, etc., as in traditional defi- nitions of emotion (de Gelder & Bertelson, 2003; see also Barrett, Chapter 11). Instead, the research discussed mainly focuses on automatic percep- tual processing of emotional signals. Within this perspective of the research on perception of emotional signals presented here, there is no compelling reason for making a distinction between absence of consciousness and absence of awareness. I therefore use these two notions interchangeably.

NONCONSCIOUS RECOGNITION OF FACIAL EXPRESSIONS

Facial expressions are, by far, the most prominent emotional objects studied in the emotion literature. This state of affairs is related as much to the wide- spread use of the stimulus set provided by Ekman and Friesen as it is to the

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prominence of facial expressions in social communication. Among the facial expressions that have been studied thus far, researchers have targeted fear. During the past decade there has been an avalanche of neurobiological studies linking the amygdala to the processing of facial expressions of fear (see Zald, 2003). To date, the link between the amygdala and fearful faces has guided the cognitive neuroscience agenda for conducting research on emotion. A number of studies has tackled the question of the role of the amygdala in nonconscious recognition of fearful facial expressions, follow- ing the first reports (Breiter et al., 1996; Morris et al., 1996).

Over the last decade, two different sets of results have converged on the notion that emotional information, in general (and fear expressions, in particular) may be processed without awareness (see also Lundqvist & Öhman, Chapter 5; Atkinson & Adolphs, Chapter 7). One set belongs to the tradition of defining the conscious versus nonconscious distinction in terms of attention. The other set of results examines noncortically based visual abilities. For the sake of clarity, I refer to these two different meanings of nonconscious emotions and the underlying differences in scope and expla- nation as unattended versus unseen. In the final sections I relate this dis- tinction to the contrast I propose between visual emotion perception and visual emotion cognition.

Facial Expressions Processed without Attention

Over the last decade studies using various methods such as priming, pop out, inattentional blindness, redundant target presentation, and masking have provided evidence for nonconscious face recognition. The majority of studies are linked in some way to theories of attention, either directly, as when a specific model of attention is tested, or indirectly, as when spe- cific attentional deficits (e.g., hemi-neglect—not paying attention to stimuli in the visual field contralateral to the lesion—or extinction) are investi- gated. Models of attention come in many varieties, but for the present pur- pose they all have in common the idea that nonconscious perception is related to availability of processing resources. When no attention is allo- cated to a stimulus, the information is not processed, or at least not pro- cessed sufficiently to sustain object recognition (Lavie, 1995; Treisman & Gelade, 1980). Patients suffering from hemi-neglect (i.e., a condition pre- dominantly following damage to the right parietal cortex, whereby the patient no longer pays attention to his or her left visual field) or extinction (a condition with an etiology similar to neglect, whereby the patient attends to left-hemispace stimuli in the absence of right-hemispace stimuli but ignores the stimulus to the left when the right stimuli is presented simulta- neously) provide an interesting opportunity for assessing the role of at-

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tention in the processing of facial expressions (Vuilleumier, 2000). As predicted, the emotional significance of faces does influence spatial atten- tion during visual processing, thereby reducing neglect in brain-damaged patients with unilateral inattention. Faces may capture attention and over- come extinction, in part, because of their special biological status as well because of the highly automatized perceptual processing that is activated.

Research on nonconscious perception that manipulates attention suf- fers from the problem that attention is a relative notion, making the conclu- sive interpretation of results somewhat difficult. It is difficult to find a task that objectively measures the degree to which a stimulus occupies the observers’ attention, because attention is difficult to quantify. An upper or a lower limit cannot be fixed in absolute terms. For example, based on their own results using functional magnetic resonance imaging (fMRI) in normal controls, some researchers have argued that, consistent with observations in animals, unattended stimuli do not produce a neural response (Pessoa, McKenna, Gutierrez, & Ungerleider, 2002), suggesting that they are not processed at all. Yet this area is a matter of hot debate. Recent studies have shown selective fluctuations in the network of attention (e.g., subcortical vs. cortical components), wherein some components are sensitive to atten- tional fluctuations, and others are not. These findings suggest that the arousal aspect of a face, in addition to its intrinsic valence, may also influ- ence how it is processed (although see Charland, Chapter 10, on the idea of intrinsic valence).

To try and avoid the problems associated with manipulating attention, research on the nonconscious recognition of emotion has used visual mask- ing techniques to block stimulus awareness (i.e., the faces of interest are unseen by the participants, who only consciously register the mask). Masking not only ensures that the face of interest is not consciously per- ceived, but it also interferes with the normal processing of that face in the visual cortex. Backward masking is thought to interfere with the specific role played by the primary visual cortex in the elaboration of a percept after initial stimulus encoding (Bullier, 2001). Studies using this technique have shown that when confronted with a backwardly masked, hence unseen, angry face, the observer nevertheless gives a reliable skin conductance response (Esteves, Dimberg, & Öhman, 1994). Facial expressions of fear increase the activation level of the amygdala, an effect that is lateralized as a function of whether or not the observer can perceive the faces con- sciously: right amygdala for unseen, left for seen masked presentation (Morris, Öhman, & Dolan, 1998). Faces displaying fear expressions fol- lowed by a backward mask lead to increased activities among the right amygdala, pulvinar, and superior colliculus (although see Atkinson & Adolphs, Chapter 7, on the consistency of this lateralization effect). This

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result and subsequent ones clearly suggest the existence of a primitive pro- cessing route for fear faces that functions independently of stimulus aware- ness.

It has been argued that presenting backwardly masked stimuli creates in normal viewers a situation that is functionally equivalent to that which exists in patients with a lesion in the primary visual cortex or hemianopia (Macknik & Livingstone, 1998). An important difference between back- ward masking and striate cortex lesion is that in the latter case, the primary visual cortex is no longer able to receive initial input whatsoever. Because subcortical structures are normally intact in these patients, they present a unique opportunity for assessing residual visual abilities when the primary visual cortex is destroyed. These patients can discriminate some elemen- tary visual stimulus attributes of visual stimuli projected to their blind field, a phenomenon called blindsight (Weiskrantz, 1986, 1997). Residual vision for emotional stimuli such as facial expressions is referred to as affective blindsight (de Gelder, Vroomen, Pourtois, & Weiskrantz, 1999). In studies of affective blindsight, patients are instructed to make guesses about a stim- ulus because they are not able to see that there is a stimulus present. This method provides researchers with a clearer instance of unconscious per- ception (when compared to studies that simply manipulate attention) because patients are literally not able to see that there is a stimulus present (Weiskrantz, 2001). Although absence of awareness makes for a comparable experience in neglect and blindsight patients, intact sensory processes in the former, but not in the latter, make their situation very different. As a result, studies of blindsight patients are extremely useful in understanding the role of nonconscious perception of facial expressions.

Affective Blindsight: Radical Nonconsciousness of Facial Expressions

Research on blindsight patients confirms that the primary visual cortex is not essential in processing visual emotional signals or in combining unseen emotional signals with auditory ones. My collaborators and I have shown that patients with lesions in the striate cortex had residual nonconscious vision for facial expressions and were able to discriminate between facial expressions they could not see and were not aware of (de Gelder, Vroomen, et al., 1999; de Gelder, Vroomen, Pourtois, & Weiskrantz, 2000). More recently, Hamm and collaborators (Hamm et al., 2003) classically condi- tioned a person with bilateral loss of the striate cortex to a visual stimulus. The subject was completely blind (both behaviorally and experientially), yet responded to a visual stimulus that had been paired with an electric shock. These results are consistent with the notion that masked facial expressions are processed in normal subjects via a subcortical pathway

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involving the right amygdala, pulvinar, and superior colliculus. In contrast, processing of consciously seen faces increases connectivity between fusi- form and orbitofrontal cortices (Morris, de Gelder, Weiskrantz, & Dolan, 2001).

The findings of blindsight have been controversial. Some older objec- tions to the phenomenon are now irrelevant, thanks in part to the use of new technologies. First, the possibility that the remarkable visual abilities of cortically blind patients were due to an island of intact striate cortex or to light scattering has been definitively laid to rest by findings from brain imaging: Structural scans show that there is no intact striate cortex in these patients (Barbur, Watson, Frackowiak, & Zeki, 1993; Cowey & Stoerig, 2004).

The interesting questions are: How effective is blindsight, and what visual functions do these different pathways sustain? We know from studies in both monkey and human blindsight patients that residual discrimination of color and movement is possible, but both forms of discrimination are quantitatively and qualitatively different from the normal situation. For example, one may argue that facial expressions are too subtle and complex to survive striate cortex damage. But it is clear from recent research that subcortical structures play a crucial role in the processing of unseen faces (whether due to lesions in the striate cortex or to backward masking). Infor- mation from the retina is sent, via the superior colliculus, to the thalamic pulvinar nucleus and on to the amygdala, where the visual information is coded for its emotional significance. This action occurs in the absence of cortical activity (for a similar argument, see Atkinson & Adolphs, Chapter 7). Research on residual vision of facial expressions of fear provides support for the model that, in animals, fear reactions to auditory stimuli can be accounted for by two separate pathways (LeDoux, 1992). This dual-route approach has gained acceptance among emotion researchers as a general model of emotion processing (e.g., Adolphs, 2002b).Yet many details about its anatomical and functional implementation are still lacking. Although there is clear evidence from animal research of a noncortical route in audi- tory processing (LeDoux, 1992), clear-cut anatomical evidence of the corre- sponding situation for visual processes in humans is still lacking. Neverthe- less, there are several reasons to assume that this route exists.

First, facial expressions should be among the most likely candidates for non-striate-based perception. Many types of information provided by the face are indeed rather subtle, such as age, gender, trustworthiness, attrac- tiveness, and, most obviously, personal identity. These sources of informa- tion are processed with contributions from multiple cortical brain areas. Yet facial expressions of emotion can be recognized even when stimuli are much degraded. For example, using images with spatial frequencies below 8 cycles filtered out, the emotional expression on a face (but not the per-

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son’s identity) can still be recognized almost faultlessly (Morrison & Schyns, 2001; Vuilleumier, Armony, Driver, & Dolan, 2003). This range of spatial frequencies corresponds to the range within which patients with a striate cortex lesion can still discriminate visual patterns, indicating that processing facial expression is within the range of the visual abilities sus- tained by a subcortical route.

Second, the subcortical route is comparatively faster than processing in the occipitotemporal cortex. And facial expressions of emotion can be processed, at least at some level, very quickly. Evidence for this speed comes from recordings of event-related potentials (ERPs), magnetoen- celography (MEG), and to some extent, single-unit recordings. Facial expressions of emotion begin to be distinguished at 80–110 millisec- onds poststimulus, with the signal located in the midline occipital cortex (Halgren, Raij, Marinkovic, Jousmaki, & Hari, 2000; Pizzagalli, Regard, & Lehmann, 1999; Streit et al., 1999). Activity at around 160 milliseconds is seen in the fusiform gyrus and superior temporal sulcus and corresponds to the time window of the N170, a negative wave form occurring at around 170 milliseconds and associated with the structural encoding of faces (but also bodies; Stekelenburg & de Gelder, 2004). We observed that the emo- tional content of faces affected the left N170, the occipitoparietal P2, and the frontocentral N2 (Stekelenburg & de Gelder, 2004). So far, all these studies concern cortical sources of activity and, as such, do not provide sup- port for a subcortical route in emotion face processing. Recordings from the amygdala in animals and in humans suggest that the earliest activity is around 220 milliseconds (Streit et al., 1999), which is later than the occipi- tal signal. But, interestingly, one study using single-unit recording in a patient reported discrimination between faces and scenes expressing fear or happiness in the orbitiofrontal cortex after only 120 milliseconds (Kawasaki et al., 2001). This latency is suggestive of a direct subcortical route from the amygdala to the orbitofrontal cortex. More recently, signifi- cant differences were found between emotion and neutral face conditions for peak amplitudes and latencies throughout the whole network of brain structures involved in emotion. The earliest peak of activation located in the calcarine sulcus (or primary visual cortex) appeared around 90 millisec- onds and showed specificity to upright faces, which cannot be attributed to the low-level features of the stimulus (Meeren, Hadjikhani, Ahlfors, & de Gelder, 2005). The second peak of activation was stronger for meaningful stimuli, in general, but faces, in particular, elicited the strongest amount of activation. These findings suggest that the early visual areas do not merely process the physical features of the stimuli but are an intricate part of the face recognition network. The most interesting suggestion comes from the various time-course data that include evidence for biphasic face activity and current models of conscious and nonconscious cortically based and

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noncortically based processing routes. Unfortunately, the methods that pro- vide highly specific information about time-course, such as ERP and MEG, do not allow direct inferences about subcortical structures.

In summary, at present the evidence for a functional role of a direct subcortical route for visual emotion signals in humans is still mostly indi- rect, with the strongest arguments provided by studies of blindsight, the points raised above, and the behavioral and brain-imaging data from unseen faces.

Reciprocal interactions between the visual system, other sensory sys- tems, and the motor system open the possibility that visual deficits in the primary visual projections to the striate cortex may be compensated for not only by alternative visual pathways but also by links between these alterna- tive visual pathways and, for example, the motor system. A relevant exam- ple is provided by the superior colliculus–putamen link that sustains orien- tation behavior. An important role of the superior colliculus in emotional perception may be directly related to its functional anatomical properties. The superficial layers of the superior colliculus consist of neurons that have predominantly visual properties, whereas the deep layers contain sen- sorimotor neurons. Superficial to deep-layer projections provide spatially ordered visual signals directly to the superior colliculus neurons that are involved in coordinating sensory inputs with motor outputs (Doubell, Skaliora, Baron, & King, 2003).

Visual perception can be achieved by the standard visual route, based on the lateral geniculate nucleus and projections to the primary visual cor- tex. However, it may or may not involve conceptual knowledge of the stim- ulus, memory, and influence from context (e.g., see Niedenthal et al., Chap- ter 2; Atkinson & Adolphs, Chapter 7; Barrett, Chapter 11; Prinz, Chapter 15). Yet even the enriched visual perception system does not operate in iso- lation. The visual system has direct links with the motor system, as shown by studies on action representation, of which the observations of mirror neurons are the most widely known (Grèzes & Decety, 2001). Our own research (de Gelder et al., 2004) has shown that a three-way modulation of the visual areas of the brain, the structures that comprise the emotional sys- tem of the brain, and the motor systems is the most noticeable when sub- jects watch fearful, as contrasted with happy or neutral, body movements, as I discuss below.

It has also been noted that dim visual abilities may be enriched in other ways than through contributions that improve the visual signal. There is increasing evidence that other phenomena accompanying visual percep- tion without awareness may be more important in nonconscious visual per- ception. During testing, patients with blindsight sometimes report feeling that a stimulus is present without having any visual experience (Weiskrantz, 2001). This report is consistent with the notion that processing of emotional

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signals is associated with changes in bodily states during the early stages of emotion processing (Damasio, 1999), perhaps producing something like a primitive core affective state (see Barrett, Chapter 11) Affective blindsight may be related, in part, to a patient’s interoceptive access to his or her bodily reactions to unseen stimuli. I have considered this possibility previ- ously (de Gelder, Vroomen, et al., 2000). Other mechanisms, such as sensorimotor correlates of mandatory eye movements toward a target in the blind field, may help explain the puzzling finding that G.Y. (a patient with a unilateral hemianopia) performed above chance in a gender-decision task (Morris et al., 2001). In keeping with the limited range of spatial frequen- cies within which the superior colliculus–putamen pathway is functional, purely visually based gender discrimination, in itself, seems to less likely, although male and female faces might have different reward functions, and reward mechanisms may, in turn, supplement poor subcortical visual dis- crimination abilities.

Emotional Conflict Situations without Awareness of Conflict

The notion of partly independent processing streams for consciously and nonconsciously perceived emotional stimuli allows for the possibility of interactions between the two. Patients with unilateral visual cortex damage provide a unique occasion to explore this intriguing processing conflict, because it is possible to present simultaneously two stimuli (left and right of central fixation) under circumstances where there is no visual awareness of one or the other stimulus. Interhemispheric cooperation or conflict can be manipulated by manipulating whether the two stimuli carry the same or different emotional significance (de Gelder, Pourtois, van Raamsdonk, Vroomen, & Weiskrantz, 2001). One experiment used chimeric faces (con- sisting of two half-faces presented to each visual half-field). A second exper- iment simultaneously presented two full faces to the right and left visual fields. The stimulus presented in the contralesional field was perceived in patients with striate cortex damage, yet we also obtained clear evidence that the stimulus presented in the blind field influenced the emotional cat- egorization of the stimulus seen in the intact field, as shown by lower per- formance in the emotion–face categorization of faces presented in the good field that were accompanied by an incongruent facial expression presented to the blind field.

Imaging studies contribute to our understanding of the neural archi- tecture underlying the interactions between processing seen and unseen faces. Interhemispheric congruence effects between seen and unseen facial expressions modulate brain activity in the medial prefrontal cortex, supe- rior colliculus, amygdala, and fusiform cortex (de Gelder, Morris, & Dolan, 2005). First, the overall congruency effects reflected in the medial pre-

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frontal cortex indicate that there is an interaction between overt, conscious and covert, unconscious processing. The increase in activity for congruent, as opposed to incongruent, pairs in the medial prefrontal cortex is consis- tent with the role of this area in behavioral regulation (Bechara, Damasio, Damasio, & Anderson, 1994) more than in specific emotion-related infor- mation processing. The prefrontal cortex has been shown to govern the top- down control of behavior, executive functioning, higher-level emotional processing, and conscious behavioral control (Dolan et al., 1996; Dolan, Fletcher, McKenna, Friston, & Frith, 1999; Miller, 2000; Miller & Cohen, 2001). In particular, the ventral medial prefrontal cortex receives sensory information from the body and the external environment via the orbito- frontal cortex and is connected with the amygdala and the ventral striatum (Bechara et al., 1994), suggesting its role in the integration of emotional and cognitive processes (by incorporating visceromotor signals into decision- making processes). By presenting facial expressions simultaneously to the two visual fields, neural processes in subcortical structures related to an interaction between conscious and nonconsiously recognized images can be investigated. The presence of unseen fear faces has an influence on how consciously recognized fear or happy faces and fear or happy voices are perceived. Our results indicate that here also emotional congruency be- tween visual and auditory stimulation led to enhancement in amygdala and superior colliculus activity for blind relative to intact field presentations. By comparing voice–face and voice–scene pairs, we were able to assess that the effect of unseen visual information on emotional voices is specific to faces and not with affective pictures. Our findings indicate that processing fear in the human face is mandatory and independent of awareness and that it remains robust even in the light of concurrent incongruent emotional information whether provided by a facial expression or an emotional voice of which the observer is aware. At the functional level, this asymmetry sug- gests that the integration between perception and behavior may be differ- ent as a function of whether the organism is engaged in automatic-reflexive or in controlled-reflective fear behavior. This asymmetry may mirror psy- chological reality: Our unconscious desires, anxieties, etc., influence our conscious thoughts and actions, but we cannot simply “think away” or remove our unconscious fears.

BEYOND THE FACE: EMOTIONAL CUES FROM VOICES AND BODY MOVEMENTS

Laboratory investigations of affective processes in humans tend to focus on one sensory system at a time—and most often, the visual system. The majority of studies focuses on affective information that can be gleaned

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from the face. In daily life, however, visual emotional signals from the face are usually accompanied by other information. Context influences how we see a facial expression (for a discussion, see Barrett, Chapter 11). The natu- ral scene context in which a face appears has some influence on how it is perceived and how well it is remembered afterward. We investigated the role of natural scenes with affective meaning on the N170 (an electro- encephalographic [EEG] wave selectively sensitive to faces, presumably reflecting the initial stage of face encoding and related to activity in fusiform cortex). We predicted that embedding facial expressions in an affective picture context would significantly modulate the N170, because viewing faces in the context of emotional scenes would trigger amygdala activation, which in turn would lead to increased activation of the fusiform cortex. Indeed, the results indicated that face expression and affective meaning of the scene interacted to generate the highest N170 amplitudes for the combination of fearful faces and fear-inspiring scenes (Righart & de Gelder, 2005). Our preliminary data also indicate an effect of natural scenes on memory for faces with a detrimental effect of fear-inspiring scenes on subsequent recognition of person identity.

In daily life, visual perception of the face is usually accompanied by signals from other sensory modalities. Multisensory emotion integration is particularly relevant for the issue of nonconscious emotional processing, because it is an automatic, mandatory process. People integrate information from multiply sensory channels even when they are unaware of the inputs or devote little conscious attention to integrating them. An increasing num- ber of studies provide evidence that integration of information across dif- ferent sensory modalities is a powerful mechanism for increasing adaptive responses (de Gelder & Bertelson, 2003). In the next section we discuss research that has expanded beyond face recognition research to consider expressions of emotion in the voice and whole body.

Emotional Voices

In contrast to the wealth of studies that explore the processing of facial expressions, there have been relatively few attempts at identifying the spe- cific neural sites for processing emotions in the voice (see Buck, 2000, for a review; George et al., 1996; Scherer, 1995). Some studies have investigated common processing resources and overlapping brain structures for face and voice expressions (Borod, Tabert, Santschi, & Strauss, 2000; Royet et al., 2000). Insights into the neurobiological basis of voice processing are also based on neuropsychological findings (Adolphs, Damasio, & Tranel, 2002). For example, impaired recognition of emotional prosody is associ- ated mostly with damage in the right frontal cortex, but also suggests a role

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of the temporal pole. The issue of common brain structures for processing emotional signals provided by different sensory systems has mainly been addressed by looking for correlations between emotional processing in dif- ferent sensory channels. For example, parallel impairments were observed in recognition of fear in the face and in the voice in patients with amygdalectomy (Scott et al., 1997; but see Anderson & Phelps, 1998). Right-brain-damaged patients were impaired in tasks of emotional percep- tion that involved facial, prosodic, and lexical stimuli. Yet to understand fully how the brain combines multiple sources of affective information, it is not sufficient to combine results obtained in studies that have investigated visual and auditory emotion perception separately. The issue of multi- sensory integration is altogether a different one from that of merely looking for common processing resources, because it concerns the online integra- tion of the two sensory sources.

Perceiving Emotion in Face and Voice

Facial expressions of fear, anger, or sadness naturally go together with spe- cific properties of the voice (for an alternative view, see Owren, Rendall, & Bachorowski, Chapter 8). People are quite confident that the shrieking voice they hear emanates from a face expressing fear rather than from one exhibiting a smile, as any parent watching children in a playground can tes- tify. The ability to associate the emotional expression of a voice with accom- panying visual information from the face seems to occur effortlessly and to be largely automatic. We have investigated a number of multisensory situa- tions involving perception of emotional signals and argued for automatic binding of fear expressed in a face with fear present in a voice (for an over- view, see de Gelder, Vroomen, & Pourtois, 2004).

Patients suffering from visual agnosia, which sometimes also includes an inability to recognize facial expressions of emotion, present a good opportunity for investigating the cross-modal processing of emotional information in faces and voices. We studied patient A.D., who has visual agnosia with severe face recognition problems due to bilateral occipito- temporal damage (de Gelder, Pourtois, Vroomen, & Bachoud-Levi, 2000). Her recognition of facial expressions of emotion is almost completely lost, whereas her recognition of emotions in the voice is intact. This combina- tion allowed us to examine her perceptual abilities within a cross-modal bias paradigm. In the critical experiment she was asked to rate the emotion expressed in short spoken fragments while watching the facial expressions appearing on the screen. The evidence clearly indicated that the presenta- tion of facial expression stimuli significantly influenced A.D.’s recognition of emotions in the voice, suggesting that she was able to process the facial

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expressions at a covert level that contributed to her ability to recognize emotion in vocal stimuli (de Gelder, Pourtois et al., 2000).

In other studies, the time-course of the integration between an affec- tive tone of voice and facial expression was examined using ERP signals that track the processing of unexpected changes in the properties of audi- tory stimuli (whether in intensity, duration, or location). In the majority of trials, subjects were simultaneously presented with congruent facial (e.g., fearful) and vocal expressions. In the deviant trials, however, the voice was accompanied by an incongruent facial expression (e.g., a fearful voice and happy face). As predicted, we found a change in the auditory ERP as a function of a change in the visual component of the stimulus pair, indicating that the perceptual system was sensitive to the combination of these inputs rather than to the auditory one alone. We replicated this finding in a subse- quent study, by showing that congruent facial/vocal stimuli (e.g., a sentence fragment spoken in an emotional tone of voice paired with a facial expres- sion) gave rise to an increase in the amplitude of auditory evoked potentials (Pourtois, de Gelder, Vroomen, Rossion, & Crommelinck, 2000). A third study (Pourtois, Debatisse, Despland, & de Gelder, 2002) suggested that the processing of affective prosody is delayed when there is an incongruent facial expression present. Source localization indicated activation in the anterior cingulate cortex, an area selectively implicated in processing con- gruency or conflict between stimuli (Cabeza & Nyberg, 2000; MacLeod & MacDonald, 2000). The anterior cingulate cortex is not normally consid- ered a multisensory processing area, but it is one of the areas associated with the processing of human motivational and emotional cues and with detection of error (Mesulam, 1998). Results indicated that adding visual affective information to the voice translates as an ERP amplitude increase of early auditory evoked potentials, an effect that obtains for both naturalis- tic (voice–face) and semantic (voice–affective picture) pairings in the intact field, but is only observed for the naturalistic pairings in the blind field (de Gelder, Pourtois, & Weiskrantz, 2002). Taken together, these four studies converge toward the conclusion that when emotional cues from the face and the voice are present, they influence each other rapidly and automati- cally. This conclusion does not imply that each stimulus is consciously per- ceived, that the observer is aware of their congruence, or that their integra- tion proceeds in a deliberate manner.

The study of cortically blind patients allows the possibility of investi- gating intersensory integration of affective information with seen and unseen faces. We investigated the neural correlates of audiovisual integra- tion when subjects categorize a facial expression while listening to an emo- tional voice (Dolan, Morris, & de Gelder, 2001). Participants were scanned while hearing a happy- or a fearful-sounding voice paired with either a con-

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gruent or an incongruent facial expression. Their task was to judge the facial emotion. When a fearful face was accompanied by a fearful voice, activation level in the amygdala and the fusiform gyrus increased. No such effect was observed when the voice and the face expressed conflicting emo- tions or when both expressed happiness. Interestingly, in contrast to our behavioral studies in which we observed that this cross-modal influence occurred equally for both “fearful” and “happy” pairs, no such increase in activation was observed for the latter. Further research is required to estab- lish whether this reflects the different ecological importance of happy and fearful emotions.

Expressions of Emotion through Body Movements

At present, we know much less about how the human voice conveys emo- tion when compared to the human face. Even less is known about the emo- tional signals provided by the human body. Historically, body movements have frequently been analyzed as potent emotional signals. In his treatise on physiognomics, Aristotle remarked that the body as a whole signaled a person’s emotional states and that facial expressions and intonations of the voice were part of a whole organism. In the 19th century German and Dutch expression physiologists and psychologists promoted the study of body expressions. Continuing initial explorations by Bell, Gratiolet, and Duchène de Boulogne, Darwin (1872/1998) described in detail the body expressions associated with emotions in animals and humans and proposed principles underlying the organization of these expressions. In his view, the expression of an emotional state by movements of the whole body is to be viewed as a simulation of the action normally associated with the emotion expressed. In view of the current usage of the term mental simulation (e.g., Niedenthal et al., Chapter 2), it should be noted that Darwin’s view did not postulate a mentalist stage at which this simulation is initiated (as com- pared with James’s ideomotor theory; James, 1890).

In general, there have been few scientific studies of emotion percep- tion based on the bodily movements in others. The few occasional reports assessed recognition of body emotions in normal adults (Ekman & Friesen, 1976). Developmental data suggest that observation of bodily behavior is a better indicator of reaction to surprise than is facial expression (Camras et al., 2002). For a discussion of these findings and others, see Atkinson & Adolphs (Chapter 7).

Recently my colleagues and I initiated research on the functional and neural basis of whole-body expressions of emotion. Our findings indicate some similarities to the way that posed facial expressions are processed. First, we found that perceptions of whole-body expressions are processed

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configurally (as are emotion expressions on the face) and showed the famil- iar inversion effect and context effects (Stekelenburg & de Gelder, 2004). These results are consistent with configural perception of neutral body pos- tures (Reed, Stone, Bozova, & Tanaka, 2003) as well as with studies of bio- logical motion indicating that the global structure of whole-body movement is perceived, and that perception is not interrupted by anomalies in local relations (Berthental & Pinto, 1994; Grèzes & Decety, 2001; Grèzes et al., 2001).

Second, we found that perceptions of whole-body expressions produced neural activations that are similar to those seen in face perception. Exposure to body expressions of fear, compared to neutral body postures, activates the fusiform gyrus and the amygdala bilaterally (de Gelder, Snyder, et al., 2004). In the emotion literature these two areas have predominantly been associ- ated with face processing (Adolphs, 2002a, 2002b; Kanwisher, McDermott, & Chun, 1997; Morris, Friston et al., 1998). These findings are consistent with those from studies of biological motion that used dance-like movements rep- resented by point-light displays contrasted with randomly moving dots. The biological movement patterns were experienced as pleasant and activated subcortical structures, including the amygdala (Bonda, Petrides, Ostry, & Evans, 1996), consistent with results indicating that the role of the amygdala in recognizing emotion is not restricted to faces. A further finding of related interest is that visual perception of biological motion activates two areas in the occipital and fusiform cortices (Grossman & Blake, 2002). This result goes in the same direction as the preceding one, in the sense that it indicates that areas hitherto best known for processing faces are also involved in processing properties associated with human bodies.

Subjects were presented with short blocks of body expressions of fear alternating with blocks of images of emotionally neutral but meaningful body gestures. The face was blurred in all images to avoid confounds due to the facial expression. The results indicated that although the processing of emotional information from faces and bodies is somewhat similar, emo- tional bodies generate activity in a whole network of areas more compre- hensive than the visual system (de Gelder, Snyder, et al., 2004). The major finding of this study is the existence of condition-specific activity associated with seeing fearful bodily expressions, as compared to neutral but meaning- ful body actions. A similar comparison for happy bodily expressions did not yield a result that was anywhere comparable. Foci of activity were located in areas involved in stimulus detection and orientation (e.g., in the superior colliculus), in visual areas so far mostly associated with the processing of fearful face expressions (e.g., amygdala and fusiform cortex). Passive view- ing of still images of bodily expressions activates areas in the occipito- parietal pathway, predominantly the supplememtary motor area, cingulate

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gyrus, and middle frontal gyrus, which have been observed in studies of voluntary imitation (Decety et al., 1997; Passingham, 1996) and suggests that passive viewing can initiate motor preparation. This finding would seem particularly important in view of the Darwinian notion that the role of emotions is to facilitate adaptive action.

In the same study we also observed activity in the putamen and caudate nucleus in subjects viewing bodily expressions of fear. Both the caudate nucleus and putamen are predominantly known for their involve- ment in motor tasks but have also been associated with motivational– emotional task components. The caudate and putamen are damaged in Huntington’s and Parkinson’s diseases, which are both characterized by motor as well as emotion deficits. Although the nature of the relation between the emotional and the motor disorders is not yet fully understood, preliminary data indicate that these patients have a significant impairment in recognition of whole-body expressions of emotion (de Gelder, van den Stock, de Diego Balaguer & Bachoud-Levi, 2005).

Taken together, the available evidence suggests that the integrated activity in processing bodily expressions of fear may constitute a mecha- nism for fear contagion. This possibility is consistent with the view that simulating an emotion may be the basis upon which emotion is perceived (see Niedenthal et al., Chapter 2; Atkinson & Adolphs, Chapter 7; Barrett, Chapter 11; Prinz, Chapter 15). Most importantly, the preparation for action in response to fear seems to operate in a direct, automatic, and noninferential fashion in fear perception.

Emotional Synergies: Combining Faces and Bodies

In natural situations, a particular body expression is most likely to be accompanied by a congruent face expression. It is also well known from animal research that information from body expressions can play a role in reducing the ambiguity of facial expression (van Hoof, 1962). Moreover, it has been shown that observers’ judgments of infants’ emotional states de- pend on whole-body behavior more than on facial expressions alone (Camras et al., 2002). My colleagues and I have begun to explore the issue of synergies between facial expressions and bodily expressions of emotion using behavioral methods and EEG measurements. In one study we used a paradigm of categorical perception (reminiscent of the cross-modal studies in which we explored the influence of an emotional voice expression on a face) to assess how emotionally congruent or incongruent bodily expression influences the accuracy and speed of face categorization (Meeren, van Heynsberger, & de Gelder, 2005). The results of this experiment were very consistent with those found in studies of face–voice interactions: The way

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in which observers rated the facial expression was clearly influenced by the emotion expressed in the body, to which they were not paying attention.

CONCLUSIONS

For many years emotion researchers have been occupied with crucial issues regarding what emotions are, how they are perceived, how the sender intends them, and whether or not there are basic emotions. For the present-day cognitive psychologist, there is nothing shocking about the idea that unconscious processing assists our conscious mind from behind the curtains of awareness. It is generally agreed that unconscious mental machinery allows the conscious mind to operate more efficiently, without overloading it with irrelevant details. In line with this understanding, sub- jective reports are no longer viewed as the stumbling block for a science of the mind. Instead subjective reports may be viewed as the output of a com- plex but presumably lawful mental machinery (Dennett, 1991). A crucial question for emotion researchers is whether or not nonconscious emotional processes can be viewed within the information-processing paradigm that has characterized mainstream cognitive psychology for several decades. The general consensus seems to be yes (see also Scherer, Chapter 13; Winkielman et al., Chapter 14; for a different view see Clore, Storbeck, Robinson, & Centerbar, Chapter 16). This assumption yields several in- sights about emotion processing, more generally.

Levels of Processing, Qualitative Differences

Conscious and nonconscious emotional processes obey different principles and may ultimately require quite different research methods. For example, a major argument against basic, culture-independent emotions has been that studies of facial and vocal expressions of emotion have failed to pro- duce convincing results (see Russell, Bachorowski, & Fernandez-Dols, 2003, for overview and discussion). It may be the case, however, that the majority of studies has been designed to measure conscious derivatives of emotion; therefore these data really do not speak to the possibility of basic unconscious emotion mechanisms.

Thus, when investigating how the organism specifically processes emotional information at the perceptual level, as contrasted with higher levels of cognition (e.g., thinking and decision making), it is important to exert proper methodological caution such that processing levels are not confounded. Without such empirical control, it is difficult to avoid the interpretation that the observed results reflect task demands and subjective

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coping strategies. When the experimental subject is aware of the goals and the design of the study, the experimental situation is transparent, and delib- erate response strategies may contaminate the findings (Bertelson & de Gelder, 2004; de Gelder & Bertelson, 2003; Weiskrantz, 2001). If control is fully achieved, participants are neither aware of a stimulus nor of its prop- erties, and the results are not contaminated by response strategies.

Awareness, Seeing, and Attending

As noted in the first part of this chapter, two kinds of neurological deficits have dominated research on nonconscious processes in the last decade: deficits of attention (e.g., visual neglect) and deficits of vision (e.g., blind- sight). Similarities and differences between neglect versus blindsight have been compared in the past (Driver & Vuilleumier, 2001). In human research, affective blindsight probably offers the clearest and most radical instance of emotional perception without awareness. Unlike inattentional recognition of emotional objects in neglect patients, blindsight is not modu- lated by degree of attention or by the fact that attentional resources are oth- erwise engaged. This finding is consistent with the view that attention and awareness can be manipulated independently (Kentridge, Heywood, & Weiskrantz, 1999), and that the cognitive processes involved in attention and alerting are spared in blindsight (Kentridge & Heywood, 2001).

Findings from studies of patients with blindsight suggest that visual awareness deficits are relatively independent from cognitive awareness deficits. Furthermore, although the networks involved in each are not well understood, it does seem to be the case that they contribute sepa- rately to the nonconscious processing of emotion. For example, the means by which the amygdala plays its role in alerting the organism to fear sig- nals and modulates visual processes may be different in the two cases. In both cases fear signals are often processed automatically. But automaticity on its own does not count as a touchstone for absence of awareness. Many daily activities are performed in an automatic fashion, but we are still aware of them taking place.

Perception and Recognition

A longstanding intuition is reflected in the association of perception with intermediate vision (linked with nonconscious processing) and recognition with conscious cognition, although more recently the boundary between perception and recognition has become blurred (e.g., meaningful but nonconscious processes are often termed nonconscious recognition). The central issue in this distinction is the role of concepts in providing a firm

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ground for empirical knowledge. The traditional association between rec- ognition and consciousness stems from the longstanding epistemological claim that knowledge (as involved in recognition and contrasted with per- ception) requires concepts, and that concepts belong to the realm of the thinking mind, not that of sensory perception. The epistemological roots are reflected in 19th- and early 20th-century psychological theories of visual perception and continue to influence our thinking, including our cat- egorizations of patients’ experiences. For example, the contrast between perception and cognition (previously called apperception) is at the basis of the classical distinction between apperceptive and associative agnosia (Lissauer, 1890).

The perception–cognition distinction also owns its persistence to the fact that it maps easily onto a traditional hierarchical model of the visual system. Yet recent findings make it increasingly doubtful that perception (sensory, visual) and recognition (cognitive, conceptual) are sequentially organized (for a similar point, see Niedenthal et al., Chapter 2; Barrett, Chapter 11). For example, findings about recurrent networks and feedback loops from frontal areas back to temporo-occipetal areas (Bullier, 2001) challenge a strictly hierarchical organization of visual perception and cog- nition. The notion that recognition requires concepts is also challenged by the discovery of new ways in which an organism can instantiate a concept outside conscious control (e.g., via perceptual categorization through auto- matic mimicry, imitation, action representation, and the “most cognitive” variant, theory of mind). When recognition involves activity in structures devoted to action representation and in motor structures, as shown for observation of object-directed actions (Grèzes & Decety, 2001) and emo- tional body movements (de Gelder, 2004), then the meaning of perception is extended to include perceptual abilities rooted in systems that involve broadly distributed abilities related to bodily implementation and embodi- ment of emotion.

In view of these developments, there is no compelling reason to distin- guish between perception and recognition, at least not along the traditional sensory–cognitive or nonconscious–conscious divide. A similar comment applies, albeit for different reasons, to partly overlapping contrasts between implicit–explicit and attended–unattended processes. Each of these dis- tinctions is built upon a mix of intuitions, behavioral findings, and experi- mental evidence obtained with widely different methodologies, experien- tial reports, and neuroanatomical facts whose interconnections we do not clearly envisage at present. As far as studies of the perception of emotions are concerned, in the conscious versus unconscious debate, we have sal- vaged one reasonably circumscribed and clear dimension that is linked to perceptual and postperceptual processes. In cases where the methodology

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used allows for applying it, conscious and nonconscious processes can be distinguished.

Seeing Is Feeling: A Thorny Issue

Traditionally, emotion researchers have focused on facial expressions of emotion, and this focus may help explain why visual perception of aspects of emotional behavior have received the most attention. This focus may have some advantages for disentangling conscious from nonconscious per- ception, however, because the methods to do so are much more advanced in the visual domain than in any other sensory domain . Facial expressions, affective pictures, vocalizations, emotional tone of voice in language, and whole-body movements are viewed as the observable consequences of internal emotional states intended by a sender and decoded by a receiver. Yet many emotional displays function in a way that transcends the relatively complex notion of making internal states visible or even of communicating them. Action-based perception models consider visual perception and com- munication from a richer and more evolutionary inspired perspective that is potentially more appropriate for emotions (de Waal, 2002). Emotional communication is more direct than envisaged in traditional models; the first data now available clearly indicate that seeing fear “contaminates” motor structures for the sake of preparing for action (de Gelder, 2004).

Interesting findings about emotional mimicry from Dimberg and col- laborators (Dimberg, 2000) are sometimes used in support of the role of mirror neurons in social communication. The activations observed in our study (de Gelder, 2004) in premotor, parietal, and inferior frontal gyri are consistent with a role for mirror neurons somewhere along the line, yet it is unknown at present just what this role may be (di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, 1992). Future research is needed to disentan- gle the role of the different components in the fear contagion system. As we suggested, this is likely to be a complex system with multipurpose compo- nents that acquire significance for emotion only in the context of the whole. This complex system suggests a limitation for accounts of social communi- cation based only on imitation implemented by neural mechanisms that model observed behavior. For example, several studies inspired by the reports on mirror neurons recently reported deficits in imitation in autistic individuals, suggesting a failure of this imitation-mirror mechanism in autism. We recently tested the hypothesis that facial expression mimicry may be impaired in autism. But our observations clearly indicated that there is no difference in EMG activity in response to facial expressions of anger or joy in autistic participants with clear deficits in recogni- tion of facial expressions and social communication (Magnee, Stekelenburg,

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de Gelder, Van Engeland, & Kemner, 2005). Given that the communicative disorders of populations with autism are well documented, this result sug- gests that caution should be exercised in jumping from a reflex-like activity in facial muscles to a conclusion regarding mirror-neuron-based imitation and ultimately to the presence of social cognition and empathy in these individuals. At present no single approach and, a fortiori, no single cause seems to be able to render the different dimensions of perceiving, produc- ing, and experiencing emotion.

ACKNOWLEDGMENTS

Many thanks to the editors for fruitful comments on earlier drafts, to W. A. C. van de Riet for assistance with the manuscript, and to the collaborators of the various studies summarized here.

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VUiNsuCalOENmSoCtIioOnUPSerAcNepDtioEnMOTIONAL PROCESSING

CHAPTER 7
Visual Emotion Perception

Mechanisms and Processes

ANTHONY P. ATKINSON RALPH ADOLPHS

Perceiving and interpreting other people’s emotional states is essential for effective social interaction. Its very importance is likely to have resulted in the evolution of complex mechanisms that underlie it. A basic capacity to attach emotional significance to stimuli and respond to them appropriately, without any conscious experience, is likely to have evolved under different selection pressures and considerably earlier than the capacity for conscious emotional responses—a hypothesis that now enjoys considerable empirical support (LeDoux, 1998). Emotion perception is similarly bifurcated in this way. At times emotion perception is automatic and fast (and thus, typically, unconscious), and at other times deliberate, slow, and effortful (and thus, typically, conscious). Recent evidence indicates that this distinction at the behavioral level reflects a division in the underlying cognitive processes and neural substrate (for a similar view, see Winkielman, Berridge, & Wilbarger, Chapter 14).

The focus of this chapter is the perception of emotion from visual cues. In the first section we highlight some of the conceptual issues surrounding the distinction between conscious and unconscious emotion perception, and the different methods used to probe these capacities. Then, in the second sec- tion, we outline the neural substrate of emotion perception from facial expressions, weighing the evidence for a degree of emotion-specific func-

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1. What is emotion?

From an evolutionary perspective, emotions are central states shaped by natural selection that enable animals to cope with threats and opportunities presented to them by their physical and social environments. Emotions achieve these effects by coordinating a large number of changes in brain, body, and behavior. Most or all of the so-called basic emotions (Ekman, 1992)—fear, disgust, anger, joy, sadness, surprise—can be thought of as packages of response coordination sculpted by evolution to meet particular environmental challenges, such as avoiding physical harm (fear) and contaminants (disgust). Somewhat more con- troversially, some of the more complex social emotions, such as jealousy, guilt, and embarrassment, can be analyzed in this way as well (e.g., Cosmides & Tooby, 2000). Such an adaptationist perspective encompasses both the produc- tion and perception of emotion signals—capacities that many have argued coevolved (e.g., Darwin, 1872/1998; Plutchik, 1980; although see Owren, Rendall, & Bachorowski, Chapter 8; Owren & Bachorowski, 2001, for an account of why the evolution of emotion signaling and perception might be decoupled in some cases). Emotion signals can be considered as aspects of coordinated systems of emotional response, as outward expressions of internal emotional states, or as communicative acts that can be causally divorced from the emotional states that they usually signal. We do not make these distinctions in this chapter, and refer to all three types of emotion signal as emotional expressions.

Consonant with this view of emotions as solutions to distinct adaptive problems is an expectation that the underlying neural systems will be organized in a modular fashion, to some degree. Both the requirement for speed and the need to trigger a particular class of behaviors may make specialized systems advantageous, and may have resulted in neural mechanisms that are relatively specialized to process certain emotionally relevant information. Some theories of emotion, in fact, categorize emotions according to the neural systems that implement ecological packages of behavioral mechanisms (Panksepp, 1998). The main purpose of this initial processing is to provide a crude assessment of the value of the stimulus (good/bad, harmful/pleasant) and thus to motivate behavior (e.g., approach–avoid). In addition to this very fast, automatic, and coarse pro- cessing, the presentation of an emotional stimulus also typically initiates more detailed perceptual and recognition processing, which is likely to be less classi- cally modular (e.g., slower, less automatic, and less encapsulated), and can include more complex attributions and rationalizations of the causes of an emo- tion and regulation of its expression.

Roughly, we view feeling (the awareness of one’s emotional state and what it is like to be in that state) and behavior (emotional response) as only dispositionally linked to emotion, as such. Measurements of feelings (via subjec- tive report) or behavior (via facial expression or autonomic response) can be taken as evidence for an emotional state, but are not themselves constitutive of that state. That is, although we use evidence of what people say and do to infer

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their emotional states, those emotional states are not to be identified with any one particular piece of that evidence (behavior, vouched feeling), nor, indeed, with that evidence in the round. This view differs from many other emotion theories. It may be closest in spirit to Russell’s notion of “core affect” (Russell, 2003), although we do not share all his views. In particular, we agree that people are often unaware of the causal networks linking stimuli, emotions, feel- ings, and behavior. In attributing an emotion to someone, or even to oneself, one might be unaware of the actual causal networks because one’s causal attri- bution is mistaken, only partial, or both, or because one has failed to attribute any causes at all (see also Winkielman, Berridge, & Wilbarger, Chapter 14). In our view, emotions are theoretical central states that are assigned to an organ- ism on the basis of our observations of its interaction with its environment, its somatic response, and (for humans) its verbal report of feelings. In this sense, we believe emotions to be implemented neurologically. Although there are par- ticular words to describe emotions, and although we use the basic emotion labels in this chapter, we fully acknowledge that emotions are continuous states that accompany all of our waking lives, not just discrete, strongly emotional epi- sodes—an idea consonant with the theoretical frameworks of Russell (2003), Damasio (1994, 1999), and others.

2. How does one measure conscious versus unconscious perception?

Implicit or covert abilities are typically measured by performance on indirect tests, whereas explicit or overt abilities are typically measured by performance on direct tests. In a direct test of a perceptual ability, subjects are given explicit instructions to perform a perceptual task, and performance on that task is the measure of interest for the experimenter. Direct tests of emotion perception include tasks that require (1) matching emotional expressions across two or more identities, (2) distinguishing between varying degrees of emotional inten- sity, (3) forced-choice emotion labeling, (4) rating viewed faces as to how much of each of a given number of emotions they contain, and (5) identifying the expressed emotion in a free-response procedure. By contrast, in an indirect test of a perceptual ability, performance on the task specified in the instructions is not the measure of interest but nevertheless involves the to-be-measured per- ceptual ability. (Indirect tests thus typically involve both direct and indirect measures.) No reference is made to the perceptual ability or measure of interest in the instructions given to the subjects. One of several examples of indirect tests of emotion perception discussed in the main text involves recording changes in the skin conductance response (SCR) in the absence of reported awareness of the very briefly presented masked expressions (Esteves, Parra, Dimberg, & Öhman, 1994); another involves measuring changes in facial electromyographic (EMG) response.

The terms direct and indirect are used to describe different types of empirical measures (performances on tasks), whereas the terms explicit or overt

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and implicit or covert refer to types of knowledge or information processes and, in particular, describe the degree of participants’ awareness of their abilities (Reingold & Merikle, 1988). Direct measures are often accompanied by explicit knowledge, and indirect measures by implicit knowledge, but not always: For instance, it is possible for certain brain-damaged patients to generate implicit knowledge on direct tests, such as when blindsight patients successfully dis- criminate stimuli presented in their blind fields in a direct, forced-choice task (Weiskrantz, 1990), even though they lack visual awareness of those stimuli.

3. What are the stimuli for the study of biological motion perception?

In order to assess our ability to make various judgments on the basis of face and body movements (biological motion), including the ability to discriminate and identify emotional expressions, it is important to be able to study the con- tribution of movement information in the absence of all other cues that might contribute to those judgments, especially static-form information. Johansson (1973) devised a technique for studying the perception of biological motion that minimizes or eliminates static-form information from the stimulus but retains motion information. In these point-light or patch-light displays, the moving figure, such as a face or body, is represented by a small number of illuminated dots or patches, positioned so as to highlight the motion of the facial muscles or body parts. Video clips are made in which the only visible elements are these bright points. When static, the display gives the impression of a relatively meaningless configuration of points, but when moving, this meaningless config- uration is transformed into a striking impression of a moving face or body. Researchers have shown that people recognize not just types of locomotive movement from point-light biological motion stimuli, but also gender from the actor’s gait (Kozlowski & Cutting, 1977), the identity of familiar people from their gait (Cutting & Kozlowski, 1977) or arm movement (Hill & Pollick, 2000), traits such as vulnerability (Gunns, Johnston, & Hudson, 2002), and emotional states from facial movement (Bassili 1978) and whole-body (Dittrich et al., 1996) or arm (Pollick et al., 2001) movement. Even young infants are sensitive to bio- logical motion in point-light displays (Fox & McDaniel, 1982). In sum, people’s ability to derive socially relevant information from such impoverished cues is striking: Facial and body movement are clearly useful sources of information about others’ states and traits.

tional organization in these neural mechanisms, and arguing the need for fur- ther research using dynamic portrayals of emotion. In the third section we consider the evidence that a subcortical pathway from the retina to amygdala, bypassing the primary visual cortex, subserves unconscious emotion percep- tion. In the fourth section we explore whether the neural structures involved in emotion perception from faces might also subserve emotion perception from other visual cues, especially body posture and movement.

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A variety of evidence suggests an intimate link between emotion per- ception and emotional experience (see also Barrett, Chapter 11; Prinz, Chapter 15), and between the neural mechanisms subserving these capaci- ties. One idea, elaborated in the fifth section, is that we come to know or recognize the emotional state of others via our perception of an emotional response within ourselves (see also Niedenthal, Barsalou, Ric, & Krauth- Gruber, Chapter 2). The importance of the dynamic aspect of emotional expressions shows itself here, for if, as we suggest, emotion understanding occurs via mimicry or simulation, then it is plausible to suppose that what is mimicked or simulated is the dynamic production of an expression, rather than some snapshot at, or near, the emotional peak.

CONSCIOUS VERSUS UNCONSCIOUS EMOTION PERCEPTION

As we illustrate below, it is possible to perceive another’s emotional expres- sion without the observer being consciously aware of perceiving the pos- ture or movement of the other person’s face or body, or, indeed, without being aware of the face or body at all. At the other end of the spectrum, the observer might consciously perceive another’s face or body, its features and their configuration, and its emotional expression. In between these two extremes lie other possible degrees or levels of awareness, such as con- sciously perceiving a face or body, its posture and movement, and its affec- tive quality (e.g., as having a positive or negative valence) without being aware of what specific emotion it conveys, without recognizing or other- wise knowing that it is an expression of fear, for example (technically, a form of fear agnosia). At work in these cases is a distinction known to philoso- phers as that between the perception of things and the perception of facts, or nonepistemic versus epistemic perception (Dretske, 1969). Perceiving an object or event, such as a fearful facial expression, does not require that the object or event be recognized or interpreted in any particular way; it does not require that we associate what we perceive with any additional knowledge about what it means. Perceiving a fact, on the other hand, means grasping the fact and entails coming to know that it is a fact. Epistemically seeing an expression of fear, for example, involves recogniz- ing or coming to know this fact via the visual modality.

In psychology, the term perception is often used to cover both non- epistemic and epistemic perception; unless otherwise noted, this is how we use the term in this chapter. Nonetheless, the two types of perception still mark a useful distinction that corresponds to discrete types or stages of pro- cessing. Perception of things refers to processes that occur very soon after

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the onset of the stimulus, and are presumed to rely largely on early sensory cortices. These processes make explicit the distinct features of stimuli and their geometric configurations to allow discrimination among different stimuli on the basis of their appearance. In contrast, perception of facts refers to processes that require additional knowledge that could not be obtained solely from an inspection of the features of the stimulus. The latter set of processes is quite heterogeneous. For instance, recognition of fear from a facial expression may occur by linking the perceptual properties of the facial stimulus to various knowledge-based processes. These include the knowledge components of the concept of fear, the lexical label fear, and the perception of the emotional fear response (or a central representation thereof) that the stimulus triggers in the observer. Although a common con- ception is that higher-level cognitive abilities such as these are grounded in knowledge-based processes that do not involve sensory cortices and are thus amodal, an alternative viewpoint, which we endorse, is that these abil- ities are, in fact, grounded in sensory–motor representations, but at a more abstract or higher level (e.g., Barsalou, Simmons, Barbey, & Wilson, 2003; Damasio, 1999; Niedenthal et al., Chapter 2).

It may be tempting to identify early perceptual processing (perception of things) with unconscious perception, and later perceptual and recogni- tion processing (perception of facts) with conscious perception. Later per- ceptual and recognition processing need not be conscious, however, as evi- denced by the various ways in which conceptual knowledge can shape perception without awareness (see Barrett, Chapter 11; Smith & Neumann, Chapter 12). Indeed, it may even be that emotionally and socially relevant conceptual knowledge is particularly adept at shaping perception with or without awareness, that recognition of emotional and other social informa- tion is, in some sense, obligatory and colors our perception of the social world, even when that perception is unconscious. If true, then early visual processing is not sufficient for unconscious emotion perception.

There are several ways of measuring unconscious emotion perception (see “A Subcortical Pathway . . . ” and “Emotion Recognition . . . ”; see also Lundqvist & Öhman, Chapter 5; de Gelder, Chapter 6), but it remains unclear as to exactly what the informational content is of the representa- tions produced by such unconscious processing. For example, one current controversy that we explore below concerns the role of a subcortical path- way from the retina to amygdala, which some investigators argue subserves unconscious emotion perception. Does activity of this pathway, in response to faces of which the subject is unaware, reflect that pathway’s ability to distinguish between certain specific facial emotions (e.g., fearful from happy and sad), or threatening from nonthreatening faces, or more simply, emotional from nonemotional faces? Bound up with this issue is the addi-

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tional question of whether this subcortical pathway subserves unconscious emotion perception on its own, or whether its activation reflects some involvement of cortical processing.

THE NEURAL SUBSTRATE OF EMOTION PERCEPTION FROM FACIAL EXPRESSIONS

Some of the most important neural structures underpinning emotion per- ception from the face are the occipital and temporal cortices, amygdala, orbitofrontal cortex (including its ventromedial aspect), right inferior pari- etal cortices, especially somatosensory cortex, and basal ganglia (see Fig- ures 7.1 and 7.2). These structures are engaged in multiple processes and at various points in time, making it difficult to assign a single function to a structure. (For a more detailed review, see Adolphs, 2002.) Early visual pro- cessing of facial emotion, up to 150–180 milliseconds poststimulus onset, proceeds along two parallel routes that later interact: a subcortical pathway to the amygdala via the superior colliculus and pulvinar, for the fast pro- cessing of highly salient, especially threatening, stimuli; and a slower corti- cal route, via thalamus and striate cortices, to regions of inferior and supe- rior temporal cortices. Later, more detailed processing of emotional faces, occurring after about 180 milliseconds poststimulus onset, appears to involve interactions between the amygdala and several cortical regions, especially fusiform, superior temporal, and orbitofrontal cortices. This claim is consistent with the findings of projections between the amygdala and orbitofrontal cortex, and projections from those two structures to the superior temporal and fusiform cortices (e.g., Carmichael & Price, 1995), and is supported by direct evidence of correlations between amygdala activity and activity in these cortical regions in response to static facial expressions (e.g., Iidaka et al., 2001; Morris, Öhman, & Dolan, 1998). Direct, causal evidence in humans that amygdala activity modulates the processing of emotional stimuli in cortical regions was, until very recently, lacking. By combining functional imaging and lesion data, Vuilleumier, Richardson, Armony, Driver, and Dolan (2004) found that amygdala activity enhances sensory processing in occipital as well as fusiform visual areas, when participants were viewing fearful, as compared to emotionally neu- tral, faces.

Along with the orbitofrontal cortex, especially its ventromedial sector, and the amygdala, the insular and parietal somatosensory cortices are involved in the modulation of emotional reactions involving the body via connections to brainstem structures (Damasio, 1994, 1999; LeDoux, 1998). This function of the insular and parietal somatosensory cortices may under-

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FIGURE 7.1. Neuroanatomy of some of the key structures implicated in recognition of facial emotion. Three-dimensional renderings of the amygdala, ventromedial prefrontal cortex, right somatosensory cortices (SI, SII, and insula), and, for orientation, the lateral ventricles were obtained from segmentation of these structures from serial magnetic resonance images of a normal human brain. The structures were corendered with a three-dimensional reconstruction of the entire brain (top) and a reconstruction of the brain with the anterior right quarter removed to clearly show location of the internal structures (bottom). From Adolphs (2002). Copyright 2002 by Ralph Adolphs. Reprinted by permission.

lie their important role in emotion perception (Adolphs, Damasio, Tranel, Cooper, & Damasio, 2000; Heberlein, Adolphs, Tranel, & Damasio, 2004; Winston, O’Doherty, & Dolan, 2003), which is likely to involve the activa- tion of conceptual knowledge associated with the emotion signaled by the viewed face, perhaps via their connections with the orbitofrontal cortex and superior temporal cortex. As we discuss in the section “Emotion Recogni- tion via Contagion . . . ,” the processes that engage parietal somatosensory

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FIGURE 7.2. The time-course of emotion processing and the associated neural struc- tures. The time-course is represented from the onset of the stimulus at the top, through perception, to final recognition of the emotion at the bottom. FFA, fusiform face area; STG, superior temporal gyrus. Many of the mechanisms outlined here may be shared when recognizing emotion from other classes of stimuli, such as body movement and prosody. From Adolphs (2002). Copyright 2002 by Ralph Adolphs. Reprinted by permis- sion.

and insular cortices may involve simulating the viewed emotional state via the generation of a somatosensory image of the associated body state.

It is clear that the perception of any given facial configuration depends on a complex interaction of multiple brain regions and that many distinct brain regions are multifunctional, participating in a range of psychological processes. Nonetheless, neuropsychological and neurophysiological re- search suggests that distinct brain regions are disproportionately involved

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in the perception of certain facially expressed basic emotions (for a review, see Calder, Lawrence, & Young, 2001). Patients with bilateral amygdala damage have particular difficulty recognizing fearful and, in some cases, angry facial expressions in static images, but have relatively little difficulty recognizing other emotions expressed in the face, such as disgust, happi- ness, and sadness (e.g., Adolphs, Tranel, Damasio, & Damasio, 1994; Cal- der et al., 1996). In contrast, people with damage to the anterior insula and surrounding tissue have particular difficulty recognizing facial expressions of disgust, but are not so impaired at recognizing other facial expressions, including fear and anger (e.g., Calder, Keane, Manes, Antoun, & Young, 2000b; Sprengelmeyer et al., 1997). More recently, a selective impairment in the recognition of anger from facial expressions has been demonstrated in patients with damage to a region of the subcortical basal ganglia known as the ventral striatum (Calder, Keane, Lawrence, & Manes, 2004), as well as in healthy participants who are administered sulpride, an antipsychotic drug that reduces aggression and operates by blocking dopamine receptors (Lawrence, Calder, McGowan, & Grasby, 2002). Although this lesion evi- dence is persuasive, it is important to note that there is some criticism and evidence to the contrary (e.g., Rapcsak et al., 2000). Moreover, that amygdala damage can sometimes impair anger as well as fear perception suggests a deficit in arousal responses to signals of threat, rather than a def- icit in recognizing a specific basic emotion. This interpretation is supported by the finding that bilateral amygdala damage can impair the ability to judge the level of arousal (but not the valence) in facial expressions and spo- ken words and sentences that depict unpleasant emotions, especially those relating to fear and anger (Adolphs, Russell, & Tranel, 1999).

One problem cited in regard to many of the older studies in the litera- ture that reported emotion-specific impairments is that they did not adequately control for effects of differential difficulty between emotions (Rapcsak et al., 2000). Functional imaging studies with static facial expres- sions, however, do not appear to be subject to the possible confounds of dif- ficulty that may be present in some of the lesion studies. Although func- tional imaging techniques support only correlational rather than causal claims about brain function, studies that make use of them nevertheless corroborate the inference from human lesion studies of a degree of emotion-specific functional organization in the neural substrate of emotion perception (see Murphy, Nimmo-Smith & Lawrence, 2003, and Phan, Wager, Taylor, & Liberzon, 2002, for meta-analyses of imaging studies, but see also Winston et al., 2003, for some recent counterevidence). In particu- lar, static facial expressions of fear are associated with bilateral amygdala functioning, especially in the left hemisphere (e.g., Breiter et al., 1996; Morris et al., 1998), whereas static facial expressions of disgust are associ- ated with functioning of the anterior insula, especially in the left hemi-

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sphere, and striatum in the right hemisphere, especially the globus pallidus and caudate nucleus (e.g., Phillips et al., 1997; Sprengelmeyer, Rausch, Eysel, & Przuntek, 1998). A recent study, however, suggests that this selec- tive activity for expressions of fear and disgust may be restricted to condi- tions of conscious perception (Phillips et al., 2004). It is noteworthy that the occasional reports of amygdala activation for happy faces may well be due to the fact that those studies did not control sufficiently for personality, because the amygdala’s response to happy faces, but not to expressions of fear or other basic emotions, has been positively correlated with degree of extraversion (Canli, Sivers, Whitfield, Gotlib, & Gabrieli, 2002). The few studies that have examined neural responses specifically to angry facial expressions have tended to find relatively widespread activation for anger compared to expressions of other basic emotions, yet the lateral orbito- frontal cortex appears to be a region of common overlap (Murphy et al., 2003).

In contrast to the current state of knowledge about the perception of basic emotions and its neural substrate, much less is known about the social and moral emotions, such as shame, embarrassment, pride, and guilt. What little research there is has focused on the amygdala. Baron-Cohen, Wheel- wright, and Joliffe (1997) explored the recognition of complex mental and emotional states, including social emotions, from the face. Their findings were threefold: (1) such complex mental states are recognized dispropor- tionately by information from the region of the eyes in the face (Baron- Cohen et al., 1997; Baron-Cohen, Wheelwright, Hull, Raste, & Plumb, 2001); (2) when making judgments about such states from images of the eye region of the face, normal subjects showed activation of the amygdala in functional imaging studies (Baron-Cohen et al., 1999); and (3) this amygdala activation was not found in individuals diagnosed with autism (Baron- Cohen et al., 1999), who are impaired in their ability to recognize complex mental states from the eyes. These findings, together with many others, have suggested that the severe impairments in everyday social behavior exhibited by people with autism may be attributable, in part, to dysfunction in circuits that include the amygdala (Baron-Cohen et al., 2000). Indeed, a lesion study (Adolphs, Baron-Cohen, & Tranel, 2002) found that amygdala damage resulted in a disproportionate impairment in perceiving social emotions from facial expressions, notably from the eye region of the face. Furthermore, there was some indication that, in fact, subjects with amygdala damage may be more impaired in their perception and judg- ments of social emotions than of basic emotions. Although preliminary, those findings are consistent with the possibility that the amygdala might be relatively specialized to process emotional information that is social- ly relevant—a function that may be particular to the human amygdala (Adolphs, 2003).

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Although studies using static face stimuli are valuable (Lundqvist & Öhman, Chapter 5) and have yielded a good deal of knowledge about visual emotion perception and its neural substrate (Adolphs, 2002), they will not provide a complete account of emotion perception and its neural basis. For one thing, postures and movement of the body or its parts can make a sub- stantial contribution to emotional and other nonverbal communication. For another, it is clear that dynamic portrayals of emotional expressions have greater ecological validity than static portrayals, because faces and bodies move a great deal in social interactions, especially when we are emotional, whereas emotions portrayed in static images correspond only to identifi- able peaks or intermediate stages of socially meaningful movements. It is also evident that dynamic properties of emotional expressions, such as their time-course and vigor, influence recognition performance and ratings of emotional intensity (Atkinson, Dittrich, Gemmell, & Young, 2004; Kamachi et al., 2001; Pollick, Paterson, Bruderlin, & Sanford, 2001; Pollick, Hill, Calder, & Paterson, 2003). Moreover, there is now considerable evidence for the existence of a neural system, critically involving the superior tempo- ral sulcus, dedicated to the perception of high-level motion stimuli, espe- cially facial and body movements (for reviews, see Allison, Puce, & McCar- thy, 2000; Puce & Perrett, 2003), with the suggestion that it might also play an important role in the perception of emotional expressions (Narumoto, Okada, Sadato, Fukui, & Yonekura, 2001).

It remains to be confirmed whether the circumscribed deficits in rec- ognizing facial expressions of fear, disgust, and anger encompass both dynamic as well as static expressions, or whether the patients might derive some benefit from facial (or body) movement—or indeed, whether the patients still show a relative deficit in recognizing expressions of fear, dis- gust, or anger, despite deriving some benefit from movement. An early report of a patient with bilateral amygdala damage indicated that she was no better at identifying basic emotions in dynamic than static full-light facial expressions (Young, Hellawell, Van De Wal, & Johnson, 1996). As we discussed above, further studies with this and other patients with amygdala lesions have shown that the recognition deficit is most evident for expres- sions of fear in static faces, but the apparent lack of facilitation for facial movement has not been pursued. More recently, there has been a report of a patient with brain damage encompassing the insula in both hemispheres, whose recognition performance was significantly better for dynamic than for static facial expressions, except in the case of disgust (Adolphs, Tranel, & Damasio, 2003).

Any facilitation of emotion perception provided by dynamic compared to static expressions may well depend on a combination of the tasks and stimuli. Wehrle, Kaiser, Schmidt, and Scherer (2000) found that dynamic presentations of synthetic facial expressions increased overall recognition

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accuracy and reduced confusions between unrelated emotions, compared to static presentations of those faces, in neurologically healthy participants. However, participants in Kamachi et al.’s (2001) study were no better at recognizing dynamic compared to static facial expressions of sadness, hap- piness, surprise, and anger (where the dynamic stimuli were generated by morphing between still images of a neutral face and an emotional expres- sion for a given actor). Nevertheless, the speed and time-course of the facial movements influenced forced-choice recognition accuracy: Happiness, and to a lesser extent, surprise, were more accurately identified from faster movements, whereas sadness was more accurately identified from slower movements, and anger from movements of medium pace. The same pattern of recognition accuracy was obtained in an emotion-rating task. Moreover, Kamachi et al. found that ratings of emotional intensity tended to be higher for the dynamic than the static expressions, when the dynamic expressions were played at the speed that produced the best recognition performance.

Emotional intensity ratings of happy and angry facial expressions did not differ between static and dynamic presentations in Kilts, Egan, Gideon, Ely, and Hoffman’s (2003) study. Thornton and Kourtzi (2002) found that the time to match the emotion of a static target face (frowning or smiling) with that of a briefly presented (540 milliseconds) prime face was essen- tially similar whether the prime was dynamic (from neutral to emotional expression) or static. The same dynamic primes did, however, facilitate reaction times for matching the identity of the same faces, compared to the static primes. Facial movement as represented in point-light displays has been shown to facilitate judgments of emotional expression and gender, rel- ative to judgments from static, fully illuminated faces, in a patient with bilateral damage to the occipital lobes who has severe visual object and face recognition impairments (Humphreys, Donnelly, & Riddoch, 1993). Yet patients with schizophrenia have shown impairment in recognizing dynamic as well as static facial expressions of emotion, although movement information does improve their ability to match the identity of unfamiliar faces and to recognize the identity of familiar faces (Archer, Hay, & Young, 1994).

To date, only a handful of functional imaging studies has examined the perception of dynamic facial expressions of emotion, and these studies have used full-light but not point-light displays. Nevertheless, these studies pro- vide further evidence for the disproportionate involvement of certain neu- ral structures in processing signals of specific emotions. Most notably, the amygdala was found to respond preferentially to fearful compared to happy and angry expressions, with greater activation for dynamic face morphs compared to static expressions and dynamic control stimuli (LaBar, Crupain, Voyrodic, & McCarthy, 2003; Sato, Kochiyama, Yoshikawa, Naito,

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& Matsumura, 2004). Furthermore, the anterior insula, and to a lesser extent, the anterior cingulate cortex, but not the amygdala, were selectively activated by dynamic facial expressions of disgust, relative to dynamic dis- plays of emotionally neutral face movements (Wicker et al., 2003). The superior temporal sulcus was strongly implicated in the processing of facial expressions of emotion, especially dynamic portrayals, in all four of these studies, consonant with previous findings of STS involvement in the per- ception of biological motion, mentioned earlier. However, whereas this dif- ferential activation of the superior temporal sulcus by dynamic compared to static expressions was found for angry faces in Kilts et al.’s study and for fearful faces in Sato et al.’s study, both studies reported that it was activity in the middle temporal cortex that better differentiated dynamic from static happy faces. Note that Kilts et al.’s participants were required to make explicit judgments of emotional expression for the angry and happy faces, but judged the spatial orientation of the neutral faces. Thus it is possible that the observed differential brain activations might reflect, in part, that difference in tasks. Indeed, it is known that different tasks can differentially modulate neural responses to facial expressions (e.g., Lange et al., 2003; Phillips et al., 1997).

A SUBCORTICAL PATHWAY FOR THE UNCONSCIOUS PERCEPTION OF EMOTION?

The subcortical pathway appears to underpin the processing of information about others’ emotional states, without any involvement of the visual cor- tex, and even, as some investigators have suggested, without any involve- ment of conscious awareness. One line of evidence comes from reports of patient G.Y., who has blindsight—that is, a lack of conscious visual experi- ence for stimuli presented in part of his visual field as a result of damage to the striate cortex (V1), yet a spared ability to discriminate and localize sim- ple visual stimuli presented in that blind field (see also de Gelder, Chapter 6). This residual vision in the blind field is thought to rely on subcortical pathways from the retina to extrastriate cortex, via the pulvinar and supe- rior colliculus, which bypass V1 (Cowey & Stoerig, 1991). G.Y. showed sig- nificantly above-chance forced-choice discrimination of happy, sad, fearful, and angry facial expressions presented in his blind field, and he was more accurate discriminating happy and sad than angry and fearful expressions, yet he was not aware of the faces to which he responded (de Gelder, Vroomen, Pourtois, & Weiskrantz, 1999). G.Y.’s performance was consider- ably better for short-duration dynamic displays than for static images, with which he had only very limited success. In a later study, his performance

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was at chance level for nonconscious discrimination between fearful and happy static facial expressions, though interestingly, another blindsight patient, D.B., was significantly above chance at this task, and both patients successfully discriminated between fearful and happy complex static scenes presented in their blind fields (de Gelder, Pourtois, & Weiskrantz, 2002). Covert perception of the emotional content of faces appears to have conse- quences over and above covert perception of the emotional content of scenes in these patients, however. Event-related potentials to words spoken in fearful or happy tones were modulated by the emotional congruency of fearful and happy faces as well as scenes when presented in D.B.’s and G.Y.’s good visual fields, but only by the emotional congruency of the faces when presented in their blind fields (de Gelder et al., 2002). Static faces elicited early extrastriate occipital activity when presented either in G.Y.’s good or blind hemifields, beginning at about 120 milliseconds poststimulus onset for his good field and at about 140 milliseconds for his blind field, demonstrating that V1 activity is not necessary for an extrastriate response to these static images (Rossion, de Gelder, Pourtois, Guerit, & Weiskrantz, 2000). When scanned using functional magnetic resonance imaging (fMRI), differential amygdala activity was observed in G.Y. to fearful versus happy static faces presented either to his blind or seeing hemifield, whereas stri- ate, fusiform, and prefrontal activation was observed only for faces pre- sented to his seeing hemifield (Morris, de Gelder, Weiskrantz, & Dolan, 2001). Although this is tantalizing evidence that the subcortical route to the amygdala subserves covert emotion perception, it is not conclusive, because the relatively poor temporal resolution of fMRI does not allow an alternative explanation to be ruled out, namely, that the amygdala activity to emotional faces is due to feedback to the amygdala from extrastriate cor- tices.

A second line of evidence that the subcortical pathway can subserve covert emotion perception comes from functional imaging studies with healthy volunteers. Morris, Öhman, and Dolan (1999) found that aversively conditioned static angry expressions enhanced the activity of the right amygdala when the faces were presented very briefly and backward masked, such that they were not consciously seen, whereas these faces enhanced activity of the left amygdala only when they were unmasked and thus consciously seen, replicating these authors’ earlier findings (Morris et al., 1998). Importantly, the responses of the pulvinar and superior colliculus were positively correlated, whereas the responses of the fusiform and orbitofrontal cortices were negatively correlated, with the right amygdala response to the masked angry (“unseen”) faces. Even without aversive conditioning, backward-masked presentations of fearful expressions can increase, whereas happy expressions decrease amygdala activity relative to neutral expressions (Whalen et al., 1998). However, in a more recent study,

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Phillips et al. (2004) did not find significant amygdala activation to sublimi- nally presented masked fearful faces. Killgore and Yurgelun-Todd (2004) reported significant bilateral amygdala and anterior cingulate activation to subliminally presented masked happy faces, and left anterior cingulate but no amygdala activation to masked sad facial expressions—which, they argue, is not consistent with the subcortical pathway account of covert emotion perception.

Although most of these studies support the idea that a subcortical pathway from the retina to amygdala subserves covert emotion percep- tion, that interpretation is not watertight for two reasons, at least. First, the reported amygdala activity in response to emotional expressions in the absence of awareness might, in fact, reflect the amygdala’s involve- ment in degraded but intact processing in cortical systems that subserve face and emotion perception (e.g., Pessoa, Kastner, & Ungerleider, 2002; Rolls, 1999). Second, the data may be subject to criterion effects. That is, subjects could be reporting that they were unaware of the stimulus or of the particular emotion when they were not completely sure about their response. Two recent studies attempted to address these problems and together strengthen the claim that the subcortical pathway to the amyg- dala is a neural substrate of unconscious emotion perception. Pasley, Mayes, and Schultz (2004) used fMRI in conjunction with binocular rivalry to investigate the subcortical discrimination of fearful faces versus non-face objects when these stimuli were not consciously perceived. Bin- ocular rivalry occurs when different monocular stimuli (such as a face and a chair) are presented independently to the two eyes. After a few seconds of apparently monocular perception, the dominant image is replaced by the other completely monocular image. This procedure allows the experi- menter to determine the effect of a visual stimulus that we can be more confident the participant does not consciously perceive (e.g., Crick, 1996). Pasley et al. found left amygdala but not inferotemporal cortex activation to unperceived or suppressed fearful static faces, compared to a non-face object, consonant with the proposition of a subcortical route to the amygdala that subserves unconscious emotion perception. The activation of the amygdala via this subcortical route does not appear to be limited to expressions of fear, however. Also using fMRI, Williams, Morris, McGlone, Abbott, and Mattingley (2004) found increased amygdala activity to both fearful and happy, compared to neutral, static faces when the faces were suppressed (bilateral for fear; right hemisphere for happy), but only to fearful faces when they were consciously perceived (right amygdala). This finding suggests that the activity of a subregion of the amygdala (primar- ily in the right hemisphere) does not differentiate between threatening and nonthreatening facial expressions, at least when the subcortical route is selectively engaged.

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PERCEIVING EMOTIONS FROM BODY EXPRESSIONS AND OTHER DYNAMIC VISUAL STIMULI

Body posture and movement stimuli have rarely been used in investiga- tions of emotion perception in patient populations or in functional imaging studies. Yet characteristic body postures and movements indicate specific emotional states (e.g., Wallbott, 1998), and distinct expressions of at least the basic emotions are readily recognized in the absence of facial and vocal cues when portrayed by static body postures (e.g., Atkinson et al., 2004) and by whole-body movement (e.g., Atkinson et al., 2004; Dittrich, Troscianko, Lea, & Morgan, 1996). The neural substrate of emotion perception from body expressions is beginning to be revealed. Three brain regions have been implicated so far, all of which are also involved in the processing of facially expressed emotion: the amygdala and the fusiform and somato- sensory cortices.

Sprengelmeyer et al. (1999) reported a patient with bilateral amygdala damage who has a deficit in recognizing fear from static body postures as well as from static faces. However, the amygdala’s role in processing emo- tional information from bodies may be less important than its role in processing emotional information from faces. Adolphs and Tranel (2003) showed that bilateral amygdala damage reduces the ability to recognize emotions from static images of complex social scenes when subjects utilize information from facial expressions, but not for negative emotions when the faces are obscured, such that participants have to rely on other cues such as body posture, hand gestures, and interpersonal stances. Remarkably, patients with bilateral amygdala damage were, in fact, more accurate in rec- ognizing anger from scenes with faces erased than with faces present—a response that Adolphs and Tranel (2003) attribute, in part, to their particu- lar impairment in recognizing anger from faces shown in isolation. The amygdala has also been implicated as a key structure in the processing of static, fearful body expressions, along with several cortical regions, includ- ing the fusiform cortex, in two fMRI studies (de Gelder, Snyder, Greve, Gerard, & Hadjikhani, 2004; Hadjikhani & de Gelder, 2003).

Further studies are required that employ dynamic as well as static body stimuli, along with expressions of other emotions. Heberlein et al.’s (2004) study is step in this direction. These researchers found that impair- ments in judging emotions from point-light walkers were associated with damage to several components of a network of neural structures, in which the most reliable region of lesion overlap associated with this impairment was in the right somatosensory cortices. In contrast, impairments in judg- ing personality traits from point-light walkers were associated with damage to the left frontal operculum. The involvement of right somatosensory corti-

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ces in emotion perception from these dynamic stimuli parallels the role of these structures in emotion perception from static facial expressions, as demonstrated by a study involving over 100 patients with focal brain dam- age, which also found that impaired emotion perception correlated best with right somatosensory cortex lesions (Adolphs et al., 2000).

As mentioned above, the superior temporal cortex appears to be selec- tively involved in processing body (as well as facial) movement, as opposed to nonbiological motion and static body (and facial) form (e.g., Grossman et al., 2000). Activity in the lingual gyrus, especially at the cuneus border (Servos, Osu, Santi, & Kawato, 2002; Vaina, Solomon, Chowdhury, Sinha, & Belliveau, 2001), and in the occipital and fusiform face areas (Grossman & Blake, 2002) also distinguishes biological from nonbiological motion. But very little is yet known about the roles these areas play in processing body expressions of emotion—for example, whether their contribution is simply in the processing of biological motion, regardless of emotional content, or whether some part of these areas might be specialized for processing the emotional meaning of body (and perhaps also facial) movement.

Another interesting class of pure visual motion stimuli that conveys emotional and social information consists of displays in which social inter- actions are depicted by relative visual motion between multiple objects. One such stimulus shows simple geometric shapes moving on a plain white background (Figure 7.3). Solely on the basis of the movements of these shapes, normal subjects attribute social and emotional states to the objects (Heider & Simmel, 1944). The reliable, automatic, and obligatory emo- tional and social perception triggered by this visual motion stimulus has been confirmed in numerous studies (Berry, Misovich, Kean, & Baron, 1992). Intriguingly, such simple geometric shapes can, in virtue of their motion, activate the fusiform face area in humans (Schultz et al., 2003); fur- thermore, people with autism (Klin, 2000) or bilateral amygdala damage (Heberlein & Adolphs, 2004) fail to perceive this stimulus in emotional– social terms. This impairment was most striking in a rare subject with bilat-

FIGURE 7.3. A representation of a frame from a version of the Heider and Simmel (1944) video.

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eral amygdala damage, who perceived the geometric motion of the stimuli entirely accurately, but completely failed to see any emotional or social meaning in those movements.

EMOTION RECOGNITION VIA CONTAGION OR SIMULATION

How do we come to associate particular postures and movements of another’s face and body with specific emotional states? Several closely related proposals, which are examples of the “embodied cognition” concept (e.g., Niedenthal et al., in press), center on the idea that processes of emo- tional contagion or simulation (or both) provide the means by which we come to know what others are feeling. Here we provide a brief summary of this class of proposals and the experimental findings that support them; the proposals are delineated in more detail elsewhere (Atkinson, in prepara- tion; Goldman & Sripada, 2005; see also Niedenthal et al., Chapter 2).

The idea that emotional contagion underpins emotion recognition is the view that a visual representation of another’s expression leads us to experience what that person is feeling, which then allows us to infer that person’s emotional state. Current versions of this idea say little, if anything, about the latter, inferential process, but all state or assume that the grounds for inferring the viewed person’s emotional state is knowledge from the “inside,” that experiencing the emotion for oneself (even in an attenuated or unconscious form) is an important, perhaps necessary, step to making accurate inferences about others’ emotions. This perspective suggests a close connection between the neural substrates of emotion perception and emotional experience. The perceptual mechanisms might relay information to separate mechanisms underlying emotional experience, either directly or via facial mimicry, or the perceptual mechanisms might also subserve emotional experience (see also Barrett, Chapter 11; Prinz, Chapter 15). A different but conceivably compatible idea is that coming to know what another is feeling involves simulating the viewed emotional state via the generation of a somatosensory image of the associated body state, or simu- lating the motor programs for producing the viewed expression.

There is direct evidence that at least some of the neural systems involved in emotion perception mediate emotional experience as well. For example, somatosensory and cingulate cortices were prominent among those structures engaged by the recall of personal episodes of happiness, sadness, anger, and fear (Damasio et al., 2000), and the medial prefrontal cortex was engaged during episodes of positive and negative emotion, and by more specific experience of happiness, sadness, and disgust, as induced

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by emotional films, pictures, and recall (Lane, Reiman, Ahern, Schwartz, & Davidson, 1997; Lane, Reiman, Bradley, et al., 1997). Moreover, several studies support a degree of emotion-specific processing consonant with the emotion perception literature. For example, procaine-induced feelings of intense fear were associated with significant left amygdala activity, com- pared to euphoric feelings, in a study by Ketter et al. (1996), and direct electrical stimulation within the medial temporal lobe, primarily of the amygdala and hippocampus, evoked unpleasant feelings that were predom- inantly reported as fear or anxiety (Halgren, Walter, Cherlow, & Crandall, 1978). Direct stimulation of insula neurons can generate reports of unpleas- ant sensations in the throat, spreading up to the mouth, lips, and nose (Krolak-Salmon et al., 2003), responses related more to disgust than to other emotions, though so can stimulation of the amygdala and hippocam- pus, which can also elicit sensations in the stomach that are typically described as nausea (Halgren et al., 1978). More recently, Wicker et al. (2003) found anterior insula activation when participants felt disgusted as well as when they saw someone else produce genuine expressions of dis- gust.

A large degree of overlap or close connection between the neural sub- strates of emotion perception and emotional experience is also suggested by the finding that patients who have circumscribed emotion perception deficits may also have a corresponding circumscribed deficit in their phe- nomenal experience of the same emotions (e.g., Calder, Keane, Manes, et al., 2000; Sprengelmeyer et al., 1997). However, not all such patients appear to have abnormal emotional experience. For example, amygdala lesions do not necessarily impair emotional experience, either as assessed by a questionnaire asking about the typicality of experienced positive and negative emotions, or by a daily diary record of experienced positive and negative emotions (Anderson & Phelps, 2002). Thus whereas emotion per- ception may engage processes that are also involved in emotional experi- ence, either their engagement is not necessary for emotion perception, or, if those processes are necessarily engaged, then their operation may not nec- essarily produce the relevant emotional experience. Nevertheless, we should record a caveat here: Given the difficulty of obtaining accurate and reliable online measures of specific emotions (for a review, see Barrett, Chapter 11), and that such measures have rarely been used in the patient studies, the possibility is left open that any processes of emotional conta- gion or mental simulation underpinning emotion perception may involve, at least as a by-product, subjects’ experience of the emotion they are view- ing in another as they are viewing it.

Further evidence that contagion or simulation, or both, may also play a role in recognition of the actions that comprise emotional facial expressions

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comes from disparate experiments. The experience and expression of emo- tion can be correlated (Rosenberg & Ekman, 1994; although they need not be—see Cacioppo, Berntson, Larsen, Poehlmann, & Ito, 2000) and offer an intriguing causal relationship: Production of emotional facial expressions (Adelmann & Zajonc, 1989) and other somatovisceral responses (Cacioppo, Berntson, & Klein, 1992) can lead to changes in emotional experience. Pro- ducing a facial expression to command influences the feeling and auto- nomic correlates of the emotional state (Levenson, Ekman, & Friesen, 1990) as well as its electroencephalographic (EEG) correlates (Ekman & Davidson, 1993). Viewing facial expressions results in expressions on one’s own face that may not be readily visible but that can be measured with facial electromyography (EMG; Dimberg, 1982) and that mimic the expres- sion shown in the stimulus (Hess & Blairy, 2001), even in the absence of conscious recognition of the stimulus (Dimberg, Thunberg, & Elmehed, 2000; see also Lundqvist & Öhman, Chapter 5). Viewing facial expressions can also elicit autonomic correlates indicative of a change in emotional state, such as the skin conductance response (Dimberg, 1982), even during unconscious stimulus presentations (Williams et al., 2004) and changes in feeling (Schneider, Gur, Gur, & Muenz, 1994; Wild, Erb, & Bartels, 2001).

We have already mentioned the finding that lesions involving right somatosensory cortices (including SI, SII, and the insular cortex) are asso- ciated with a general impairment in the recognition of emotion from facial (Adolphs et al., 2000) and body (Heberlein et al., 2004) expressions. These findings suggest that emotion recognition may involve simulating the viewed emotional state via the generation of a somatosensory image of the associated body state. Indeed, Adolphs et al. (2000) also found a correlation between impaired perception of emotion from facial expressions and impaired somatic touch sensation in the viewer! What is not yet clear, how- ever, is exactly how somatosensory cortices contribute to emotion percep- tion. If, for example, emotion recognition involves the unintentional mim- icry of the viewed expression, then one might expect the activity of the facial muscles to be reflected in the face regions of primary and secondary somatosensory cortices, which raises the question of whether it is such proprioceptive activity that plays a role in emotion recognition, either directly or by inducing the corresponding emotional state. The possibility has also been raised of a more direct connection between the visual pro- cessing of emotional expressions and activity in the primary and secondary somatosensory cortices, which does not involve mimicry of the other’s expressions: namely, that observing another’s facial emotion directly elicits the proprioceptive activity in the observer appropriate to the viewed expression, as if the observer were making the movements him- or herself (what Goldman & Sripada, 2004, call “reverse simulation with ‘as if’ loop”).

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(In the case of observing emotional body postures and movements, one might also expect activity in regions representing proprioceptive informa- tion about the corresponding parts of the observer’s body.) Another possi- bility is that primary and secondary somatosensory cortex activity in emotion perception arises as a consequence of the offline simulation of another’s facial (or body) movements, either as a by-product of that simula- tion process or as a causal link in the chain leading eventually to emotion recognition and attribution.

Both lesion and imaging studies indicate a more general role for the insula cortex in emotion perception, in addition to the role its anterior por- tion seems to play in the perception and experience of disgust. The insula’s role in emotional experience is likely linked to its function in representing visceral and other interoceptive, rather than proprioceptive, information (Craig, 2003), suggesting several possibilities for which one would expect insula involvement in emotion perception. One is that viewing an emo- tional expression induces that same emotion in the observer, either directly or via some mediating process such as motor mimicry. Another possibility is that visual representations of the emotional expression directly modulate interoceptive structures that generate the feeling, without causing actual bodily changes—that is, the offline simulation of an emotional state (akin to Damasio’s, 1994, 1999, “as-if” loop). That this simulation proposal requires the possibility of such a direct, central mechanism is borne out by the find- ing that patients with congenital facial paralysis are able nonetheless to rec- ognize facial emotion (Calder, Keane, Cole, et al., 2000).

If emotion perception involves mimicking the viewed expression or executing its motor program offline, then we might expect to find neural mechanisms common to both the perception and production of facial expressions. Evidence of such a common neural substrate comes from work on mirror neurons. Neurons in the premotor cortex of monkeys respond not only when the monkey prepares to perform an action itself, but also when the monkey observes the same visually presented action performed by another individual (monkey or human, e.g., Rizzolatti, Fadiga, Gallese, & Fogassi, 1996). Various supportive findings have also been obtained in humans. Observing another’s actions results in desynchronization in the motor cortex, as measured with magnetoencephalography (Hari et al., 1998), and lowers the threshold for producing motor responses when transcranial magnetic stimulation is used to activate the motor cortex (Strafella & Paus, 2000). Imitating another’s actions via observation acti- vates the premotor cortex in functional imaging studies (Iacoboni et al., 1999); moreover, such activation is somatotopic with regard to the body part that is observed to perform the action, even in the absence of any overt action on the part of the subject (Buccino et al., 2001). There may also be

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mirror neurons for emotional facial actions: A largely similar neural net- work is activated when subjects either passively view or deliberately imi- tate static facial expressions of basic emotions (Carr, Iacoboni, Dubeau, Maziotta, & Lenzi, 2003) and dynamic smiling and frowning expressions (Leslie, Johnson-Frey, & Grafton, 2004). Premotor areas, especially the inferior prefrontal area responsible for face movement, are prominent in this network. Imitation elicited greater and more bilateral activation of these areas than passive viewing, corresponding to an additive effect of expression observation and execution. Other regions implicated in this net- work include the superior temporal cortex (in both studies), insula, and amygdala (in Carr et al.’s study).

The findings discussed so far suggest that viewing dynamic expres- sions may facilitate simulation, compared to static expressions. However, the results of one study were taken by its authors to suggest the opposite, namely, that emotion perception in dynamic facial expressions relies less on motor simulation. Kilts et al. (2003) found that judging the emotional inten- sity of static, but not dynamic angry and happy, compared to neutral, faces activated cortical motor-related regions, including primary motor and premotor cortices, and the left somatosensory cortex. Presumably the idea is that the brain, in implementing a simulation process, has to try harder or do more to decipher the emotion in static compared to dynamic images. Clearly, though, this interpretation is in stark contrast to our earlier sugges- tion that the dynamic production of an expression is more likely to be simu- lated than some snapshot at or near the emotional peak. A decision between these alternatives awaits further research, using facial and body expressions.

CLOSING REMARKS

Regions of the visual cortex and certain other structures, including the amygdala and insula, appear to be relatively specialized to process emo- tionally and socially relevant information. Some of this processing occurs very early in time, subsequent to the onset of an emotionally salient visual stimulus, with latencies around 100–300 milliseconds. It is likely that much of this early processing is driven by feed-forward connections between lower visual areas and higher regions, including the amygdala. Yet, as we noted, the amygdala also receives emotional information via a subcortical pathway involving the superior colliculus and pulvinar; this pathway might underpin the processing of information about others’ emotional states with- out the involvement of the visual cortex—and even without any conscious awareness. There are at least three reasons to suspect that this early cortical

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and subcortical processing does not contribute directly to the contents of our conscious perceptual experience of the emotional expression (Prinz, Chapter 15; Clore, Storbeck, Robinson, & Centerbar, Chapter 16). First, it happens too quickly, apparently permitting insufficient time for a window within which integrated neural activity could generate a conscious percept (cf. Libet, 1981). Indeed, the early phase of emotional information process- ing can occur with stimuli that are either backward masked or suppressed under binocular rivalry, and especially in the latter case we can be sure that the emotional expression cannot be consciously perceived. A second reason to doubt that the informational contents of such early processing constitute the contents of our conscious perception of the emotional expression is that the representation of the stimulus or of the emotional response that the stimulus produces is somewhat impoverished or lacking in detail, relative to the properties of the visual world represented in experience. That is, the information that is represented by such early processing looks to be of a much coarser grain than our conscious experience. For example, the subcortical route to the amygdala carries only low-spatial-frequency infor- mation that is nevertheless sufficient to activate the amygdala in response to fearful faces (Vuilleumier, Armony, Driver, & Dolan, 2003), yet we expe- rience the stimulus with much richer perceptual and emotional content. Hence it is prima facie doubtful that the contents of this early processing are directly related to the contents of conscious perception. (Nevertheless, they could be related indirectly, insofar as the informational contents of this early processing might contribute to, or be necessary precursors of, the informational contents that constitute the contents of experience.) A third reason is more empirical: Recent findings argue strongly that feedback pro- jections from higher processing stages back to lower ones are necessary in order for conscious experience to occur (e.g., Pascual-Leone & Walsh, 2001).

Nonetheless, research (Pascual-Leone & Walsh, 2001) has also shown that conscious experience depends on lower-processing regions, anatomically— just at a later point in time. So, although conscious processing requires temporally later stages, it draws upon anatomical regions that are both “higher” and “lower” in a processing hierarchy. Occipital visual cortices, the amygdala, and other structures that are engaged very early in process- ing do indeed contribute directly to conscious experience, but they do so during a later iteration of processing, when the activity driven by the exter- nal stimulus can be compared with activity driven by feedback from higher regions. Thus it is fallacious to assign conscious perception to any particular anatomical regions: Both anatomy and time are critical. Certain sets of structures, engaged at certain points in time, are the subvenience base for conscious experience.

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Having said this much, an obvious next question is: What is the con- tent of the conscious experiences so generated? Suppose we see an emo- tional facial expression. Our argument has been that perception of the emo- tion can include at least the following components. We perceive the structural features of the visual stimulus (i.e., the features of the face and their configuration). We also perceive the emotion shown in the face, and, we have argued, one mechanism whereby we do that is by perceiving our own emotional response to the face shown. This latter component depends on first triggering an emotional response to the face, via structures such as the amygdala, and second, neurally representing that emotional response, via structures such as the somatosensory cortices and insula. Finally, the way we actually perceive the emotional face in our conscious awareness is not merely as a combination of these different components, but as the face imbued with the emotion that we attribute to it. A key open question con- cerns exactly how this process occurs. From what we have said so far, we might expect that the viewer would simply perceive a face, and perceive his or her own emotional state. But that is not what happens—the emotional state is attributed to the face, not to oneself as the viewer. Clearly, there must be mechanisms in place that automatically prevent such misat- tribution and permit the emotion to be linked to the stimulus in the right way. The sense of self—and thus the ability to distinguish between self and others when attributing emotions, thoughts, and actions—develops as a consequence of interpersonal interactions and a capacity to imitate, and may well be implemented by a system involving the inferior parietal cortex in conjunction with the prefrontal cortex (Decety & Chaminade, 2003).

ACKNOWLEDGMENTS

The writing of this chapter was aided by a conference travel grant awarded to Anthony P. Atkinson by the British Academy. Ralph Adolphs’s work reported here was funded by grants from the U.S. National Institutes of Health and the James S. McDonnell Foundation. We are grateful to Lisa Feldman Barrett and Piotr Winkielman for helpful comments on an earlier version of the chapter.

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PART III

Unconscious Emotional Behavior

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UNNonCliOngNuSisCtiIcOVUocSaEl CMoOmTmIuOnNicAatLioBnEHAVIOR

CHAPTER 8

Conscious and Unconscious Emotion in Nonlinguistic Vocal Communication

MICHAEL J. OWREN DREW RENDALL JO-ANNE BACHOROWSKI

Human and nonhuman communication occurs in many forms, across diverse modalities, and likely representing a wide variety of mechanisms and functions. In spite of this diversity, researchers and laypeople alike tend to understand communication from a particular standpoint; namely, that signals have content, convey messages, and have meaning. This stand- point is the canonical approach in linguistic communication, where words are arbitrary constructions that convey a specific message by virtue of their symbolic relation to objects and events in the world. Although different in many respects, an emotion-related signal, or expression, is nevertheless often conceived of in the same way. It is, for example, often considered the outward manifestation of a specific internal emotional state. In this chapter we attempt to account for the phenomenon of nonlinguistic vocal behavior from a different perspective. Rather than conceiving of these signals as vehicles for conveying encoded messages, we argue that they function first and foremost by engaging low-level psychological processes in the listener, such as attention, arousal, emotion, and motivation. This approach is dis-

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1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

The affect-induction model is meant to have broad scope, applying to nonlinguistic vocal communication in both humans and other mammals. The basic claim is that all such signaling is fundamentally rooted in the affective impact that the sounds have on listeners. This interpretation contrasts with those arguing that the primary function of signaling is to activate cognitive rep- resentations. The affect-induction model thus conceives of emotions as founda- tional processes of attention, arousal, valenced affect, and motivation. These very basic processes can include both conscious and unconscious components and are critical in guiding an individual’s moment-to-moment decision making and behavior. This concept of emotion is meant to contrast with the classic view of cognition as elaborated, abstract, and amodal processing. However, we deem affective processes to be fundamental to the psychological and physiological scaffolding that precedes, underlies, and supports cognitive representations (see Niedenthal, Barsalou, Ric & Krauth-Gruber, Chapter 2). A term such as fear can be conceived as a label of a region in a multidimensional state–space of psychological and physiological processes, whose common consequence is an increase in the probability of avoidant behavior (see Barrett, Chapter 11). Con- tributing dimensions include increased attention, heightened arousal, a nega- tively valenced subjective experience, and a concomitant goal of evading the triggering stimulus.

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

Definitions of conscious and unconscious used in this chapter follow the spirit of Öhman’s (1999) discussion of these concepts. The term unconscious is used to refer to processes that underlie a behavior or a feeling state but that are not accessible to introspection or perceptible as causes of that behavior or state. Conversely, the process is considered conscious if it is accessible to examination through introspection and is perceptible. The conscious processing of external stimuli implies that these events are attended to, noticed, and trigger aware- ness. In contrast, unconscious processing includes learning about stimuli and events that may be noticed as they occur, but either do not form explicit memo- ries or are not retained as such. The contrast between conscious and uncon- scious is used synonymously with the distinction between implicit and explicit, and between automatic and controlled. We consider the difference to be impor- tant both for the affective processes driving nonlinguistic vocal production and for those shaping perception of these kinds of vocalizations.

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not

(continued)

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like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

The affect-induction framework relies on a basic distinction that is aligned with, if not identical to, conscious versus unconscious, explicit versus implicit, and controlled versus automatic processing. This account particularly stresses sig- naler exploitation of unconscious perceiver biases, over which the perceiver has little direct control. Specifically, sound stimuli are proposed to routinely induce affective responses rooted in foundational nervous-system properties, over which listeners have little or no conscious or explicit control. Try as one might, for example, it is difficult to suppress psychological and autonomic responses when hearing fingernails on a chalkboard, a wailing baby, a noxious car alarm, or a cat screaming when its tail is stepped on. Some of the neural circuits involved may lie both literally and figuratively close to those that maintain unconscious vegetative functions such as breathing, heartbeat, and alertness. The framework also stresses the importance of learned responses in listeners, in whom crucial conditioning processes are unconscious, implicit, and automatic.

However, both unconditioned and conditioned effects of sounds also bring the listener’s conscious, explicit, and controlled processes into play. These are processes through which listeners may attempt to minimize the sound’s impact or execute planful behavior as a result of that impact. Similar points also can be made about signalers who unconsciously use vocalizations to exert influence over listeners. To the extent that vocal production can become subject to con- scious, explicit, or controlled processes, individuals who learn that producing calls can affect the behavior of others may come to deploy their sounds more deliberately or reflectively. On both the perception and production sides, then, the conscious–unconscious distinction likely reflects a continuum of states that can gradate from one to another, both developmentally and evolutionarily.

cussed in the context of vocalizations produced by both nonhuman pri- mates and humans, where the interplay of conscious and unconscious emo- tion processes exerts a critical role.

AN AFFECT-INDUCTION APPROACH TO NONLINGUISTIC VOCAL SIGNALING

Whether produced by humans or nonhumans, and occurring in the visual, auditory, or other modalities, communication signals are commonly under- stood to stand for, or be about, something. This approach has been impor- tant in interpreting human facial affect, where particular expressions have been argued to be linked to particular signaler emotions (e.g., Keltner & Ekman, 2000; Keltner, Ekman, Gonzaga, & Beer, 2003) or social intentions (Fridlund, 1997). A proposed function of a facial expression is that, through

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such expression, signalers are conveying information about their emotional or intentional states to perceivers, thereby allowing more effective interac- tion for both parties (see Lundqvist & Öhman, Chapter 5). A similar inter- pretation is common in animal research (reviewed by Hauser, 1996), where such expressions are referred to as motivational signaling. The underlying explanatory metaphor in both cases is that the physical signal is a medium by which signalers can transmit encoded information to perceivers.

A recognized problem for this view is that both human “emotional expressions” and nonhuman “motivational signals” are often much less tied to specific underlying states or external contexts than one would expect. That problem led Frijda and Tcherkassof (1997) to argue that human facial expressions show only general affinities, rather than specific or exclusive relationships, with particular emotions. In fact, a given emotion may be associated with a variety of expressions at different times, whereas various expressions may be associated with the same underlying emotion (see also Russell & Fernández-Dols, 1997). Similarly, Owren and Rendall (2001) point out that although a few primate vocalizations are linked to quite spe- cific triggering circumstances, many are not. Indeed, examples of acousti- cally similar vocalizations that occur across contexts, and of dissimilar calls that appear in the same context, are readily available (e.g., Owren, Rendall, & Bachorowski, 2003).

Focusing on vocal signals, in particular, we suggest that the properties of sound as a medium allow vocalizers to influence perceivers in immediate ways, and that the strategies involved can explain the observed lack of spec- ificity. One proposed strategy is that vocalizers can contact low-level nervous-system processes in listeners through the direct, unconditioned impact of the acoustic signal itself. A second strategy is that vocalizers can create indirect, conditioned responses in listeners by pairing their own dis- tinctive sounds with affectively significant outcomes experienced by those listeners. These are functions that likely emerged early in the evolution of mammalian vocal communication, given that neither require agreed-upon meanings, encoding and decoding processes in signaler and perceiver, or even coincident fitness interests for the two parties (Owren & Rendall, 2001).

Sound Induces Affect

A striking feature of sound is that it can powerfully influence a listener’s affective state. As a simple example in humans, tapping a pencil in an other- wise quiet room can be remarkably distracting and annoying to others. Another common experience is that sounds can be so noxiously intrusive as to become viscerally disturbing, such as when a human infant’s shrieks and cries aggravate everyone within earshot. Sound is also a highly effective

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medium to use to make warning signals, such as fire alarms, because it can be used to divert attention instantly from whatever task is at hand and to virtually compel a response, such as exiting the premises. In these cases, sound works as a medium of communication, first and foremost, because it directly engages the listener’s nervous system and does not require learn- ing or symbolic value in order to be effective. Sound is also a ready media- tor of emotional learning, as demonstrated over decades of animal research in which tones and buzzers have been used as cues of upcoming events such as food or shock delivery. Humans also routinely acquire affective responses to particular sounds through simple associative learning, for instance, to stimuli such as school bells, police sirens, or even the theme music of a favorite television program.

Recent empirical work on sound-induced affect has confirmed that sound can both modify arousal levels and elicit valenced (positive vs. nega- tive) emotional responses in human listeners (Bradley & Lang, 2000). In these studies, participants first provided explicit ratings of a variety of com- mon sounds, with separate characterizations of the arousal and valenced emotions experienced upon hearing each stimulus. Their ratings were then found to be aligned with the psychophysiological reactions that occurred in response to the sounds. Using stimuli as disparate as machine noises, non- human vocalizations, nonlinguistic human vocalizations, and sounds associ- ated with appetitive human behaviors, Bradley and Lang’s work reported that listeners experienced both nonspecific nervous-system activation ef- fects and specifically positively or negatively valenced reactions. Responses to the sound of beer being poured was one particularly compelling example of the accrual of salient associations to an affectively significant stimulus. Although unremarkable and unobtrusive as an acoustic event, this distinc- tive sound is routinely paired with the very pleasant behavior of ingesting beer. Participant responses revealed that the sound alone induced unequiv- ocally positive emotion.

Using Nonlinguistic Vocalizations for Affect Induction

Initially inspired by demonstrations of highly diverse acoustics and usage in the calls of various primate species, Owren and Rendall (1997, 2001; Rendall & Owren, 2002) have suggested that affect induction may play a key role in the normative vocalizations of many mammalian species (see Owren & Bachorowski, 2003, where they apply the model to human laugh- ter). Here the term “affect” was broadly construed to include perceiver pro- cesses that mediate the psychological dimensions commonly characterized as attention, arousal, emotion, and motivation. This affect-induction, or affect-conditioning, approach notes that these low-level psychological pro- cesses in perceivers can become an avenue of influence for signalers. By

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changing the affective states of listeners, vocalizers can thereby also influ- ence their behavior. In this view, the nature of the auditory system itself creates opportunities for signalers, the most basic of which are to capitalize on direct and indirect impacts on perceiver affect.

Direct (Unconditioned) Effects of Vocalizations

The simplest way that one individual can influence another by vocalizing is to produce acoustic energy that elicits an affective response, in and of itself. The cross-species generality of that claim is illustrated by the acoustic star- tle phenomenon (Davis, 1984). This response is a reflexive interruption of ongoing behavior elicited by features such as abrupt onsets and high ampli- tudes, and is believed to occur in all hearing species (Eaton, 1984). Although vocalizations are unlikely to have evolved specifically to evoke startle, its occurrence demonstrates that sound can affect listeners at foun- dational levels. Abrupt onsets and phenomena such as rapid upward fre- quency sweeps have been linked to increased arousal in both humans and other mammals, in which slow-onset sounds with gradually falling frequen- cies are found to decrease arousal levels (reviewed by Owren & Rendall, 2001). In the affect-induction view, these links indicate that callers can potentially modulate listener affect by producing sounds with particular kinds of acoustic properties—regardless of other aspects of the vocal or social circumstances.

In fact, producing direct-impact vocalizations may be one of the few ways in which socially impotent vocalizers can influence the behavior of more powerful individuals. A classic example is the plethora of shrieks, screams, wails, and whines that human and nonhuman youngsters produce when attempting to shape caregiver behavior. In the human case, infants can use crying to draw attention, induce response motivation, and even “train” caregivers in how to “turn off” these sounds. Infant crying is typi- cally perceived as a markedly negative event, routinely described as grat- ing, aversive, and distressing by adult listeners (Zeskind & Lester, 1978). It also has marked impact on listener arousal (Bradley & Lang, 2000). This strategy of producing noxious sounds is indisputably crude, one that can only work because caregivers are usually deeply invested in the infant’s well-being. When that bias is absent—for example, with biologically unre- lated stepparents or adoptive caregivers—crying, in particular, places the infant at risk of physical abuse (e.g., Frodi, 1985; Murry, 1985). Although it is commonly contended that caregivers can distinguish among putative variants of crying that are specific to experiences of pain, hunger, and a wet diaper (Berry, 1975), there is little evidence to support this contention of language-like function (Gustafson, Wood, & Green, 2000). Instead, these potent sounds appear to be effective primarily due to their direct impact

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on listener arousal and affect, with acoustic variability in crying being most strongly correlated with perceptions of urgency and infant distress (Barr, Hopkins, & Green, 2000; Dessureau, Kurowski, & Thompson, 1998; Gustafson & Green, 1989; Gustafson et al., 2000; Protopapas & Eimas, 1997).

Nonlinguistic aspects of spoken language also likely exert effects via their direct impact. For example, adult humans routinely rely on the direct effects of vocalizations in infant-directed speech, thereby capitaliz- ing on infant sensitivity to auditory stimulation (Fernald, 1991; Papoucek, Bornstein, Nuzzo, Papoucek, & Symmes, 1990). Sounds with pronounced upward frequency sweeps engage and arouse an infant, whereas sounds with marked downward sweeping frequencies are quieting (e.g., Fernald, 1992). Equivalent impacts on infant state have been found using synthetic stimuli (Kaplan & Owren, 1994), indicating that infant responsiveness derives from the direct effects of the acoustics themselves. In adult- directed speech, it is likely no coincidence that features such as pitch, amplitude, and rate are the ones that consistently emerge as emotion- related cues to talker affect (reviewed by Banse & Scherer, 1996). The affect-induction perspective is that when listeners are able to draw in- ferences about talker affect from emotion-related acoustics, they do so based on the impact of acoustics on their own affect-response systems (Bachorowski & Owren, 2002; Russell, Bachorowski, & Fernández-Dols, 2003; also see Hietanen, Surakka, & Linnankoski, 1998).

Indirect (Conditioned) Effects of Vocalizations

A second simple strategy is for signalers to pair their individually distinc- tive vocalizations with the occurrence of affect-inducing actions or events, thereafter being able to use those sounds to elicit corresponding learned responses in perceivers. In other words, if vocalizers can associate their calls with the salient, affective responses occurring in others, conditioning effects can give them leverage over those individuals’ emotional states. Dominant primates thus routinely vocalize before attacking subordinates, which we propose makes them able thereafter to use their threat calls to elicit learned fear. Affiliative calls are also common, for example, when a dominant animal approaches a subordinate for grooming. If the calls have been paired with friendly grooming episodes in the past, hearing these sounds will elicit decreased arousal and fear in the wary subordinate, thereby making it more likely to tolerate the dominant animal’s approach without moving away.

These examples involve a vocalizer that inherently has control over the likely outcome of an interaction. That control allows it to take advantage of basic conditioning processes in another to influence that individual’s affec-

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tive state and expectations, and thereby make this listener more likely to behave as the caller desires. This strategy can thus best be used by socially potent vocalizers, such as mothers of dependent offspring or higher- rather than lower-ranking group members. However, it is also available to any creature that can reliably associate its particular calls with a salient affect occurring in a listener.

Human vocalizers regularly produce individually distinctive sounds paired with behaviors that affect others in important ways. For example, a parent’s comforting tone can effectively soothe a distressed child, in part, because that tone has been paired with past nurturing behaviors and the gradual calming effects the child experienced at those times. The distinc- tive features of the caregiver’s voice play an important role; the calming response will not occur in relation to any vocalizer who might adopt a simi- lar tone. Repeated pairings of individually distinctive laugh sounds with affiliative behavior on the part of the laugher and positive affect on the part of the listener should also support the development of learned emotional responses to those laugh acoustics (Owren & Bachorowski, 2003). Corrobo- rative evidence for such learning includes finding that pairs of friends who interact while performing tasks that elicit frequent laughter are more likely to laugh in close temporal proximity than are stranger pairs (Smoski & Bachorowski, 2003). This result suggests that the participants who were friends rather than strangers experienced laughter-induced affect learned during past interactions in which their partners’ laughter had been paired with positive emotions in themselves.

The Lack of Specificity Problem

The affect-induction approach has a number of implications for non- linguistic vocal signaling (Owren & Rendall, 1997, 2001), one of which is that signals are not expected to routinely show specific and exclusive rela- tionships with particular vocalizer states. For example, many sounds are proposed to be effective through the direct impact they have on listener affect rather than because they provide veridical information about signaler state. Any of a variety of acoustic features might have the desired effect in a particular situation, or using a diversity of sounds may be the most effec- tive. Vocal variability is particularly likely when a listener fails to behave as the vocalizer desires. Socially impotent individuals who are not getting what they want are thus predicted to produce ongoing streams of variable vocalizations that both take advantage of the impact of diverse forms of acoustic energy and that help avoid or overcome listener habituation. This variability is undeniably evident in vocalizations of socially impotent indi- viduals, both human and primate (reviewed by Owren et al., 2003).

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Vocalizations by socially potent individuals, on the other hand, are pre- dicted to show marked individual distinctiveness rather than affective or context specificity. Here the mechanism of influence is the perceiver’s con- ditioned response to the vocalization, occurring both as a generalized reac- tion to hearing sounds from many different vocalizers, and through specific associations with the distinctive properties of these sounds when produced by particular vocalizers. These expectations result from basic learning prin- ciples. For example, a given monkey hears threat calls produced by many different individuals through the course of the day, some of which have been previously followed by attack (higher-ranking animals), and some of which have not (lower-ranking animals). Overall, there may be a modest affective response to threat calls, in general. However, affective responses to calls from higher-ranking animals will be strong and specific, if the threats of these animals are individually distinctive. Stated as a prediction, the claim is that nonlinguistic vocalizations used by socially potent individ- uals should occur in forms that readily include cues to the identity of the signaler. We suggest that this is the case for many of the most common calls in the vocal repertoires of primates (Owren et al., 2003).

It also follows that if socially potent vocalizers are not having the desired effect in a given situation, they will increasingly fall back on the strategy of direct acoustic impact. In primates, for example, threat calls should become louder and occur at a higher rate when a subordinate is not backing down, as desired. In humans, linguistic components of speech are routinely supplemented by direct-impact acoustics such as increased loud- ness, pitch, and sharpness of attack when targets of an utterance are unre- sponsive. For instance, when unruly offspring fail to heed the linguistic commands of adults, conversational tones (e.g., “Stop that, right now”) became high-impact ones (“STOP THAT—RIGHT NOW!”). This strategy appears to be so deeply ingrained that it occurs even in circumstances in which it cannot possibly be effective, such as when tourists who are unable to speak the local language resort to speaking their own language more loudly.

CONSCIOUS AND UNCONSCIOUS PROCESSES IN EMOTION-RELATED VOCALIZATIONS

The remainder of the chapter examines the roles played by conscious and unconscious emotional processes in the affect-based interpretation of the nonlinguistic vocal behavior we have presented. There are points to make about both production and perception of vocalization, and we particularly draw on Öhman’s (1999) distinctions between the conscious and uncon-

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scious (and see Smith & Neumann, Chapter 12). It will also be convenient and illustrative to compare and contrast the processes critical to non- linguistic vocalization with those underlying human spoken language.

Nonlinguistic Vocal Production

Öhman (1999) suggests a conceptual separation between unconscious pro- cesses that can underlie a consciously experienced event and the conscious processes that make up the experience. That distinction is applicable to both the production and perception sides of the communicative equation, and it is particularly apt for the former. Whether vocalizers are human or nonhuman, there are important differences between nonlinguistic vocaliza- tion and human language production. The semantic and syntactic knowl- edge involved in language competence are, of course, unconscious or implicit. However, language behavior is nonetheless importantly different from nonlinguistic vocalizing in showing intentionality or theory of mind— meaning that talkers tacitly attribute mental states to perceivers and pro- duce signals that are specifically designed to alter those states (Dennett, 1983).

On one hand, the low-level machinery involved in representing, selecting, and sequencing words is itself not directly accessible, nor are talkers likely to be consistently aware of the motivations that underlie say- ing particular things at particular times. On the other hand, the decision to speak or not to speak, to discuss a particular topic or some other, to select some words or word sequences over others, and to sometimes inflect a sen- tence in a particular way that alters its perceived significance are all explic- itly controlled by the talker. Sentences can be spoken aloud or merely in one’s head; talkers can thus be said to have a conscious intention to use speech specifically so as to activate representations in listeners that are fun- damentally similar to those occurring in their own minds (Rendall & Owren, 2002).

Research on primates suggests something quite different. Here, vocal- izing appears to be rooted almost exclusively in the signaler’s own circum- stances, with surprisingly little impact on the circumstances and mental states of perceivers (reviewed in Seyfarth & Cheney, 2003). For example, producing alarm calls would seem a prime instance in which the vulnera- bility of other primates is critical to either producing or not producing a call. Instead, call production is often orthogonal to listener needs, with alarm callers routinely continuing long after everyone in the group has already escaped to safety and begun calling themselves. Even primate mothers appear to call based solely on their own vulnerability, as dramati- cally illustrated by a failure to call to predators that are a threat to their

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infants but not to themselves. This phenomenon has been observed both under natural circumstances (Cheney & Seyfarth, 1990a; Rendall, personal observation) and in experiments with captive animals (Cheney & Seyfarth, 1990b). Evidence of intentionality is also absent in contact calling that occurs when primates (1) are out of sight of one another (Cheney, Seyfarth, & Palombit, 1996; Rendall, Cheney, & Seyfarth, 2000) or (2) produce food- discovery vocalizations (Clark & Wrangham, 1993; Chapman & Lefebvre, 1990). Overall, primates exhibit surprisingly circumscribed attributional or perspective-taking capacity (e.g., Povinelli & Bering, 2003; Tomasello & Call, 1997), whereas humans routinely show these abilities both as a pre- requisite for effective language use and in other aspects of everyday life.

Neural Mechanisms in Production

Results such as these suggest important differences between the mecha- nisms involved in nonlinguistic primate vocalizations versus human lan- guage. In regard to the former, the available neurobiological evidence indi- cates a primary role of subcortical structures (e.g., Jürgens, 1998) that are unlikely to be under volitional control (e.g., Kappas & Scherer, 1995). In contrast, whereas spoken language relies on subsystems distributed throughout the brain (e.g., Lieberman, 2002), consciously accessible corti- cal circuitry is central. Human–nonhuman similarities are much greater for nonlinguistic vocalizations, as exemplified by spontaneous human laughter. Here the critical neural structures and motor programs are not only believed to be primarily subcortical, but also to be homologous with those of primates (Deacon, 1997; although see Fried, Wilson, MacDonald, & Behnke, 1998). The emergence of intentional communication through lan- guage is thus connected to the emergence of volitional control of the vocal apparatus as well as to a more sophisticated understanding of the psycho- logical states of others—with conscious processing and the cerebral cortex likely being central contributors in each case.

Nonlinguistic Vocal Perception

Öhman’s (1999) distinction between unconscious underpinnings and con- scious experience also applies to vocal perception, in which, for instance, a sound may trigger inaccessible perceptual and appraisal responses that then give rise to conscious feeling states (see Scherer, Chapter 13). Öhman further notes that although external stimuli such as sounds may fully engage the perceiver as they happen, their occurrence may subsequently be retained only as an implicit, rather than explicit, memory. Both points are central to the affect-induction view, in which implicit and learned affec-

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tive responses in listeners are primary contributors to the effectiveness of nonlinguistic communication for vocalizers. Tulving (2002) goes so far as to argue that nonhuman animals are entirely lacking in episodic memory, meaning that they cannot retain the particulars of individual events or form broader associations and generalized knowledge. This argument is particu- larly relevant in that autobiographical episodes from the past are likely to be the most consciously experienced of all memories. Whether or not Tulving’s claim is literally correct for all species, nonhumans and humans are clearly alike in showing powerful and pervasive implicit learning pro- cesses, while being much less similar in the domain of episodic memory.

Neural Mechanisms in Perception

In perception, as in production, neurobiological evidence reveals a primary role of subcortical circuitry. As a result, our characterizations of conscious and unconscious locate the major effects highlighted in the affect-induction approach squarely on the unconscious side. Although vocal communication events may be salient and attended to by perceivers as they occur, from the vocalizer’s point of view the locus of action lies in automatic, inaccessible processes that originate as early as the brainstem level (e.g., attentional and arousal effects mediated in the medulla and pons) and, importantly, involve subcortical forebrain nuclei that mediate affective learning (e.g., limbic sys- tem). The amygdala, in particular, has been found to be central in learned fear (e.g., LeDoux, 1996, 2000; see Bouton, Chapter 9) and is suspected of being critical in other forms of affective conditioning as well (e.g., Aggleton & Young, 2000).

There are, of course, many contributors to affective learning, which may nonetheless place the amygdala in a central role. This structure has reciprocal connections to a variety of other centers, including the thalamus, hypothalamus, hippocampus, and multiple cortical areas (e.g., Emery & Amaral, 2000). The amygdala is thus likely to affect memory formation mediated by the hippocampus, as well as to modulate cortical processing through its effects on general arousal in multiple forebrain regions and by altering processing in primary and secondary sensory cortical areas (also see Phelps, Chapter 3). Cortical inputs to the amygdala are, in turn, believed to reflect the later, more sophisticated stages of sensory- perceptual processing and the results of more complex evaluative and social–cognitive processing. The important point for us is that the amyg- dala, a low-level and likely consciously inaccessible structure, is both shap- ing and responding to processing occurring in a variety of higher-level neu- ral structures, whose activities are much more likely to be wholly or partially subject to conscious awareness.

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SPIRALING TOWARD CONSCIOUS, CONTROLLED PROCESSES

Summarizing previous points, both we and other authors have argued that unconsciously controlled emotional and motivational processes are critical in the production of nonlinguistic vocalizations; we have also noted that it can be difficult to find exclusive, one-to-one relationships between these signaler states and vocal acoustics. The spontaneous, egocentric nature of these signals is further underscored by the finding that subcortical rather than cortical circuitry is primary in producing the sounds. We have also placed subcortically mediated unconscious processing in a central role in perceivers, arguing that nonlinguistic vocalizations work from the sig- naler’s point of view, first and foremost, because they can be used to influ- ence listener behavior through these low-level systems. The overarching view is that the evolutionary origins of nonlinguistic vocal communication largely involve automatic systems in which unconscious processes in vocal- izers trigger production, and implicit responses in perceivers play a pri- mary role in mediating the influences that these sounds exert on their behavior.

However, an important component of the affect-induction approach is also that signaler and perceiver interests cannot be assumed to be coinci- dent under all, or even most, circumstances. Rather, a fundamental tenet of contemporary evolutionary theory is that two organisms never have exactly the same reproductive interests (unless they are genetically identical). In the face of divergent fitness interests, signaling among biologically unre- lated individuals cannot be assumed to evolve as inherently cooperative, information-sharing events (Owren & Rendall, 2001). Even when signaling is parent-to-offspring or sibling-to-sibling, a situationally dependent mosaic of overlapping and conflicting interests is involved. As a result, any success that vocalizers have in influencing perceivers also creates selection pres- sure on those individuals. Those pressures trigger changes whose outcomes depend on whether the effects either benefit or detract from perceiver fit- ness, and in turn create selection pressure that feeds back onto signaler behavior. Our conclusion is that this reciprocally driven spiral of selective pressures is likely a key mechanism by which cortically mediated and explicit cognitive operations come into play in the emergence of controlled and consciously modulated communicative behavior.

Signaler Success Creates Selection Pressure on Listeners

The affect-induction view argues that signaler vocal behavior is not predi- cated either on listener decoding processes or an ability to infer vocalizer

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intentions. Instead, the claim is that the evolutionary origins of vocal signal- ing ultimately lie in the impact that vocalizers could have on listener affect due to preexisting, unconscious mechanisms. These underlying processes would specifically involve attention, arousal, positive or negative emotional responses, and motivational or appraisal processes that mediate behavior such as approach or avoidance. This argument, in turn, rests on viewing audition as a preattentive, sentinel-like system designed to detect, localize, and identify functionally significant sounds related to imperatives such as evading predators and capturing prey by commandeering listener attention and marshaling the physiological resources needed for rapid action.

The upshot is that signal evolution does not require a foundation of mutual benefit for signaler and perceiver—signals can evolve regardless of the net fitness impact on perceivers. However, any leverage that signalers gain over perceivers also necessarily creates selection pressure on those individuals. Listeners may benefit from signal impact in some circum- stances, such as when a mother responds to her infant’s piercing shrieks or a subordinate shies away from a formidable, threat-calling opponent. But the situation can also be quite different, as illustrated by infants that shriek incessantly during weaning or a formerly unbeatable but now vulnerable foe continuing to elicit conditioned fear responses with its threat calls.

Signaler success in influencing others therefore inevitably selects for more effective perceiver appraisal of such events and their significance. For example, whereas infants may selfishly benefit from crying, screaming, and shrieking in order to elicit maternal resources in excess of actual need, mothers benefit by becoming better able to habituate more effectively to the jarring effects of these sounds, and to “see through” their uncondi- tioned and conditioned power. In nonhumans, that argument can be cast in terms of selfish gene selection, whereas in humans it has also been consid- ered a form of emotional intelligence (Bachorowski & Owren, 2002). In both cases, signaler behavior could prompt the emergence of automatic as well as controlled, effortful, and evaluative processes in perceivers (see Gray, Schaefer, Braver, & Most, Chapter 4; Clore, Storbeck, Robinson, & Centerbar, Chapter 16). These observations thus suggest that an escalating evolutionary process, initiated by vocalizers leveraging listeners via their unconscious processes, could create the selection pressure that ultimately gives rise to explicit, consciously controlled countermeasures.

Perceiver Success Creates Selection Pressure on Signalers

Although selection pressure exerted on listeners is thus separable from the mechanisms and functions of vocalizing, resulting changes in these perceivers can, in turn, feed back on the unconscious and conscious pro-

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cesses in signalers. The reciprocal nature of the selection pressures may be a major contributor to the confusing variety of relationships that seem to exist between spontaneous emotional signals and affective states. Although theorists have disagreed over the extent to which there are one-to-one rela- tionships between the two, there is little doubt that signaler arousal, emo- tion, and motivation all play a central mechanistic role in nonlinguistic sig- naling (e.g., Kappas & Scherer, 1995; Keltner et al., 2003; Russell et al., 2003). One interpretation is that signaler state is crucial both as mechanism and function: An affective state mechanistically triggers a corresponding outward expression, the function of which is to convey that the state has occurred. However, the picture is different if mechanism and function are recognized as separable components. Logically, one should no more infer that the function of vocalizing is to signal affect than, for instance, to show that the vocalizer’s laryngeal motor neurons are active.

An alternative is to view the connection between affect and signal as a causal but purely mechanical link that has no necessary implications for function. Again, we argue for assuming only that the function of signaling is to influence listener behavior in a manner that, on average, has some net benefit to the vocalizer. Instead of viewing affect as being manifested in sig- naling, we suggest viewing affective states as having “access” to the motor neurons and programs that are the proximal cause of vocal production. The evidence suggests that various affective states show differential probabili- ties of triggering a given vocalization program, with those probabilities likely being adjusted by natural selection. The relationship between a par- ticular state and a given kind of motor output might thus be one-to-one, many-to-one, one-to-many, or many-to-many—depending on historical fac- tors in the evolution of the behavior.

If the connection begins as a one-to-one relationship in a vocalizer, it could, but need not, remain that way. For example, if fitness interests in sig- nalers and perceivers are closely aligned, then both parties benefit from the latter being able to draw increasingly accurate inferences concerning states and likely behaviors in the former. However, if the impact of the signal more routinely benefits vocalizers than it does listeners, then perceivers eventually will become able to modulate the effects being exerted on them. In this case, the resulting changes will create selection pressure on signal- ers to decrease specificity and predictably in accordance with the selfish interests in the parties involved. Signaling might also begin as a relatively undifferentiated event, with a single affective state being able to trigger more than one vocalization-producing motor program, or with many affec- tive states having access to multiple programs. Here again, the degree of specificity would likely change over evolutionary time, reflecting complex interactions between vocalizer and listener interests, resulting effects on

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conscious and unconscious mechanisms in perceivers, and the degree to which these changes are beneficial or detrimental to signaler interests.

As a final point, this interaction through evolutionary time may also produce changes in signalers’ conscious control of vocalization. There is only modest evidence of such outcomes among primates, whose vocal behavior appears to be unconsciously controlled, as discussed above. How- ever, both primates and humans can suppress affectively related vocal behavior to some degree (e.g., Cheney & Seyfarth, 1990a; Deacon, 1997), whereas humans can also produce, to some degree, volitional simulations of otherwise spontaneous sounds such as laughter and crying. Owren and Bachorowski (2001) have argued that the emergence of an unconsciously based mechanistic connection between positive affect and the motor program underlying spontaneous, emotion-dependent, and subcortically mediated smiling in early hominids also made the evolution of a volitional, conscious, and cortically mediated version of this expression virtually inevi- table. Although modern humans do not appear to have gained the same degree of volitional control over affect-related vocal expressions, there is little doubt that conscious processes play a role here as well.

FINAL THOUGHTS

Whether or not the perspective described here ultimately proves to be cor- rect, we suggest that some of its underlying points at least should have some lasting value. The first underlying point is that there is good reason to avoid making the common but mistaken assumption that there is an inevita- ble symmetry between signalers and perceivers in communicative events. On the contrary, the fitness interests, neural mechanisms, psychological processes, and affect-related links involved may all be significantly differ- ent and should always be considered separately for the two parties. Second is that both parties show an undeniable and intimate connection between internal state and vocal signaling, and that connection becomes all the more interesting when one has abandoned implicit and explicit assumptions of coincident interests and mutual benefits in signaling. We believe that work- ing to understand the complexities of how conscious and unconscious pro- cesses give rise to vocal signals will eventually be much more revealing about both topics than proceeding by force-fitting preconceived notions of function in emotion-related signaling. In a similar vein, our final point is that nonlinguistic vocal signals and human speech are obviously and impor- tantly different, and it was specifically language that came later. In other words, it seems most sensible to work toward understanding affectively related vocalization in its own right, and to avoid implicitly or explicitly

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relying on language as a general model of communication. We believe that grappling with affect-related signaling is much more likely to produce insights into language than the converse approach, with even the most sophisticated linguistic representations being importantly grounded in the interplay of conscious and unconscious emotion.

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CUoNnCteOxtNuSalCCIOonUtrSolEoMf AOnTxIieOtyN, AFeLarB, EanHdAPVaInOicR

CHAPTER 9

Behavior Systems
and the Contextual Control of Anxiety, Fear, and Panic

MARK E. BOUTON

There is little question that classical conditioning can influence emotions and emotional behavior. Ever since Watson and Rayner’s (1920) famous experiment demonstrating emotional conditioning in an infant boy, classical conditioning has been seen as a mechanism that allows emotions to be trig- gered by new stimuli. Today, conditioning is still viewed as central to the learning of emotional triggers (see Owren, Rendall, & Bachorowski, Chap- ter 8; Barrett, Chapter 11) and emotional disorders (e.g., Barlow, 2002; Bouton, Mineka, & Barlow, 2001; Lang, 1995; LeDoux, 1996; Nelson & Bouton, 2002; Öhman & Mineka, 2001). Conditioning has also become an important methodological tool allowing investigators to study the neurosci- ence of emotion (e.g., LeDoux, 1996; see also Phelps, Chapter 3; Lundqvist & Öhman, Chapter 5).

The present chapter addresses a specific topic within the general study of emotional conditioning—namely, how the context in which conditioning occurs controls the triggering of emotional behavior. In a typical fear condi- tioning experiment with rats, a signal such as a tone (a conditional stimulus, or CS) might elicit fear once it has been paired with an electric foot shock (an unconditional stimulus, or US) on several occasions. The context is typi- cally defined as the experimental chamber the rat is placed in before it

205

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1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

In this chapter emotion is defined in terms of its behavioral aspects; emotions are viewed as loosely coordinated sets of behavioral, physiological, and cogni- tive responses that function to cope with events in the environment (see Scherer, Chapter 13; for an alternate view, see Barrett, Chapter 11). Because much of the research described in this chapter focuses on behavior elicited in nonhuman animals, it may be taken as an illustration of the richness inherent in the organization of emotions in the absence of consciousness or conscious awareness.

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

This chapter focuses on emotional behavior in nonhuman animals, such that dis- tinctions between consciousness, awareness, and so on, are not relevant for this chapter.

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

Humans produce behavioral and interoceptive states to emotional challenges that are homologous to those in animals, as discussed in this chapter. It is possi- ble to speculate that in humans, these states can be consciously experienced and represented in awareness, either as affect or emotion.

receives these crucial conditioning events. Quite a lot is now known about the associative learning that goes into Pavlovian conditioning (see Pearce & Bouton, 2001, for one review). Here I provide a somewhat selective review of what we know about how the context in which the CS is presented fur- ther influences how the organism responds to it. The fact that emotion trig- gered by the CS is itself modulated by the context may have important implications for an understanding of emotion and emotional disorders.

In typical fear conditioning experiments in my own laboratory, a rat is put in an experimental chamber each day for a 90-minute session. In these sessions, four to eight 60-second tones might be presented; some of these might end in a brief, 0.5-second foot shock. The animal is usually in the box for 10–20 minutes before the first tone occurs. The context—the experi- mental chamber—is thus a long-duration stimulus that has an onset long before the crucial conditioning events occur. There is a sense in which the chamber embeds the conditioning events in time and space. I mention this

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to make it clear that the context in a typical conditioning experiment truly is a background stimulus. Its temporal duration makes it somewhat differ- ent from the 60-second tone that directly elicits fear. This difference could have implications for how it might influence anxiety, fear, and panic.

CONDITIONING AND BEHAVIOR SYSTEMS

Time is unquestionably important in conditioning. To develop the point I want to make, however, it is necessary to observe that classical conditioning is a richer and more complex phenomenon than many people appreciate. Once conditioning has occurred, the CS triggers more than a simple uni- tary reflex; it elicits a large and interesting system or constellation of responses. All psychology students know about Pavlov’s original experi- ment, in which a bell CS was paired with a food US. They also know that thanks to conditioning, the bell acquired the ability to elicit a salivary response. Modern researchers recognize that conditioning is an important means by which humans and other animals adapt to biologically significant events (e.g., Hollis, 1982, 1997); the salivary response is clearly functional in the sense that it helps the animal digest the upcoming meal. But a CS for food can elicit much more than this solitary response. Signals for food can evoke an entire set of behaviors and physiological reactions that prepare the organism to digest food. For example, in addition to the well-known sal- ivary response, Pavlov’s bell probably also elicited the secretion of gastric acid, pancreatic enzymes, and insulin. All of these facilitate food absorp- tion, so that animals that have signaled meals are better at digesting them than animals that have unsignaled meals (e.g., Woods & Strubbe, 1994). In freely moving animals, signals for food can also elicit approach behaviors, and thus they guide and direct foraging. Food signals also elicit eating, if food is available, even in the satiated rat (e.g., Weingarten, 1983). CSs for food evoke a whole “behavior system,” a set of behaviors and responses that are functionally organized to capture and consume food (e.g., Timberlake, 1994, 2001).

The same is true in fear conditioning. CSs associated with foot shock can elicit a whole system of conditioned fear responses that is, once again, organized to help the animal deal with the US (e.g., Bolles & Fanselow, 1980; Fanselow, 1994). A CS may evoke several behavioral responses that have evolved to prevent attack by predators. The most familiar one is freez- ing; when a CS for shock is presented, the animal becomes motionless. Freezing in the presence of a predator decreases the likelihood of death by attack—it thus has a documented payoff (Hirsch & Bolles, 1980). In the presence of stimuli that support alternative behaviors, the rat might flee

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from the situation or, when shock is delivered from a small prod attached to the wall of the chamber, it might bury the stimulus with sawdust (e.g., Treit, Pesold, & Rotzinger, 1993). CSs for shock also elicit corresponding changes in respiration, heart rate, blood pressure, and an endorphin response that decreases sensitivity to pain (e.g., Fanselow, 1979). Fear conditioning gives rise to a whole system of behaviors that are designed, through evolution, to help the organism adapt. When we say that an organism is afraid, we usu- ally mean that some aspect of this system has been mobilized.

Behavior systems are often organized such that different behaviors come into play depending on how close in space and time the organism is to the US. For example, Fanselow and Lester (1988) argued that the defen- sive (fear) system is organized such that different behaviors are called forth depending on the animal’s psychological distance from a predator—“preda- tory imminence.” When imminence is low, the animal goes about its daily business, finding food sources and mates. (These behaviors might actually be timed and coordinated to minimize detection by predators.) But when predatory imminence increases, as it does when the animal detects a preda- tor nearby, a different set of behaviors becomes functional. At this point, the rat might freeze, and to support the freeze, the heart rate might slow down and respiration become shallower. At a still higher point on the imminence scale, when a predator actually strikes, still other behaviors may come into play. At this point, the animal might jump, return the attack, and/or flee, with all the supporting physiological responses, such as increased heart rate and deeper breathing. The point is that qualitatively different defen- sive behaviors are available to the animal and are evoked according to when they are most functional. Fanselow and Lester suggest that each type of defensive behavior is designed (i.e., selected through evolution) to pre- vent movement to the next higher point on the imminence scale.

Timberlake (e.g., 1994, 2001) has written extensively about the rat’s feeding behavior system. Here again the system is organized according to the imminence of the motivational object, although in this case the goal is to increase (rather than decrease) contact. When food is distant, there are general search behaviors that function to find it. When the possibility of food is detected, there may be focal search behaviors that function to locate and apprehend it. And finally, there are consumption and handling behav- iors. Interestingly, in Timberlake’s system, CSs that predict food at long, medium, or short time intervals will theoretically evoke different behav- iors that correspond to general search, focal search, and consumption. Timberlake’s system thus explicitly recognizes an important, but often overlooked, fact about conditioning: that the form of the conditioned response depends on the duration of the CS (Holland, 1980; Silva & Timberlake, 1997; Timberlake, Wahl, & King, 1982).

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The last point is made extremely clear in studies of sexual behavior in the male Japanese quail. Michael Domjan and his students have studied this behavior system in detail (e.g., Domjan, 1994, 1997). In a typical exper- iment, a male quail is presented with a visual CS that is paired with the opportunity to copulate with a female. The response that comes to be evoked by the CS as a consequence of the pairings depends crucially on the duration and nature of the CS. For example, if a localized visual CS (pre- sentation of a foam object with terrycloth or feathers on it) is presented for 20 minutes and then copulation with a female occurs, the CS will come to evoke pacing back and forth over trials (Akins, 2000; Akins, Domjan, & Gutierrez, 1994). However, if the same CS is presented for just 30–60 sec- onds immediately prior to copulation on each trial, it comes to evoke sim- ple approach (e.g., Akins, 2000; Akins et al., 1994). It is as if the long stimu- lus elicits a general search behavior, whereas the shorter one elicits focal search. Further, when the CS is a 30–60 second presentation of a taxi- dermically prepared model that includes the head and neck of a female, the CS comes to evoke consummatory behavior—i.e., copulation responses (e.g., Akins, 2000; Domjan, Huber-McDonald, & Holloway, 1992; Cusato & Domjan, 2000). And interestingly, the strength of copulatory responses is increased when the model is presented in a context that has been sepa- rately associated with copulation (Domjan, Greene, & North, 1989; see also Hilliard, Nguyen, & Domjan, 1997). The result is consistent with the idea that conditioned “preparatory” responses, presumably elicited by the con- text, can augment or potentiate “consummatory” responses elicited by other stimuli (Domjan, 1994, 1997; Konorski, 1967).

The same point has been made for defensive conditioning. Following Konorski (1967), Wagner and Brandon (1989) have emphasized that animals associate a CS with both the emotional and sensory aspects of the US, and that the associations with these different aspects of the US evoke different responses. The emotional response is especially likely to be elicited by a long-duration CS. Consistent with this idea, in rabbit eyeblink condition- ing, a mild shock delivered near the eye will elicit both a blink response and fear (indexed, in part, by a change in heart rate). With short CSs (typi- cally those terminating in a US less than 1 second after CS onset), the CS elicits a protective blink of the eye near the site where the US is delivered. With longer CSs (e.g., 6.75 seconds or more), the CS elicits a change of heart-rate response (instead of the blink) that suggests fear (VanDercar & Schneiderman, 1967). Unlike the blink response, conditioned fear does not depend on where the US is actually delivered (either eye or a hindleg will do). One effect of fear is to potentiate the blink. Bombace, Brandon, and Wagner (1991) found that when a 1-second CS that elicited the blink was presented within a 30-second CS that was separately associated with shock,

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it elicited the blink more strongly (see also Brandon & Wagner, 1991). The phenomenon is similar to fear potentiated startle, in which a fear CS poten- tiates the acoustic startle reflex (e.g., Davis, 1992; see also Brandon, Bombace, Falls, & Wagner, 1991; McNish, Betts, Brandon, & Wagner, 1997). Although the long CS elicited no blink, it presumably elicited fear. In the defensive system, as in others, the nature of the conditioned response depends on CS duration, and CSs that have a distal temporal rela- tion with the US can potentiate responding to CSs with a more proximate relation.

Research on behavior systems thus suggests that the nature of the con- ditioned response depends on the duration and qualitative aspects of the signal, and that the strength of a response can be influenced by stimuli in the background.

CONTEXT, CS DURATION, AND THE NATURE
OF THE AVERSIVE CR: ANXIETY, FEAR, AND PANIC

The general characteristics of how behavior systems are organized have implications for emotion. Like other parts of the behavior system, emotions function to deal with the US (cf. Scherer, Chapter 13). In this light, it seems apparent that the type of emotion elicited by a signal may depend on the temporal and qualitative nature of the signal that triggers it. Conceiv- ably, such flexibility and variability may contribute to the difficulty in finding a stable physiological signature for the different emotions (e.g., Cacioppo, Berntson, Larsen, Poehlmann, & Ito, 2000; Zajonc & McIntosh, 1992).

Bouton et al. (2001) accepted a behavior systems view in a condition- ing account of panic disorder, the anxiety disorder in which panic attacks occur, intensify, and become debilitating with experience. They assumed, as had others before them, that out-of-the-blue panic attacks can be potent USs that generate aversive conditioning. Panic disorder develops in vulner- able individuals at least in part because they learn to fear the next panic attack (e.g., Goldstein & Chambless, 1978; Wolpe & Rowan, 1988). But in considering the behavior systems literature, Bouton et al. suggested that the attacks may worsen for two reasons. First, proximate cues connected with the early onset of a panic attack (e.g., the feeling of a pounding heart, feeling dizzy) become associated with the rest of the attack. These proxi- mate cues, which are closely correlated with, and even resemble aspects of, the panic attack, acquire the ability to evoke panic as a conditioned response. Recent work studying drug effects confirms that the onset of an

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event can serve as a CS for the rest of the event (e.g., Kim, Siegel, & Patenall, 1999; Sokolowska, Siegel, & Kim, 2002).

The second mechanism that increases the intensity of panic attacks is more like the one we have just seen in other behavior systems. Bouton et al. supposed that certain CSs that signal a panic attack more remotely in time (e.g., the shopping mall) might come to elicit a preparatory emotional conditioned response (CR), anxiety, a forward-looking fear reaction that “prepares” the organism for the next panic attack. Anxiety differs from the panic elicited by a shorter, proximate CS; the latter is designed to deal with a traumatic event that is highly imminent or even already in progress. But equally important, the conditioning of the long-duration anxiety CR would be expected to potentiate the next panic attack, in the same way that longer-duration cues potentiate copulatory, eyeblink, and startle responses.

A distinction between anxiety and panic is consistent with at least two types of evidence. First, quantitative analyses of patient symptoms have distinguished between states of extreme fear and autonomic arousal that seem consistent with panic and a different state of apprehension and worry with tension that appears more like anxiety (e.g., Brown, Chorpita, & Barlow, 1998). Second, research in behavioral neuroscience has begun to separate at least two aversive motivational systems. For example, Michael Davis and his colleagues have distinguished between anxiety and fear at both the behavioral and neural levels (e.g., Davis & Shi, 1999; Davis, Walker, & Lee, 1997). In the Davis conceptualization, although there is considerable overlap in the effects of these two states, fear is a relatively short-term state that is activated by Pavlovian CSs, whereas anxiety is a lon- ger-term state that is activated by more diffuse and unlearned cues. Fear appears to be mediated by activity in the amygdala; for instance, lesions of the amygdala abolish fear conditioning, including fear conditioning as mea- sured by the potentiated startle response (e.g., Hitchcock & Davis, 1986; Kim, Campeau, Falls, & Davis, 1993; see also Fanselow, 1994; Kapp, Whalen, Supple, & Pascoe, 1992; LeDoux, 1996). In contrast, amygdala lesions do not abolish the rat’s preference for covered arms in a plus maze, a widely accepted measure of anxiety (Treit et al., 1993). Amygdala central nucleus lesions also do not abolish startle responding potentiated by extended exposure to a bright light or by the infusion of corticotropin releasing hormone (Davis et al., 1997), both of which create a longer-lasting anxiety, as suggested by the fact that they are reduced by anxiolytic drugs (Walker & Davis, 1997a; Swerdlow, Geyer, Vale, & Koob, 1986). Impor- tantly, the latter two effects are abolished by similar lesions of another part of the extended amygdala, the bed nucleus of the stria terminalis (BNST; Davis et al., 1997; Walker & Davis, 1997b); these lesions have no effect on

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fear conditioning, however (Davis et al., 1997; Hitchcock & Davis, 1991; LeDoux, Iwata, Cicchetti, & Reis, 1988; Walker & Davis, 1997b). The pat- tern thus begins to suggest a double dissociation between behavioral tasks affected by lesions of the amygdala (fear) and the BNST (anxiety).

Although anxiety might not always depend on learning (e.g., a bright light might presumably evoke anxiety in a rat as an unconditioned re- sponse), recent research in my laboratory suggests that it can be learned and elicited by long-duration CSs. In recent experiments, Jaylyn Waddell, Richard Morris, and I have compared the effects of BNST lesions on aver- sive conditioning with short and long signals for shock (Waddell, Morris, & Bouton, submitted for publication). In one experiment, over a series of ses- sions, rats received presentations of a clicking noise that ended in a moder- ately intense, 1-mA, 0.5-second foot shock. For one set of animals, the dura- tion of the noise was 60 seconds, the standard duration used in fear conditioning experiments in my laboratory. For another set of rats, the duration of each noise was 600 seconds. For these animals, the CS signaled the US at a long enough distance that we did not expect it to generate a strong fear CR; it might evoke conditioned anxiety. Several weeks before conditioning, some of the animals in each condition received excitotoxic lesions of the BNST. Control groups received sham lesions in which they underwent similar surgeries, but no excitotoxins were delivered to the brain. The experiment thus asked whether the BNST affects aversive con- ditioning, and more importantly, whether it selectively affects a CS that has a long temporal relationship with the US.

We used the conditioned suppression method in which aversive condi- tioning was measured in terms of the extent to which the CS suppressed an operant lever-pressing response reinforced by food (Estes & Skinner, 1941). With the 1-minute CS, the lesion did not have a significant impact on fear conditioning, as is consistent with previous research (Hitchcock & Davis, 1991; LeDoux et al., 1988; Walker & Davis, 1997b). But the picture was dif- ferent with the 10-minute CS. In this case, the BNST lesion significantly reduced conditioning. The lesions had no effect on baseline lever-pressing rates. The results were thus consistent with the idea that long-duration sig- nals, but not shorter-duration signals, arouse an anxiety state that might be mediated by the BNST. Although the 10-minute CS evoked less suppression than the 1-minute CS did, the results of an additional experiment suggested that the BNST lesion still had an impact on 10-minute CSs that evoked more suppression. If the BNST plays a role in aversive CR to long-duration stimuli, it may well be that the duration of the CS, rather than merely a weak level of conditioned suppression, is what matters.

Of course, long-duration contextual cues are also a candidate for anxi- ety conditioning. It would be especially interesting to identify a situation in

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which a contextual anxiety cue potentiates a conditioned fear response in a manner analogous to that suggested for panic disorder (Bouton et al., 2001). One situation in which a context’s direct association with a US augments fear of a CS is reinstatement (e.g., Bouton & Bolles, 1979b; Rescorla & Heth, 1975). In reinstatement, the subject first receives fear conditioning (e.g., tone–shock pairings) and then extinction (tone alone presentations) in several daily sessions. Although the original tone–shock pairings allow the tone to trigger fear, extinction undoes that effect; it eliminates the learned fear. However, in reinstatement, the shock is presented several times alone—independently of any behavior, and independently of the tone CS. With our typical methods, these shock presentations are sparse and widely spaced in time (i.e., 4–8 shocks are presented in a 90-minute session). But when the tone is presented alone, typically the next day, it elicits fear again. After extinction, exposure to the US again reinstates fear of the CS.

Many experiments in my laboratory have shown that reinstatement is an effect of context conditioning. When the reinstating shocks are pre- sented, the animal associates them with the current context. This creates a dangerous context, and the presence of that danger when the tone is next presented somehow triggers fear of the extinguished CS. The main evi- dence supporting this idea is that when the shocks are presented in a differ- ent, irrelevant context, they produce no reinstatement (e.g., Bouton, 1984; Bouton & Bolles, 1979b; Bouton & King, 1983; Frohard, Guarraci, & Bou- ton, 2000; Wilson, Brooks, & Bouton, 1995). Thus, for reinstatement to occur, the CS must be tested in the context that has been made dangerous by recent exposure to the US.

Despite clear evidence that the context was important, in our early reinstatement experiments few rats showed overt signs of fear when they were returned to the context on the test day. Baseline lever-pressing rate was not significantly suppressed (see also Rescorla & Heth, 1975), and the animals showed little freezing, the classic sign of fear in the frightened rat. To provide an independent measure of contextual conditioning, we there- fore attached side compartments to the Skinner boxes. For the first 6 min- utes of the session, we allowed the rats to choose between sitting in the side box or earning food pellets while lever pressing (on a variable interval rein- forcement schedule) in the Skinner box. Access to the side box was pre- vented once the test was over. Compared with rats shocked in another box, the rats that had been shocked in the current Skinner box preferred to sit in the side compartment, and the degree of this preference was strongly cor- related with the strength of reinstatement that was observed when the CS was presented a minimum of 15 minutes later (Bouton, 1984; Bouton & King, 1983). However, as usual, there was little overt freezing or suppres- sion of the lever-pressing baseline.

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I now see this pattern as a possible consequence of the fact that the long-duration context evoked anxiety rather than fear. Freezing is primarily a response of the rat when it perceives a relatively high level of shock immi- nence. As a test of this, we have further examined the effect of BNST lesions on the reinstatement effect (Waddell et al., submitted for publica- tion; see also Frohardt, 2001). Excitotoxic lesions were created a few weeks before the behavioral part of the experiment. The lesion had no impact on either fear conditioning or extinction with the 60-second CS. However, it significantly attenuated the reinstatement effect: After fear conditioning and then extinction, eight shocks in a 90-minute session reinstated fear to the CS in control subjects. But animals with BNST lesions showed no rein- statement effect. The results are consistent with our idea that the context might evoke a conditioned anxiety state that can potentiate (reinstate) fear of an extinguished CS. The CS and the context thus appear to elicit differ- ent emotional states that (1) depend differentially on the BNST, a brain area linked to other indices of anxiety, and (2) interact in a way predicted by a behavior systems view (Bouton et al., 2001).

We had previously shown that lesions of the hippocampus (Frohardt et al., 2000) or disruption of one of its major outputs, the fimbria fornix (Wil- son et al., 1995), could also abolish the reinstatement effect. Those results were consistent with a fair amount of research indicating that the hippo- campus is involved in contextual learning (e.g., Kim & Fanselow, 1992). But our experiments also indicated that an intact hippocampus or fornix is not necessary for at least one other important context learning effect (the renewal effect, described below; Frohardt et al., 2000; Wilson et al., 1995). Details of the neural circuitry are beyond the scope of this chapter, but the point of our work with the BNST is that it is consistent with a role for con- textually controlled conditioned anxiety. Like other possible behavioral indicators of anxiety, conditioning of the context (by our typical, fairly sparse reinstatement shock presentation schedule) or a long-duration noise CS, may depend on the BNST.

One question is whether there is a one-to-one correspondence be- tween anxiety and fear dissociated here and in the Davis laboratory, on the one hand, and anxiety and panic emphasized by Bouton et al. (2001), on the other. The answer may be “no.” It seems possible that the panic response elicited by an extremely proximate early-onset cue might be rather differ- ent from the anticipatory fear evoked by a CS whose onset precedes the US by 60 seconds. Fanselow (e.g., 1994) has emphasized the distinction between the freezing elicited by such a CS and the activity burst that is directly elicited by shock. The activity burst responds to an aversive US that is already in progress, which might also be true of panic responses. Future research may therefore support a separation between three aversive

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emotional states: anxiety (supported by a very long CS), fear (supported by a less distal CS), and panic (perhaps supported by an extremely proximate and biologically prepared CS). Interestingly, the three states loosely corre- spond to the general search, focal search, and consummatory modes that have been proposed in appetitive systems.

INHIBITION AND THE CONTEXTUAL CONTROL OF CONDITIONED RESPONDING

Thus far I have focused on the emotional effects of contexts and CSs that are directly associated with a US. However, contexts can also control emo- tional behaviors through another mechanism that is less direct. To illus- trate, consider the renewal effect, another important effect in which the context controls the response to the CS. In the simplest demonstration of renewal (e.g., Bouton & Bolles, 1979a; Bouton & King, 1983), rats receive fear conditioning with a tone in one context (Context A) and then extinction (tone-alone trials) in either the same context or a different context (Context B). Once extinction is complete, so that the animals are no longer afraid of the CS, they are returned to the original context, Context A, where they receive further tests of the CS. At this point, the animals extinguished in the other context (Context B) show a strong return (renewal) of fear. The renewal effect, like reinstatement, indicates that extinction does not destroy the original learning, but instead leaves the CS sensitive to the con- text.

One of the interesting things about renewal is that it does not require that Context A or B have demonstrable direct associations with the US. Many conditioning models would allow Context A to acquire direct associa- tions with the US during conditioning, and Context B to acquire inhibitory associations with the US during extinction (e.g., Rescorla & Wagner, 1972). Such associations would then add or subtract from the associative strength of the CS to generate performance. Although direct context–US associa- tions are no doubt learnable, none of our tests provided evidence that they are necessary (or sufficient) to influence response to the CS in our standard procedures (see Bouton, 1991, for a review). In this sense, the renewal effect is different from reinstatement, which is mediated by a direct associ- ation between the context and the US. In renewal, the contexts appear to work as cues that retrieve the current “meaning” of the CS, or its current relation to the US, in the way occasion setters do (e.g., Holland, 1992; Schmajuk & Holland, 1998; see Pearce & Bouton, 2001). Casually speak- ing, Context A retrieves or activates the CS–US association, and Context B retrieves or activates a CS–no-US association. In this sense, they “disam-

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biguate” the CS’s current meaning. A more detailed discussion of the mechanism is provided by Bouton and Nelson (1998).

There are several versions of the renewal effect. In the “ABA” effect just described, the animal is returned to the original conditioning context (Context A) after extinction in a different context (Context B). But we and others have also shown an ABC renewal effect, wherein tests in a neutral third context (C) also cause a renewal of the original conditioned response (Bouton & Bolles, 1979a; Bouton & Brooks, 1993). We have also observed an AAB renewal effect, wherein conditioning and extinction occur in the same context (A), and testing occurs in a second context (B) (Bouton & Ricker, 1994). The fact that ABC and AAB renewal can occur indicates that conditioning (fear of the CS) generalizes more readily to a new context than extinction (inhibition of the CS) does.

In fact, one especially important discovery in our work on the renewal effect is exactly that: Extinction is more specific to its context than conditioning is. This is also evident in the ABA renewal design. After conditioning in Context A, we find that the CS elicits just as much fear in the group that then receives extinction in Context B as the group that receives extinction in Context A. That is, switching the context after conditioning has surprisingly little impact on fear of the CS, even in the presence of independent evidence that the animals recognize the differ- ence between the contexts (e.g., Bouton & Brooks, 1993). We have seen this pattern in many experiments, regardless of the motivational system. For example, even if we study appetitive (tone–food) conditioning instead of fear (tone–shock) conditioning, the switch after conditioning has no effect, but the switch after extinction does (e.g., Bouton & Peck, 1989). The context is more important after extinction than it is after original conditioning.

Interestingly, our research on reinstatement provides converging sup- port for this conclusion. Although the contextual conditioning created by shocks delivered after extinction has a clear effect on extinguished fear of the CS, the same contextual conditioning created by the same shock expo- sure after conditioning alone has surprisingly little effect on fear of the CS. For example, we have compared groups that received a small number of fear conditioning trials with other groups that received conditioning and then partial extinction to a point where the CS elicited the same amount of fear (Bouton, 1984). Animals in both sets of groups then received shocking in the same or different contexts, and it created the pattern of contextual fear (context preference) that I described earlier. Although there was clear context-dependent reinstatement in the extinguished rats, there was no evidence that the same contextual conditioning had an effect on fear of the

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CS that had not been extinguished. It was as if contextual conditioning was not relevant until after extinction. Subsequent experiments showed that the extent to which CS fear was increased by contextual conditioning depended on the extent to which fear of the CS was “depressed” by extinc- tion during the test (Bouton & King, 1986). Anxiety conditioned to the con- text does not potentiate fear automatically or unconditionally; it seems to remove the inhibition created by extinction.

The fact that extinction is more context dependent than conditioning led us to ask whether inhibitory learning is generally context specific. Byron Nelson and I studied this question in experiments with the “feature- negative” procedure (Bouton & Nelson, 1994; Nelson & Bouton, 1997). In this procedure, one CS (X) is paired with a US on trials when it is presented alone, but without the US on trials when it is presented with another CS (Y), that is, X+, YX–. After repeating and intermixing the two types of trials, Y develops purely inhibitory properties—it predicts the absence of a US that is otherwise presented with X. But Nelson and I discovered that inhi- bition to Y is not disrupted by context change: Like simple excitation, inhi- bition to Y generalized nicely across contexts. Instead, the ease with which responding to X could be inhibited was reduced when the context was switched. Nelson (2002) then confirmed what we had long suspected: that it is the second thing learned about the CS that is specific to its context. Both inhibition and excitation generalized across contexts, unless they were the second thing learned about the CS. The system thus seems to code the second thing learned about the CS as a conditional exception to a rule. In effect, the context is especially important in controlling retroactive inhibi- tion. The fact that the inhibitability of responding to X was lost is also con- sistent with this rule. Generally speaking, an association you have learned to inhibit in one context is more difficult to inhibit in another.

RELAPSE AND THE MAINTENANCE OF EMOTION

Renewal and reinstatement have clear implications for relapse after ther- apy (e.g., Bouton, 2000, 2002; see also Quigley & Barrett, 1999), which is theoretically based on extinction. One should be aware that an emotion generated by an extinguished trigger cue can always return, depending on the background. But the idea is more general than this. Up to this point, I have stuck with a fairly conventional definition of context, namely, the physical background cues provided by the room or apparatus in which the CS and US are presented. In reality, though, “context” is probably much more than that. For instance, I have argued that learning and remembering

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are also sensitive to the gradually changing context provided by the passage of time (e.g., Bouton, 1993). This is not a controversial idea within the area of human memory, where it is not uncommon to think of forgetting over time as due to a growing mismatch between the contexts present during learning and testing. In this light, the context dependency of extinction explains spontaneous recovery, one of the earliest phenomena connected with extinction that suggests that extinction is not unlearning (Pavlov, 1927). Our idea is that spontaneous recovery is merely the failure to retrieve extinction outside the temporal extinction context. That is, just as we find a renewal effect if conditioning, extinction, and testing are con- ducted in physical contexts A, B, and C, so we may find spontaneous recov- ery when conditioning, extinction, and testing are conducted at times 1, 2, and 3. Spontaneous recovery is the renewal effect that occurs when the ani- mal fails to retrieve extinction in a new temporal context.

One prediction of this view is that, if spontaneous recovery and renewal both result from failures to retrieve extinction, then both should be abolished by presenting a retrieval cue that reminds the animal of extinc- tion just before the test. Cody Brooks and I found this to be the case (Brooks & Bouton, 1993, 1994). We found that a cue that was presented during the intertrial intervals of extinction could attenuate the effects if it was presented just before the test (see also Brooks, 2000; Brooks & Bowker, 2001). That sort of result supports the idea that spontaneous recovery and renewal are caused by the same mechanism—that is, a failure to retrieve extinction. It also suggests that either form of relapse can be reduced or perhaps prevented by reminders of the extinction/therapy experience. Interestingly, Collins and Brandon (2002) also found that a retrieval cue reduced renewal in human social drinkers when they tested alcohol cues in a context that was different from the one in which extinction exposures had taken place.

Another kind of context that is important is the interoceptive context produced by ingestion of a drug. There is an extensive literature on state- dependent retention effects, in which memory for material learned while under the influence of a drug is best remembered in that drug state. We have shown state-dependent fear extinction effects. For example, when fear conditioning occurs while the animal is in the sober state but fear extinc- tion is conducted while the animal is under a benzodiazepine tranquilizer chlordiazepoxide (Librium) or diazepam (Valium), there is a strong, dose- dependent renewal effect that occurs when the animal is tested again in the sober state (Bouton, Kenney, & Rosengard, 1990). In effect, the drug works as Context B in the ABA renewal design. Cunningham (1979) has shown a similar effect of alcohol, and we have recently replicated and extended the

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findings with midazolam, another benzodiazepine that is often used in human anesthesia protocols (Pain, Oberling, & Bouton, 2001). A recent study with human subjects suggests that caffeine can also function in a sim- ilar way when spider fear is extinguished while patients are under the influ- ence of caffeine (Mystkowski, Mineka, Vernon, & Zinbarg, 2003). It thus seems clear that renewal effects can be obtained with interoceptive drug contexts.

Such results have an obvious clinical implication: Using a drug to facil- itate anxiety therapy can potentially backfire, creating relapse when the cli- ent encounters the CS again in the absence of the drug. Perhaps consistent with this possibility, there is evidence that the combination of drug and cognitive behavior therapy is less effective at long-term follow-up than is cognitive behavior therapy alone (Barlow, Gorman, Shear, & Woods, 2000). There is a subtler implication as well. State-dependent extinction would serve to insulate a person from the beneficial effects of natural extinction. That is, a person might take an anxiolytic drug to reduce anxiety; drug tak- ing would be reinforced by anxiety reduction. But state-dependent extinc- tion might preserve the original anxiety, which might ordinarily undergo some extinction through natural exposure to the anxiety stimulus. Thus the drug might paradoxically maintain the anxiety that motivates drug use. Renewal effects might contribute to the long-term maintenance of the dis- order in addition to generating relapse.

Recent studies in my laboratory have isolated a new kind of renewal effect that might also contribute to the maintenance of emotion and emo- tional disorders. Bouton, Frohardt, Sunsay, and Waddell (submitted for publication) gave rats repeated CS–shock pairings in one context over sev- eral sessions. (There were additional daily sessions in which a different CS received the same treatment in a different context.) What we often (but not always) observed is a phenomenon that sometimes reveals itself in fear con- ditioning experiments: The acquisition of fear reached a maximum at a point in training and then began to decline, as if the fear response began to extinguish a little, despite continued pairings of the CS and the shock. Although such “nonmonotonic” learning curves have been observed in sev- eral laboratories, we have an incomplete understanding of them at the pres- ent time. Our own experiments indicate that they do not depend on the gradual development of “inhibition of delay,” in which the animal learns to time the shock and confine its fear to late parts of the CS and extinguish fear to early parts. In addition, the decline is not due to recruitment of an endorphin response that makes the shocks less painful; administration of the opiate antagonist naloxone does not appear to abolish the effect (Vigorito & Ayres, 1987). Instead, the effect is usually attributed to the

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acquisition of an ill-defined adaptation process that allows the rat to cope with the US and/or fear.

One of the interesting things about the adaptation process is that, like extinction, it appears to be specific to the context in which it develops. At the end of experiments in which we have observed nonmonotonic fear learning curves, a context switch caused a significant increase in fear of the CS. Over a series of experiments, we discovered that the strength of this increased fear was correlated with the degree to which fear had declined from its maximum point to the start of testing (Bouton, Frohardt, Sunsay, & Waddell, submitted for publication). That is, when adaptation was evident, there was an increase in fear when the context switched. When less adapta- tion was evident, there was less increase in fear. Thus what appears to be lost with a switch in context is the animal’s adaptation response. And fur- ther, the adaptation is to the CS or to the fear that it elicits; notice that the tests were of the CS, not the US, in the different context. As in extinction, the animal’s fear of the CS is renewed if the context is switched after adap- tation has occurred. The second thing learned about a CS is again attenu- ated by a context switch.

These findings might have implications for how organisms express and regulate emotion. It is interesting to think about a panic patient who expe- riences repeated pairings of a pounding heart and panic attacks while at home. With repeated attacks, she learns to panic when her heart begins to race, but she might eventually also learn to cope and adapt to the fear, to some extent. On the other hand, if she were now to encounter the CS (the pounding heart) in another context such as the shopping mall, the coping process would be lost, and a very strong panic response might result. Stronger fear outside the conditioning context might motivate the person to stay at home—and thus provide a mechanism for agoraphobia. The fact that coping and extinction processes are relatively context-specific could easily contribute to the maintenance and persistence of emotional disorders.

SUMMARY

This chapter has sketched a fairly complex role for context in the control of emotion and behavior. In the first part I considered consequences of an organism associating a context with the US, arguing that classical condi- tioning, and the conditioning of emotional processes, engages whole- behavior systems. Based on what we know about the organization of such systems, cues that have different temporal relationships with the US will evoke different kinds of responses, because the type of response that pays when the US occurs immediately may not have the same value when the

Contextual Control of Anxiety, Fear, and Panic 221

US is due to occur more remotely in time. The argument suggests that long-duration contextual cues—with a relatively distal temporal relation- ship with a frightening US—might elicit emotional responses that are dif- ferent from those evoked by more proximate cues. A context might elicit anxiety, a forward-looking response designed to deal with the threat some- time in the future, whereas proximate cues might elicit panic, a kind of response designed to deal with the traumatic US now (Bouton et al., 2001). The existence of at least two aversive motivational states is consistent with a behavior systems perspective, with the analysis of symptomatology in anx- ious patients (Brown et al., 1998), and with neurobiological evidence sug- gesting at least two dissociable aversive motivational states (e.g., Davis et al., 1997; Fanselow, 1994). I have also described preliminary evidence from my laboratory suggesting that long-duration cues, including contextual cues, can elicit an aversive motivational state that depends on the BNST, an area in the extended amygdala thought to mediate anxiety. Anxiety condi- tioned to a context may exacerbate the emotion elicited by a fear CS— especially one that has been through extinction.

Other research has uncovered a role for context that does not depend on a direct context–US association. Work in my laboratory suggests that extinction itself is coded as specific to its context, as if the system were designed to use contextual information primarily when the CS acquires a second meaning. This means that emotional responding evoked by an extinguished CS is on unless the context switches it off. This role of context may be played by many different kinds of background stimuli, which seem to be important in forms of retroactive interference other than extinction, including counterconditioning (see Bouton, 1994) and the adaptation and coping effect that appears to emerge with continued fear conditioning. Like other aspects of the behavior system, the context’s role can be seen as adap- tive; the learning and memory system seems designed to preserve first- learned information, which on a statistical basis might provide the better sample of the true state of the world than second-learned information (Bou- ton, 1994). All of these processes may be expected to contribute to the evo- cation of anxiety, fear, and panic.

ACKNOWLEDGMENTS

Manuscript preparation and the yet-unpublished research reported here were sup- ported by Grant No. RO1 MH64847 from the U.S. National Institute of Mental Health. I thank Erik Moody, Ceyhun Sunsay, William Timberlake, Jaylyn Waddell, and Amanda Woods, along with Lisa Feldman Barrett and Piotr Winkielman, for their comments.

222 UNCONSCIOUS EMOTIONAL BEHAVIOR

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PART IV
The Experience of Emotion

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ThHeEInEdXePteErmRIinEaNcyCoEf VOaFleEncMeOTION

CHAPTER 10

Emotion Experience and the Indeterminacy of Valence

LOUIS C. CHARLAND

Words are like the film on deep water. —LUDWIG WITTGENSTEIN, Notebooks

(1914–1916, p. 30.5.15)

Many aspects of emotion are said to be valenced and labeled positive or negative. Indeed, valence is generally considered to be a central feature of emotion. For example, it is probably not an exaggeration to say that “many investigators consider the valence of emotions to be the single most impor- tant dimension of affective experience” (Fossum & Barrett, 2000, p. 679). Yet, despite its theoretical proclivity, the philosophical status of valence in emotion science remains largely unexplored. What is valence? Is it an objective, intrinsic property of emotion experience, a “given” that is discov- ered? Or is it instead an outcome of emotion experience, a “product” that is subjectively created in consciousness?

In what follows, emotion experience will be defined rather strictly. Fol- lowing John Lambie and Anthony Marcel, “emotion experience” is under- stood as “referring to and including (1) the phenomenological aspect of an emotion state, and (2) second-order awareness of this experience, although the latter is not always present” (Lambie & Marcel, 2002, p. 230). An emotion state, in turn, is defined as “what is common to a certain set of evaluative representations, attitudinal behaviors, and physical states (pp. 229–230). The definition is meant to capture the bare minimum of

231

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1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

My discussion deals with emotion valence (the idea that emotions can be classi- fied as positive or negative) and affect valence (the idea that emotional feelings or affects can be classified as positive or negative). The main focus of the dis- cussion is affect valence, although there are implications for emotion valence. The scope of my discussion extends to all studies and theories that rely on the idea that we can classify emotions and emotional feelings or affects as positive and negative.

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

In my chapter emotion experience is understood as “referring to and including (1) the phenomenological aspect of an emotion state, and (2) second-order awareness of this experience, although the latter is not always present” (Lambie & Marcel 2002, p. 230). Emotion state is defined as “what is common to a cer- tain set of evaluative representations, attitudinal behaviors, and physical states (pp. 229–230). This definition is meant to capture the bare minimum of what “people are referring to in mutually understood discourse that uses the term ‘emotion’ ” (p. 230).

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

Following Lambie and Marcel (2002), my account relies on the distinction between first-order phenomenology and second-order awareness in conscious emotion experience. I propose an argument that shows that affect valence is limited to conscious awareness only. This argument makes the notion of uncon- scious affect valence extremely problematic, and that of nonconscious affect valence impossible. My argument also implies that the attribution of valence to objects and stimuli outside of, or apart from, conscious awareness is metaphori- cal only. This position creates problems for studies or theories that rely on valence as if it were an objective, reliable property of external objects and stim- uli themselves.

what “people are referring to in mutually understood discourse that uses the term ‘emotion’ ” (p. 230). The principal reason for introducing this particular conception of emotion experience is its important distinction between first-order phenomenology and second-order awareness. That dis- tinction plays a central role in our discussion.1

Technically stated, the central claim of this chapter is that valence understood as hedonicity (pleasure or displeasure) is not an intrinsic objec-

The Indeterminacy of Valence 233

tive property of felt affect in first-order emotion experience. Rather, it is a property of second-order emotion experience that is highly variable and fundamentally indeterminate. Because the scientific literature on valence and affect is so idiosyncratic and complex, explaining and defending this thesis requires considerable background preparation. But intuitively the point should be clear. Very simply, feelings are not intrinsically pleasant or unpleasant in themselves. Their “positive” (pleasant) or “negative” (unpleasant) character is not an objective property that is intrinsic to them. Instead, valence is fixed by the process of attending to feelings in second- order awareness. Some element of “interpretation” appears to be involved (Lambie & Marcel 2002, pp. 220, 244).

The culmination of this argument is called the indeterminacy thesis. According to this thesis, there is no intrinsic objective scientific fact about what the valence of a particular emotional affect or feeling is apart from its elaboration in second-order awareness in emotion experience. Valence is objectively indeterminate because it is impossible to report or measure it without at the same time changing it. The exact character and personal meaning of an emotional feeling is created in second-order awareness by attention. But attention does not create the underlying phenomenology out of which valence is created. Neither does it create the nonconscious mech- anisms that underlie valence. Here it is crucial to distinguish between the conscious subjective experience of valence and the nonconscious mecha- nisms that underlie it.

One important consequence of the indeterminacy thesis is that de- scriptive structural models of the valence dimension of affect probably fall much shorter of their explanatory goals than is typically thought. This is because the indeterminacy thesis poses serious problems for the idea that felt valence is an objective commodity that can be measured reliably. But that is a central assumption of many scientific efforts to explain affect (Carroll, Michelle, Yik, Russell, & Barrett, 1999; Barrett, Chapter 11; Rus- sell, 2003; Watson & Tellegen, 1985).

DESCRIPTIVE STRUCTURAL THEORIES OF AFFECT

To get a clearer grasp of what is at stake in our opening questions, consider the well-known circumplex model of emotion (Russell, 1980; Barrett & Russell, 1998). According to that model, emotion experience is said to include a component of “affect,” which informally is referred to as “feel- ing.” Lisa Feldman Barrett probably speaks for many emotion researchers when she says that “self-report represents the most reliable and possibly only window that researchers have on conscious, subjective, emotional experience” (Barrett, 1996, p. 47). She and many others employ self-reports

234 THE EXPERIENCE OF EMOTION

to inquire into valence. The conscious felt subjective experience of valence in these discussions is construed as a component of affect—which, in turn, is considered to be a fundamental constituent of emotion experience (Rus- sell, 2003).

Certainly, much valuable work has been done in mapping the descrip- tive structure of valence and other components of affect using self-reports (Barrett & Russell, 1998; Cacioppo & Berntson, 1999; Carroll et al., 1999; Larsen & Diener, 1992; Russell, 1980; Watson & Tellegen, 1985). It is in- teresting that the word description is often used in characterizing the epistemological aim of these studies. Thus the aim is to describe affect (Carroll et al., 1999, p. 14; Russell & Carroll, 1999, p. 5; Larsen, MacGraw, Meter, & Cacioppo, 2001, p. 692). What is sought is an explanatory model of the “descriptive structure” of affect (Barrett & Russell, 1998, p. 967; Carroll et al., 1999, p. 14).

But how can description capture something that is inherently eval- uative? How can we hold valence still, to measure and describe it objec- tively, without at the same time changing its normative character? Of course, evaluations can sometimes be treated descriptively: thus “formally, an evaluation is a valenced (i.e., positive or negative judgment about a stim- ulus” (Fossum & Barrett, 2000, p. 669; emphasis added). But resorting to evaluative judgments does not solve our problem. The reason is that, in substance as opposed to form, valence is a very peculiar characteristic of conscious experience. To explain why, it is helpful to distinguish two differ- ent but related senses of the term valence: (1) a pretheoretical, substantial, experiential one; and (2) an abstract, theoretical, formal one. Note that it is the explanation and description of the experience of valence that is at issue here, not the explanation and description of the nonconscious mechanisms which may correspond or contribute to it (Lambie & Marcel, 2002, p. 227; Larsen et al., 2001, p. 686).

On a pretheoretical experiential level, valence is a felt conscious ten- dency or orientation toward or away from features of experience. This is reflected in the etymology of the term, which signifies a power or capacity to react. It is crucial that valence is not viewed simply as the experience of brute and blind physiological urges. On the contrary, it is laden with per- sonal meaning and is inseparably tied to an experience of the personal sig- nificance of what events in the environment mean for us. This personal meaning is what makes valence fundamentally evaluative and interpretive. Through valence, we feel moved toward or away from things, in a manner that is accompanied by an experience of what those things mean to us per- sonally. This pretheoretical conscious felt sense of valence is what the sci- entific study of valence is meant to explain. It serves as the explanandum for many theories of valence. Other starting points are possible. But this one has the notable distinction of starting with the assumption that,

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paradigmatically, valence is a property of conscious emotion experience. The question then is whether objective descriptive methods that employ self reports can adequately capture the evaluative and interpretive core of this subjective phenomenon. How well can self-report measures succeed in capturing this qualitative aspect of emotion experience, the subjective “qualia” that self-reports are allegedly about (Scherer, Chapter 13). How can science capture what it is that these reports allegedly report (Scherer, Chapter 13)?

We can now restate our opening questions. Is the special felt qualita- tive tendency in valence, as it is structurally represented in descriptive the- ories, an intrinsic feature of emotion experience as such; that is, something that exists prior to the self-reports that describe it? Or is it instead created and structured by features of second-order awareness, such as these self- reports? The argument here is that valence is created by attention in sec- ond-order awareness. There is nothing scientifically objective or precise that we can say about valence apart from its elaboration in second-order awareness. Second-order awareness does not create the underlying phe- nomenology of emotion experience, but it does shape and articulate what exactly it means to us. This conclusion would appear to threaten the scien- tific foundation of descriptive theories of affect, because it undermines the objectivity of the phenomenon they claim to study. It also contradicts the driving assumption of several dominant neuroscientific theories of valence, according to which valence is an intrinsic objective property of affective experience.

Affect and valence are the central terms involved in our discussion; both have widely variable uses. There are several options available for defining affect, and the matter is partly subject to stipulation (Carroll et al., 1999, p. 21; Russell & Carroll, 1999, p. 7). For present purposes, affect is initially defined as the conscious felt experience of emotion (Berkowitz, 2000, p. 4; Cacioppo & Bernston, 1999, p. 134; Russell & Carroll, 1999, p. 3). Affects, then, are “subjectively experienced feelings” (Buck, 1999, p. 301). In some theories, affect is said to consist of two dimensions; valence and activation; the latter is also sometimes referred to as arousal or activity. This, for example, is how affect is understood in the circumplex model of emotion (Russell, 1980; Feldman, 1995): It treats valence as a component dimension of affect, which in turn is treated as an element of emotion expe- rience.

The circumplex model of emotion and theories like it generally treat valence as a component of affect; other approaches treat valence as an attribute of emotions (Frijda, 1986; Lazarus, 1991; Ben-Ze’ev, 2000; Prinz, 2004). Accordingly, one of our first tasks is to clarify the distinction between affect valence (i.e., valence attributed to individual distinct affects) and emotion valence (i.e., valence attributed to individual whole emotions). This

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distinction will enable us to focus on affect valence without, hopefully, inviting too much confusion. It is the valence of the subjective feelings or affects in emotion experience with which we are concerned, not the valence of emotions as such.

DISTINGUISHING EMOTION VALENCE AND AFFECT VALENCE

Valence can be defined as the positive or negative “charge” associated with a particular physical or mental state, or a particular combination of these. The view that individual emotions have valence is widespread in both philosophical and psychological theories of emotion (e.g., Ben-Ze’ev, 2000; Gordon, 1987; Lazarus, 1991; Ortony, Clore, & Collins, 1988; Prinz, 2004). In this case, valence is held to be a property of individual emotions. Thus it is often said that fear is a negative emotion, whereas, joy is a positive one. Call this emotion valence. Normally, emotion valence is considered to be an intrinsic objective property of individual whole emotions. A given emotion is simply said to be positive or negative.

Sometimes it is not individual whole emotions that are said to be posi- tive or negative but, rather, individual affects (e.g., Barrett, 1996; Larsen & Diener, 1992; Russell, 1980; Watson & Tellegen, 1985). In this case, valence is held to be a property of individual affects. Thus it is often said that feel- ing frightened is a negative affect, whereas feeling joyful is a positive one. Call this affect valence. Note that valence can also be attributed to the indi- vidual affects in moods. However, in what follows, it is the valenced dimen- sion of affect in emotion experience that concerns us.

To summarize, there are at least two kinds of valence that are some- times referred to in emotion theory: emotion valence and affect valence.2 The distinction is helpful exegetically. For example, sometimes individual emotions are said to inherit their emotion valence from the valence of their underlying affective states; that is, affect valence (Russell, 2003). At other times, the valence of individual affects is said to be determined by the valence of their underlying emotion states; that is, emotion valence (Damasio, 2003). There are also cases in which emotion valence is treated as if it were a distinct phenomenon of its own, and affect valence is not mentioned (Gordon, 1987; Lazarus, 1991). Finally, there are cases in which affect valence is the object of study, and emotion valence is not mentioned (Zajonc, 1980).

Evidently, the distinction between emotion valence and affect valence is not trivial, and there are important reasons to respect it. But it is a rather crude distinction. As described, it does not address the various internal components of emotion episodes that might be valenced, such as goals and

The Indeterminacy of Valence 237

appraisals. Neither does it address cases in which the cause or object of an emotion is said to be valenced. The point is simply that it is often consid- ered useful to list individual affects or emotions under columns labeled pos- itive and negative. This practice is what the distinction between emotion valence and affect valence is meant to capture.

PLEASURE AND ITS OPPOSITES

The general definition of valence provided above characterizes it as biva- lent; a contrast between two polar opposites. There is a positive “charge,” on one hand, and a negative “charge” on the other. The definition is meant to remind us of the chemical connotations of the term but says nothing spe- cific about what valence is. The reason is that specific proposals vary con- siderably. Typical interpretations of the concept of valence in emotion the- ory include the polarities of good and bad (Kahneman, 1999), hot and cold (Berkowitz, 2000), pleasant and unpleasant (Russell, 1980), pleasure and pain (Frijda, 1986), approach and withdrawal (Davidson, 1992), and joy and sorrow (Damasio, 2003).

When it is defined in terms of pleasure, valence is sometimes referred to as hedonicity (Lambie & Marcel, 2002). This is probably the most com- mon understanding of the term. Generally, pleasure and one of its puta- tive opposites are the qualities referred to by the positive and negative “charges” of valence, respectively (e.g., displeasure, unpleasantness, pain, etc.). This is true for both emotion valence and affect valence. Indeed, this usage and its variants are so common that sometimes affect, hedonic qual- ity, and valence, are all used synonymously to denote a pleasant–unpleasant quality, or positive and negative affect, respectively (Barrett, 1996; Russell, 1999). It is, of course, true that affect is often said to have other dimensions, such as activation or arousal. But affectivity, as such, is more closely allied with hedonicity. In the words of John Lambie and Anthony Marcel, “the most markedly affectively valenced aspect of emotion experience is hedonic tone or quality: pleasure and displeasure” (Lambie & Marcel, 2002, p. 343). Lisa Feldman Barrett makes the same point when she states that “the valence dimension typically refers to the hedonic quality of an affective experience (pleasant or unpleasant)” (Barrett, 1996, p. 48).3

The distinction between emotion valence and affect valence is funda- mental to how pleasure figures into emotional valence. To say that positive emotions are associated with pleasure is one thing. To say that positive affects are associated with pleasure is another. The supporting theories and arguments are usually quite different. One theory ranges over emotions, the other over affects. As we saw above, it may be that individual emotions inherit their pleasurable characteristics from the pleasurable qualities of

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their underlying affects (Russell, 2003). An alternative model of the geneal- ogy of valence might be that the pleasurable qualities of affect are derivable from the pleasurable qualities of individual emotions (Damasio, 2003). Both of these proposals involve valence; they simply differ on which aspect of valence is primary in the genealogy of valence. According to the former, affect valence is primary. According to the latter, emotion valence is pri- mary. These two examples should reinforce the reason why it is important to distinguish between emotion valence and affect valence.

To summarize, in the context of emotion theory, valence is generally defined in terms of pleasure and its opposites. This is the most common and central sense of what is meant by the term. In this sense, valence “is an obvi- ous and central feature of emotion” (Lambie & Marcel, 2002, p. 434). An emo- tion or affect is said to be “positive” because it is associated with pleasure. An emotion or affect is said to be “negative” because it is associated with some opposite of pleasure; perhaps unpleasantness, displeasure, or pain.

One of the most interesting areas of debate in contemporary emotion theory involves affect valence in this hedonic sense. The issue is whether pleasure and its opposites are statistically independent measures, or whether they are linked by correlation (Barrett & Russell, 1998; Russell, 1999; Watson & Tellegen, 1985). This issue is an excellent example of what scientific histo- rian Thomas Kuhn meant by “puzzle-solving” in “normal science” (Kuhn, 1970). There is a widely shared body of experimental practices, or paradigms, and a thriving research industry working on related problems. The associa- tion between positive and negative valence, and pleasure and its opposites, is equally popular in discussions of emotion valence. But here we do not find the same focus on sharply defined problems and experimental techniques. Scientific efforts to understand valence therefore tend to be focused in the area of affect valence. The widespread use of the concept of valence in this domain is a prominent feature of the scientific study of emotion. To be sure, there are theorists who downplay or ignore the contribution of valence to emotion (James, 1890/1981; Mandler, 1984; Schacter & Singer, 1962). Never- theless, when it is combined or identified with hedonicity, valence is funda- mental to large segments of emotion theory. Indeed, it is so pervasive that it is hard to imagine emotion theory without it.

WHEN EMOTION VALENCE IS INTRINSIC

In a provocative critique of emotion valence, Robert Solomon and Lori Stone claim that the origins of the concept of valence lie in ethics (Solomon & Stone, 2002, p. 418). This may be true in the case of emotion valence, but it is inaccurate in the case of affect valence, which they hardly mention. In

The Indeterminacy of Valence 239

fact, a plausible history of the scientific origins of affect valence can be found in the development of the physiological concept of irritability (Hall, 1975; Pagel, 1967; Temkin, 1964). And certainly many contemporary theo- ries of affect valence do not originate in ethics, although they may have implications for ethics. Solomon and Stone therefore appear to be wrong that the origins of affect valence lie in ethics. But actually their critique of emotion valence ignores affect valence almost entirely. As a result, their discussion of valence is incomplete. However, Solomon and Stone are right in claiming that the concept of emotion valence is more problematic than is commonly realized. In particular, they are right in stating that valence can- not be a fixed objective and intrinsic feature of emotions.

Very roughly, what Solomon and Stone (2002) argue is that valence is always a matter of interpretation and that interpretation is always relative to a context and a scheme of meaning or evaluation. It therefore makes lit- tle sense to say that an emotion is positive or negative, in itself, apart from some scheme of meaning that provides criteria for the application of the “positive” and “negative” valence operators. Hence, it makes little sense to speak of emotion valence as if it were a fixed objective and intrinsic feature of emotion states themselves. It is neither objective nor intrinsic because it is based on interpretation, which involves the assignment of a positive or negative value to those states.

Solomon and Stone (2002) conclude their critique of emotion valence in a rather iconoclastic manner. They write:

The analysis of emotions in terms of “valence,” while it recognizes something essential about emotions (that is, that they involve appraisals and evaluations of the world and are relevant to a life well or ill-lived), is an idea that we should abandon and leave behind. It serves no purpose but confusion and per- petrates the worst old stereotypes about emotion, that these are simple phe- nomenon unworthy of serious research and analysis. (p. 432)

This certainly is a radical conclusion that would mean the end of large segments of emotion theory as we know it. However, on closer look Solomon and Stone (2002) appear to endorse a more moderate conclusion. They write:

All emotions involve some positive or negative appraisals (Solomon, 1993). But to collapse all appraisals into a single evaluative polarity, positive-and- negative, is, to put it simply, simple-minded. (p. 427)

What, then, is the correct interpretation of Solomon and Stone’s conclu- sion? The first passage states that we should give up the concept of valence entirely, and the second one denies this. This seems blatantly inconsistent. However, there is a way to resolve the inconsistency. What Solomon and

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Stone are really arguing against is the “facile” and “simple-minded” mono- lithic application of the concept of valence to emotions (p. 433). More spe- cifically, they object to emotion valence as a monolithic concept; that is, a concept that is indiscriminately applied to all the various emotions in an attempt to reduce their multifarious evaluative aspects to a single uniform bipolar dimension. As they say, “our argument is not that there is no such thing as valence or no such polarity or contrasts, but rather that there are many such polarities and contrasts” (p. 418). To document their case, they list 18 examples of how positive and negative bipolarity is understood in emotion theory (p. 418). They also appeal to Aaron Ben-Ze’ev’s rich account of the subtlety of emotion (Ben-Ze’ev, 2000).

So, on closer examination, what Solomon and Stone are against is the “facile” and “simple-minded” monolithic application of the concept of valence to emotions. They do not believe that we should give up the con- cept of valence entirely. Instead, their point is that there are many varieties of emotion valence. This still means doing away with the idea that valence is an intrinsic feature of emotions. That is quite a radical conclusion. As we shall see, the same conclusion applies in the case of affect valence, with equally radical consequences. But here the argument will be quite differ- ent; it is the indeterminacy thesis. The consequences will also be more drastic, since they create doubt over the very possibility of a scientific approach to affect valence.

WHEN AFFECT VALENCE IS INTRINSIC

We have seen that a strong case can be made that valence cannot be an intrinsic objective feature of individual whole emotions. The assignment of valence to individual emotions always depends on interpretation and con- text. What about affect valence? Is the valence of individual conscious feel- ing states (“affects”) ever an intrinsic objective feature of those states?

The various descriptive theories of affect discussed earlier all appear to endorse the assumption that valence is an intrinsic objective feature of affect states. An especially vivid expression of that assumption can be found in two recent neuroscientific theories of affect valence (Damasio, 2003; Panksepp, 1998). These proposals share the assumption that valence some- how resides in individual affects as an intrinsic objective feature of those states themselves. Thus, in affect valence, subjective affects or feelings are often thought to be positive or negative in themselves. They wear their meanings—their “charges”—on their sleeves. In this view, when we report the valence of an affective state, we uncover and reveal something deter- mined and fixed that is already there. In other words, the assignment of a positive or negative value to that state is verified by the fact that the state is

The Indeterminacy of Valence 241

positive or negative—prior to being assigned that value. Let us very briefly consider two important examples.

According to Jaak Panksepp, the mammalian brain is genetically pre- disposed to develop several basic emotion command systems. These natu- ral kinds of emotion embody and reflect values that are fundamental to the survival of the organism. According to Panksepp, there are probably seven basic emotion systems: seeking, rage, fear, panic, play, lust, care (Panksepp, 2001, p. 156; see also Panksepp, 1998). The language of values is important here. What it means is that each basic emotion system provides a distinct kind of evaluative orientation to the world; that is, each system specifies a particular kind of direction the organism may take as it deals with changing features of its environment.

Panksepp’s basic emotion systems are all valenced, and, at times, he uses the standard chemical metaphor of positive and negative “charges” to characterize valence (Panksepp, 2001, p. 156, Table 2). But note that in his view, some basic emotions can generate both positive and negative charges, depending on the circumstances. Thus lust can generate erotic feelings, which are pleasurable, and jealous feelings, which are not. And seeking can generate interest, which is pleasurable, and frustration, which is not (p. 156). Clearly, for Panksepp there is sometimes more to valence than sim- ply pleasure and its opposites. However, this does not prevent him from resorting to that simple opposition in order to organize and simplify his overall discussion of affect valence.

Another important example of the view that valence is an intrinsic fea- ture of affective states can be found in the work of Antonio Damasio. He presents a vigorous defense of the idea that valence is an intrinsic and objective feature of affective states themselves. Damasio has a distinct view of the genealogy of affect valence. First, there is the emotion body state. Each basic emotion constitutes an automatic response and particular evaluative orientation to the world and is designed to protect and improve the conditions of the organism (Damasio, 2003, pp. 34–35). Then comes the corresponding affective feeling state, which is the consciousness of that underlying body state. According to Damasio, the feeling state inherits its valence from the underlying emotion state that gives rise to it. In short, “a feeling of emotion is an idea of the body when it is perturbed by the emo- tion process” (p. 88). This account of the genealogy of affect is accompanied by a thoroughgoing commitment to bivalence. Thus we are told that “all feelings contain some aspect of pain or pleasure” (p. 123). Indeed, in Damasio’s view, it is a “well-established” fact that feelings are bivalent:

There are organism states in which the regulation of life processes becomes efficient, or even optimal, free-flowing and easy. This is a well-established physiological fact. It is not a hypothesis. The feelings that usually accompany

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such physiological conducive states are deemed “positive,” characterized not simply by the absence of pain but by varieties of pleasure. There also are organism states in which life processes struggle for balance and can even be chaotically out of control. The feelings that usually accompany such states are deemed “negative,” characterized not just by absence of pleasure but by vari- eties of pain. (p. 131)

In a complex series of steps, Damasio extends these observations about the origins of bivalence in bodily regulation and homeostasis to the psycho- logical and social domains. He presents a classification of emotions in which social emotions such as shame and sympathy are labeled as posi- tive or negative, depending on their innate valenced character (p. 156). Damasio actually traces the bivalent character of valence all the way back to the mechanisms of cellular activity. Even the “unbrained paramecium” is capable of emotional reactions, according to him. In this case, valence is characterized as “detection of the presence of an object or event that rec- ommends avoidance and evasion or endorsement and approach” (p. 41).

Like Panksepp, Damasio is a believer in intrinsic valence. In his view, the positive or negative character of the various affective states is not a con- textual matter of interpretation requiring comparison with some external standard of meaning. One simply detects and experiences what it is like to be in that state and that’s it. The experience of valence is seen as a kind of conscious registration of information. Damasio does insist that consciousness and perception are dynamic. However, in his account of affect valence, the information that a state is valenced is not fundamentally changed or altered by the awareness of it, nor is it altered by the process of becoming con- scious of it. It is simply read off as that state.

To conclude, both Panksepp and Damasio appear to endorse some form of the thesis that valence is an intrinsic objective feature of affective states themselves. In this they agree with the defenders of descriptive structural models of affect discussed earlier, who also maintain that valence is an intrinsic objective property of affective states. If our indeterminacy thesis is true, then this assumption must be wrong. To explain why, we turn to John Lambie and Anthony Marcel’s novel account of emotion experi- ence. Although they do not defend an indeterminacy thesis, such a thesis can be constructed from their account of emotion experience.

THE HETEROGENEOUS CHARACTER OF EMOTION EXPERIENCE

In a highly original discussion of emotion experience, John Lambie and Anthony Marcel argue that emotion experience is not single or uniform.

The Indeterminacy of Valence 243

According to them, “emotion experience takes various forms and is hetero- genous” (Lambie & Marcel, 2002, p. 219). They also argue that “there is no one essential type of content of emotion experience” (p. 256). Thus there is a variety of emotion experiences, and the content of emotion experience is both “varied and variable.”

There are important lessons in Lambie and Marcel’s discussion for our understanding of affect valence. First, their account of the varieties of emo- tion experience poses special problems for the view that affect valence is a single uniform phenomenon. Valence, for Lambie and Marcel, turns out to be multidimensional and multiple. Secondly, their claim that valence is multidimensional and multiple points toward an even more radical thesis— which they, however, do not explore. This thesis is that affect valence is fun- damentally indeterminate. However, before this thesis can be stated, it is first necessary to consider more closely Lambie and Marcel’s account of emotion experience.

Lambie and Marcel (2002) start by distinguishing two orders of emotion experience, which they refer to as phenomenal experience and awareness (p. 220). These constitute emotion experience, in their sense of the term (p. 230). First-order phenomenal experience is a very basic “what-it’s-like” experience. Second-order awareness is normally directed at first-order phe- nomenal experience (p. 230); it is a kind of reflexive knowledge of that first- order phenomenology (p. 228). First-order phenomenology does not have propositional structure (p. 239); it is ineffable, although it is not inexpressible or indescribable (p. 237). Nevertheless, it is significant that “reports of phe- nomenology tend to distort it” (p. 237). Second-order awareness is a kind of knowing directed at first-order phenomenology; its content is created by attending to first-order phenomenal experience, which is logically and temporally prior. Normally, we can only know first-order phenomenology through second-order awareness, “which usually transforms it” (p. 237). Attention is central to second-order awareness. Lambie and Marcel (2002) actually state that “focal attention in particular creates awareness” (p. 235).

Lambie and Marcel (2002) cite numerous sources of evidence for their distinction between first- and second-order emotion experience. They illustrate the distinction by arguing that “blindsight is a first-order prob- lem, and Anton’s Syndrome, or unawareness of a sensory deficit, is a second-order problem” (p. 228). They also mention the case of people who remember pains or sensations of which they were previously unaware. To make sense of these and other similar phenomena, it is necessary to sup- pose that phenomenal experience can be independent of awareness. This supposition requires something like the distinction between first- and second-order emotion experience.

Phenomenology can be independent of awareness, although usually it is not. Normally, they are linked by focal attention, a mechanism whereby

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some part of first-order phenomenal experience can become the content of second-order awareness (Lambie & Marcel, 2002, p. 234). Lambie and Marcel are careful to note that even though “phenomenology as such is in- dependent of and prior to focal attention, it is nonetheless subject to two aspects of attention” (p. 234). These are general directedness and at- tentional mode. General directedness addresses whether one’s experience is oriented to the self or to the world. Mode of attention addresses whether one’s stance is analytic or synthetic and/or immersed or detached. An ana- lytic perspective tries to break things down into their component parts. Its opposite is the synthetic perspective, which considers the whole (p. 235). The detached perspective tends to remove the self from the object of atten- tion. Its opposite is the immersed perspective, which puts the self closer to the object of attention (p. 235). With all these factors operating in emotion experience, it is a far more complex and variable affair than is typically sup- posed. So is the question of the supposed content of emotion experience. The consequences of this line of thinking for the concept of valence are enormous, particularly when valence is understood as hedonicity.

Lambie and Marcel (2002) sometimes distinguish between valence and hedonicity. They limit hedonicity to pleasure and pain and relegate valence to positive and negative evaluation (p. 229). For them, there is a distinction between the evaluation underlying and causing an emotion— namely, valence—and the pain or pleasure of the experience—namely, hedonicity (p. 243). However, as we have seen, many writers on affect valence appear to identify valence with hedonicity. And recall Lambie and Marcel’s claim that “the most markedly affectively valenced aspect of emo- tion experience is hedonic tone or quality: pleasure and displeasure” (p. 343). For our purposes, the central point at issue is the claim that valence is an intrinsic feature of affective states. On that question, Lambie and Marcel also appear to defend a form of the thesis that affect valence is intrinsic. However, somewhat ironically, they also provide good reasons for doubting it. To see why, we need to look closer at the relationship between attention and hedonicity. Recall that, according to Lambie and Marcel, hedonicity is the most “markedly affectively valenced aspect of emotion experience” and “an obvious and central feature of emotion” (p. 243; emphasis added).

Lambie and Marcel (2002) argue that “hedonicity may be of different kinds” partly because “hedonic tone is not a single simple dimension but differs according to the specific intentionality of the emotion” (p. 244). For example, “the pleasure in relief is different from that in simply satisfying an unhindered concern” (p. 244). Likewise, the “pain of grief is different from that of frustration” (p. 244). In other words, each distinct emotion episode can have its own particular hedonic tone. This pluralistic position on

The Indeterminacy of Valence 245

hedonicity appears to be inconsistent with Damasio’s theory of affect valence, and others like it. However, the divergence from traditional approaches to valence gets even more pronounced when we add the fact that Lambie and Marcel are not simply saying that each individual emotion episode has its own single hedonic tone. In addition, they also maintain that within a single emotion experience there can be different, sometimes con- trasting, varieties of hedonicity. As they put it, “the different sources of hedonics do not contribute to a single hedonic tone but to different hedonic tones coexisting at one moment” (p. 245). Thus the object of love may be experienced as pleasant while the state one is in is not. This means that even within a single emotion experience there can be multiple sources and experiences of hedonicity that range from the appraisal itself, to what is appraised, the result of the appraisal, and the experience of the action ten- dency associated with that particular emotion state (p. 245).

ATTENTION IN EMOTION EXPERIENCE

So, according to Lambie and Marcel (2002), different hedonic tones can be experienced at a given time; attention determines (1) which one enters awareness, (2) the degree of awareness, and (3) how pleasant or unpleasant it is. The key to all this is the relationship between hedonicity and atten- tion. Hedonicity is determined by mode of attention (p. 243). Focal atten- tion also plays an important role in the generation of hedonicity by selec- tively focusing consciousness on a particular hedonic tone and making it available for awareness. This formulation sounds very much as if hedon- icity were entirely a psychological construction effected by attention. Yet Lambie and Marcel also say that hedonicity is intrinsic: “Hedonicity both is intrinsic to bodily states, movements, and rhythms and depends on the interpretation placed on them” (p. 244). But what really does this statement mean? Is hedonicity somehow there, determinate and fixed, temporally and logically prior to its revelation in awareness through attention? And, if so, what is the nature of the theoretical vocabulary used to capture it scientifi- cally?

One way to understand what Lambie and Marcel (2002) mean by the claim that hedonicity is intrinsic is to suppose that the set of hedonic tones one experiences at a given moment is determinate in the sense of being fixed and constrained by the specific nature of the particular emotional epi- sode in question and its attendant circumstances. What varies is the partic- ular hedonic tone that enters awareness and the degree to which the person becomes aware of it (determined by attention). Thus even though there may be variation and fluctuation in awareness of hedonic tone, there is still

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something fixed and determinate underneath it all: namely, the first-order experience in which multiple hedonic tones are normally present. Yet there are problems making sense of the claim that hedonicity might be intrinsic in this way.

Recall that in Lambie and Marcel’s (2002) view, attention affects the hedonic tone of which one is aware. For example, a detached stance can make hedonicity virtually disappear, whereas an immersed stance can allow it to dominate one’s being. Attending to the self or to the world brings dif- ferent features of each into focus while others disappear. And, of course, this happens not only with different emotion experiences; it can also hap- pen within a single ongoing emotion experience. A good example is pain. Lambie and Marcel note that “the more analytically that one attends to a painful sensation, the less its painfulness: The more that one attends to the sensations themselves and the less one’s attention encompasses [their] sig- nification, the less is [their] hedonicity” (p. 235). They even go so far as to say that “if one attends to one’s bodily sensations in a sufficiently analytic and detached manner, hedonic tone may be distanced, diminished, and dis- appear” (p. 243). In this way, “the painfulness of the pain is often reduced and sometimes vanishes” (p. 243).

The same mechanisms of attention govern the hedonic character of pleasure, and secondary appraisal can also influence hedonicity. Thus “judging that one can change the situation or that nothing can be done has a large effect” (p. 244). Here Lambie and Marcel (2002) cite the fact that “the pain of torture is increased by knowledge of helplessness” (p. 243).4 Note that although variations in attention and appraisal may alter the char- acter of hedonicity in second-order emotion experience, they do not create the underlying phenomenology of first-order experience. Nevertheless, as Lambie and Marcel clearly state, the precise nature of first-order experi- ence normally eludes us until it is shaped and revealed in attention (p. 228); this is a crucial point. We are now ready to consider the indeterminacy the- sis for affect valence.

INDETERMINACY OF AFFECT VALENCE

Lambie and Marcel (2002) tell us that there is something “it is like” to be in a first-order phenomenological emotion state prior to attention. The char- acter of that particular experience may be expressible but it is not report- able apart from second-order awareness and its mechanisms and processes (p. 229). It is a sort of experience-in-itself that cannot normally be cap- tured except through awareness, which forms and shapes it and therefore changes it. In general, “one’s experience is not independent of how one

The Indeterminacy of Valence 247

attends to it” (p. 226). Different forms of attention therefore translate into different forms of emotion experience. The “what-it’s-like” underneath it all is there but cannot be captured verbally. The problem is that whenever we try to capture, in words, the hedonicity of an emotion state—its hedonic valence—we also change the nature of what is being experienced. The key here is the special subjective evaluative character of the awareness of hedonic valence. Although it may true that the mechanisms underlying first-order emotion experience can be explained scientifically, the first- order subjective evaluative character of that experience—its emotional meaning—cannot. To try and capture the subjective character scientifically is simultaneously to change and transform the nature of what is supposed to be explained. This is the principal reason behind the indeterminacy thesis for affect valence.

The indeterminacy of hedonic valence follows from the fact that valence is semantically and evaluatively permeable to attention. The same is true of affect valence, more generally. Valence cannot be intrinsic to first- order phenomenal emotion experience in the manner Lambie and Marcel (2002) appear to suggest. Neither is it externally created by attention ex nihilo outside first-order phenomenal experience. Rather, it is a dynamic relational evaluative phenomenon that emerges out of the interaction of attention with first-order phenomenology. In other words, affect valence is neither purely intrinsic and “found,” nor purely extrinsic and “con- structed.” It is enacted (Varela, 1989). A consequence of this ambiguous ontological status is that to attend to the valence of an affective state is to disrupt and change it. Every act of attention is like a new evaluative bap- tism. In a nutshell: Affect valence is indeterminate until it is fixed by atten- tion.

The perplexing ontological status and indeterminacies of affect valence are reminiscent of early interpretations of quantum mechanics, especially Heinsenberg’s uncertainty principle (Heisenberg, 1958). The analogy lies in the fact that to attend to or “measure” affect valence is to disrupt and change the very phenomenon one is attempting to capture. Until hedonic valence is “measured” and becomes fixed and determined through atten- tion, its precise character must therefore remain uncertain and indetermi- nate. In slogan form, there is no fact about the exact valence of an affective state apart from the act of attention that fixes and determines it.5 But note again that the act of attention does not create the underlying phenomenolo- gy of emotion experience. What attention does is create the form in which the emotion experience reveals itself in awareness; its particular subjective and evaluative meaning—its emotional meaning—for that person.

This leaves the suggestion that hedonicity might be intrinsic in serious trouble. Because hedonicity is typically the main or sole component of

248 THE EXPERIENCE OF EMOTION

affect valence, the same conclusion applies to affect valence more generally. The indeterminacy thesis shows valence is not a subjective evaluative phe- nomenon with emotional meaning until it is created and revealed by atten- tion. For this reason, felt body temperature may not be a good analogy for explicating the nature of “core affect” and affect valence (Russell, 2003), because felt body temperature is subject to the mechanisms of attention just described. “Temperature” in this felt sense falls in the domain of the subjective and evaluative and often has emotional meaning. However, the objective physical temperature recorded by a thermometer is an entirely different matter. Its ontological status is very different: It is not relational in the same way, and it has no subjective meaning. The indeterminacy thesis implies that there is no fact about the valence of felt bodily temperature until that valence is shaped and revealed by attention. To say or assume that the objective temperature recorded by a thermometer is somehow the intrinsic material out of which felt bodily temperature is created therefore seems incorrect. It appears to involve a fallacy of equivocation, because temperature means two entirely separate things in both cases. Similar prob- lems with equivocation are likely to arise in attempts to capture first-order phenomenal emotion experience indirectly (Lambie & Marcel, 2002, 237– 238).

The above considerations strongly suggest that there is no scien- tifically defensible sense in which valence can be intrinsic in first- order emotional phenomenal experience. Affect valence is a dynamic en- acted, phenomenon that emerges out of the interaction between attention, second-order awareness, and first-order emotion experience. The indeter- minacy thesis also shows that there is no scientific fact about the valence of a particular state until that valence is formed and fixed by attention in sec- ond-order awareness. Valence, then, is multiple and multidimensional, as Lambie and Marcel (2002) argue. But it apparently cannot be intrinsic in the manner they seem to suggest, and it is subject to a radical indetermi- nacy they do not anticipate or countenance. In a sense, valence in emotion theory is much like gravity in Newton’s Principia. It is a “force” we can wit- ness and scientifically describe, up to a certain point; but beyond that point it cannot be scientifically captured and analyzed any further. The funda- mental nature of valence must therefore remain a scientific mystery.

CONCLUSION

This discussion began with a definition of affect as the conscious felt dimension of emotion. It follows that affect is invariably conscious. How- ever, the distinction between first- and second-order emotion conscious-

The Indeterminacy of Valence 249

ness complicates this picture. Based on that distinction, the argument was made that affect valence, as such, is solely and entirely a property of second-order emotion experience, because affect valence is created and sustained by second-order awareness, which selects and shapes it through attention. It follows that, strictly speaking, there is no such thing as uncon- scious or nonconscious affect valence. There is no scientific sense in which valence can be said to reside intrinsically in mental or physical states that fall outside of the active range of attention. Hence, to speak of first-order phenomenology or stimuli as valenced makes the character of first-order emotion experience even more problematic than it already is. Lambie and Marcel (2002) are certainly right that it is a crucial aspect of emotion expe- rience. They may, however, have overestimated what can be known about it scientifically.

The indeterminacy thesis also contends that the nature of affect valence within second-order experience is problematic. The ontological and semantic vagaries of indeterminacy seriously undermine attempts to generalize about valence as a uniform scientific phenomenon. In particular, indeterminacy makes the concept of core affect particularly problematic and the status of experimental studies that employ it precarious (Barrett, Chapter 11; Russell, 2003). The reason is that there is no verifiable fact underneath it all, nor can there be, because once one tries objectively to isolate and identify a subjectively valenced conscious state, one has simul- taneously changed it.

Admittedly, the indeterminacy thesis is hard to reconcile with the fact that there appear to be fixed and determinate unconscious affective pro- cesses in emotion experience (Winkielman, Berridge, & Wilbarger, Chapter 14; Clore, Storbeck, Robinson, & Centerbar, Chapter 16). These processes are perhaps best conceptualized as a sort of proto-valence but not valence itself. There is also the problem of modularity. The indeterminacy thesis explains the plasticity of affective experience, which would appear to be important for evolutionary success. Yet there is also convincing evidence that fixed modular affective processes exist and are equally important for evolutionary success. So perhaps not all aspects of affect valence are equally permeable to attention; some may be relatively fixed and modular (Charland, 1995; Zajonc, 1980). Finally, there is the question of animal affect. Homology in underlying neurobiological mechanisms suggests that, like humans, many animals probably have some experience of subjective valence and affect (Panksepp, 1998). But just what that experience consists of may be scientifically impossible to identify. Recall Wittgenstein’s dictum that even if a lion could talk, we would not understand it. All of these facts and findings do seem hard to square with the indeterminacy thesis. But it is also hard to see how they could constitute a total refutation of that thesis,

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which has strong independent supporting reasons of its own. This is proba- bly a good place for philosophy to step aside and invite the relevant sci- ences to the challenge.

PHILOSOPHICAL POSTSCRIPT

It might be thought that the perplexities of affect valence outlined here are of the same kind as those associated with the qualia problem discussed by contemporary philosophers (Chalmers, 1996; McGinn, 1999). That would be an error. The qualia problem, at least as it is typically discussed by phi- losophers, has more to do with the descriptive nature of the felt conscious quality of experience. Touch and vision are the paradigmatic sensory modalities discussed, although pain is also often mentioned. But, in fact, pain is a very different kind of phenomenon that has more to do with emo- tional meaning and valence, which is an evaluative and normative matter. The difference is crucial.

Standard philosophical qualia are typically considered to be descrip- tive phenomena that inform us about the state of the world and the body. Not surprisingly, these are the paradigmatically favored qualia of “cogni- tive” science. However, the valenced qualia in emotion are vastly different: They are evaluative and normative phenomena that address the way the world or the body should be. Their primary function is to orient and move us. These are the paradigmatically favored qualia of “affective” science.

So there appear to be two quite different kinds of qualia in our “phe- nomenological garden” (Dennett, 1991, pp. 43–65). There are qualia that inform us and qualia that move us. The valenced qualia in emotion pull and push us in a way that standard sensory qualia do not. Those valenced qualia involve concern, orientation, and personal meaning of a sort that is very dif- ferent, and is usually absent, from standard sensory qualia. Valence is what makes the difference. There may also be mixed qualia that somehow com- bine informative and motivational functions (Millikan, 1996). But the possi- bility of mixed qualia does not annul the fact that, in mammals at least, cog- nitive and affective qualia are distinguishable. Indeed, they appear to be under the control of relatively distinct neurobiological systems (Panksepp, 2003; see also Panksepp, 1998, p. 62). This neurobiological distinction con- stitutes an important strand for the hypothesis that emotion is a special nor- mative natural kind of its own, distinct from cognition (Charland, 1997, 2002; Griffiths, 2003).

To sum up the importance of this philosophical postscript: The signifi- cance of the distinction between the cognitive qualia that inform us and the emotional qualia that move us may be reflected in what can be scientifically

The Indeterminacy of Valence 251

known about them. Even if we could solve the famous “hard problem” for standard cognitive qualia, we would not have explained the mysteries and perplexities of affect valence. The difficulties posed by the scientific expla- nation of affect valence appear to be of a different order. This is not simply a hard problem for the science of mind. It may constitute a genuine inexpli- cable mystery.

ACKNOWLEDGMENTS

Thanks to Aaron Ben-Ze’ev, Sylvia Berryman, John Lambie, Anthony Marcel, Har- old Merskey, Jim Russell, Robert Solomon, and Evan Thompson for helpful com- ments on earlier drafts of this chapter.

NOTES

1. See Buck (1999, p. 304) for an interesting but different variant of this distinc- tion, which he traces to Bertrand Russell’s famous discussion of “knowledge- by-acquaintance” and “knowledge-by-description” (Russell, 1912).

2. Different aspects of valence can be stressed in different contexts. For example, Fossum and Barrett (2000) allude to emotion valence when they state that “the valence of an emotion term refers to both its hedonic tone and evaluative conno- tation” (p. 670; emphasis added). However, in another context, Barrett alludes to affect valence when she states that “the valence dimension of the circumplex refers to the hedonic tone of the mood” (Barrett, 1996, p. 49; emphasis added). One can also treat affect as the “conscious subjective aspect of an emotion” (Cacioppo & Berntson, 1999, p. 134; emphasis added). The circumplex model can sometimes be interpreted this way (e.g., Barrett, 1998; Russell, 2003).

3. Note that the valence of an affective state in this sense is quite different from its desirability (Barrett, 1996). The “positively” valenced affect allegedly referred to by the statement “I feel good” is different from the “positively” evaluated affect reported by the statement “This is a good feeling to have” (p. 49). How- ever, this does not imply that the valence dimension of affective states is not inherently evaluative. This is precisely what makes valence so special and important.

4. I leave open the question of whether affect valence is so permeable and muta- ble that a painful affect can be completely transformed into a pleasurable one that is in no way unpleasant. In a fascinating discussion of masochism, psychia- trist Harold Merskey considers the question whether “ ‘pain’ is ever solely pleasant” (Merskey & Spear, 1967, p. 122). He states that “it is possible, although it is disputed, that in some cases ‘pain’ is pleasant and in no way unpleasant” (p. 121). Noting that the issues may be semantic as well as clinical, he concludes that the question “must remain open to investigation” (p. 122). I agree. The issue is important, because it bears directly on the validity of the

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5.

definition of pain. According to the International Association for the Study of Pain, pain is defined as “an unpleasant sensory and emotional experience asso- ciated with actual or potential tissue damage, or described in such terms” (Merskey & Bodguk, 1994, p. 210). In this definition “pain is always subjective” (p. 210). The paradoxical possibility of pains that are not subjectively experi- enced as unpleasant is therefore extremely theoretically significant. As Merskey notes, “if it should prove to be the case that something called ‘pain’ by masoch- ists is experienced without any quality of unpleasantness the definition [of pain] would need revision” (p. 122).

The indeterminacy thesis for affect valence is partly inspired by Quine’s (1960) argument for the indeterminacy of translation. Another inspiration is Amelie Rorty’s (1986) argument that emotional states are dynamic and permeable. Finally, a third inspiration is the problem of indeterminacy in quantum mechan- ics. William Reddy (2001) appears to defend a related thesis. According to him, emotions are a kind of performative utterance, since they “do something to the world” (Reddy, 2001, p. 111). But they are different from performatives, because of the special way in which “they are both self explorative and self- altering” (Reddy, 2001, p. 122; see also pp. 104–111). Reddy makes use of Quine’s principle of the indeterminacy of translation to argue that there is an unavoidable indeterminacy to emotional experience (pp. 78–96, 320, 332).

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TFeHeElinEgXIsPPEeRrcIEeiNviCngE OF EMOTION

CHAPTER 11 Feeling Is Perceiving

Core Affect and Conceptualization in the Experience of Emotion

LISA FELDMAN BARRETT

What is the experience of emotion? This question fascinates friends and family members, novelists and poets, psychologists and philosophers alike. In this culture we ask and answer questions pertaining to feelings many times each day. Over coffee, we gossip about the emotions of others and speculate about why they reacted as they did. We pay large sums of money to psychotherapists to help us understand why we feel the way we do, and to grapple with ways of changing those feelings. Poets and novelists attempt to capture the indescribable nature of what emotion feels like, bringing its richness and complexity to life. In psychological science, ques- tions about feelings are ubiquitous. Whether to explain, predict, or control for feelings, scientists ask participants how they feel, and participants easily answer. Scientists debate whether or not feelings lie at the heart of emo- tion, but presumably no one would deny that the experience of emotion is something important to understand in its own right. Many people, both in the scientific study of emotion and in everyday life, often presuppose a the- ory of emotion experience that goes unexamined: We experience emotion because we have “emotions”—internal causal mechanisms that, when trig- gered, leave measurable traces of their existence.

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1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

Emotions are not causal entities. They are not a set of facial movements, a vocal signal, changes in peripheral physiology, and some voluntary action that are coordinated in time and correlated in intensity. In this chapter, emotions are defined as perceptions. A state of anger (fear, etc.) is the categorization of a core affect state, which itself is the neurophysiological state that results from the pro- cess of evaluation.

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

The distinction between conscious and unconscious processes is more phenom- enological than mechanistic (see Barrett, Tugade, & Engle, 2004). The idea of endogenous (stimulus-driven) and exogenous (goal-driven) forms of attention is more relevant to the ideas presented in this chapter. Also, the definitions of experience and awareness used in this chapter follow the spirit of Lambie and Marcel’s (2002) discussion of these concepts.

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you think this is not a good question to ask, can you say why?

In this chapter I suggest that core affect can influence behavior in a way that
is driven by both exogenous (or stimulus-driven) and endogenous (or goal- driven) forms of attention, and that this can happen outside of awareness
(and can therefore result in unconscious affective behavior). I also suggest
that core affect (and its resulting behaviors) have sensory–motor consequences that are available to be consciously represented and felt (although they need not be).

In this chapter I challenge the view that emotions are entities causing experience, and offer an equally plausible model to account for the experi- ence of emotion. This account involves the recently defined scientific con- cept of core affect (i.e., the affective state that results from the process of evaluation; Russell, 2003; Russell & Barrett, 1999), ideas and evidence from the social-psychological literature on “person perception,” and work on embodied conceptual knowledge in cognitive science. Specifically, I pursue the idea that we experience an emotion when we categorize an instance of core affective feeling. From this perspective, the experience of emotion is a perceptual act, guided by conceptual knowledge about emo- tion.

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EMOTIONS AS CAUSAL ENTITIES

Many contemporary models of emotion assume that emotions have onto- logical status as causal entities—that is, emotions are believed to exist in the brain or body and cause changes in sensory, perceptual, motor, and physiological outputs. Each emotion, in this view, can be characterized by a set of recognizable behavioral and physiological outcomes (including a set of facial movements, a vocal signal, changes in peripheral physiology, and some voluntary action) that are coordinated in time, correlated in intensity, and constitute the components of an emotional response. These aspects of emotional responding are thought to give evidence that kinds of emotions exist. Although not all scientific models of emotion expound this view (e.g., Mandler, 1975; Ochsner & Barrett, 2001; Russell, 2003), the idea of emo- tions as causal entities characterizes both popular (e.g., Goleman, 1995) and scientific models (e.g., Lundqvist & Öhman, Chapter 5; Scherer, Chapter 13; for a review, see Barrett, 2004a; Barrett, Ochsner, & Gross, 2004). Even when emotion models are more complex, they often continue to assume that traditional emotion categories exist as real entities in nature, whether nature is defined as residing in the brain, body, or the deep structure of the situation (depending on the preferred level of description). The general idea is that the category emotion is a natural kind, unlike other psychologi- cal phenomenon (say, cognition or attention; e.g., see Charland, Chapter 10), and each category of “basic” emotion, referred to by such English words as anger, sadness, and fear, is a natural kind (Barrett, 2005).

The Experience of Emotion

A correspondingly simple perspective on the experience of emotion falls out from the natural kind view of emotion: the experience of an emotion is the simple, veridical sensory detection of the causal mechanism (or, in some models, the detection of the other outputs, such as facial muscle move- ments). The emotion is an object of consciousness, like a table or a chair. Some models make additional assumptions about the attentional processes involved in becoming aware of an emotion experience (e.g., Lambie & Mar- cel, 2002; Prinz, Chapter 15), but the fundamental assumption remains the same: emotion mechanisms (e.g., an anger mechanism) trigger an emotion state (e.g., a state of anger), producing the experience of an emotion (a feel- ing of anger). From the emoter’s perspective, the awareness of this experi- ence is taken as clear evidence that the causal mechanism—the emotion— has been triggered. Feeling angry is evidence that the anger mechanism has fired.1

The idea of emotions as causal mechanisms produces an easy answer to questions about emotions and consciousness. Emotions (i.e., the causal

258 THE EXPERIENCE OF EMOTION

mechanisms) are unconscious and can cause us to behave in ways of which we are not aware. To be sure, there is considerable evidence that uncon- scious affect exists and that affective behaviors occur without awareness (e.g., Niedenthal, Barsalou, Ric, & Krauth-Gruber, Chapter 2; Winkielman, Berridge, & Wilbarger, Chapter 14). But the question is whether this is really evidence of “unconscious emotion” (i.e., an inescapable, involuntary, and automated set of synchronized changes in response systems that pro- duces a signature emotional response; e.g., Scherer, Chapter 13). According to several emotion models (e.g., Charland, Chapter 10; Scherer, Chapter 13; Prinz, Chapter 15), the answer to that question is yes. And when the resulting sensations register, the experience of emotion results. The sensory and perceptual processes involved are typically thought to occur uncon- sciously, although deliberate introspection can also take place (and might be better thought of as emotion regulation, because it usually involves lan- guage). The endpoint—the feeling—is conscious, by definition, although it may not be a focal point for attention (e.g., Lambie & Marcel, 2002; Schooler, 2002).

EVALUATING THE IDEA OF EMOTIONS AS CAUSAL ENTITIES

The assumption that emotions are entities that cause behavior and experi- ence has been valuable in the scientific study of emotion. It has helped define emotion as a topic worthy of study in its own right, and it has gener- ally organized scientific inquiry for several decades. The idea of emotions as causal entities has several strengths as a scientific view. It is simple to state: Emotions cause behavior and experience. It explains why our own feelings of anger, fear, etc., have a given quality. We experience feelings as erupting or “happening to us” because the causal entity—the emotion— hijacks our mind and body and sometimes causes us to behave in ways that we would rather not (i.e., ways that interfere with the more reasoned responses that we identify as part of human selves). The idea of emotions as causal entities is also consistent with a variety of scientific assumptions that guide psychological theorizing and measurement (for a discussion, see Barrett, 2005).

Much to everyone’s surprise, however, research has not established a strong evidentiary basis for the idea that anger, sadness, fear, and so on, constitute natural kinds of emotion that cause behavior or experience. Thus far, researchers have yet to identify patterns of observable behaviors that consistently distinguish among types of emotion, nor have they identified clear and consistent evidence for distinct neural systems corresponding to each kind of emotion. Most importantly, they have not observed the kind of

Feeling Is Perceiving 259

response clusters within categories that would confirm their status of emo- tions as natural kinds (for a more detailed review of evidence, see Barrett, 2005). It is instructive to review this evidence briefly before considering what it means for the scientific study of emotion experience.

The Evidence

Perhaps the most compelling idea in the psychology of emotion is that emo- tional states have specific and unique patterns of somatovisceral changes. Although individual studies sometimes report distinct autonomic correlates for different emotion categories (e.g., Christie & Friedman, 2004; Ekman, Levenson, & Friesen, 1983; Levenson, Ekman, & Friesen, 1990), meta- analytic summaries generally fail to find distinct patterns of peripheral nervous-system responses for each discrete emotion (Cacioppo, Berntson, Larsen, Poehlmann, & Ito, 2000). Peripheral nervous-system responses configure for conditions of threat and challenge (Quigley, Barrett, & Weinstein, 2002; Tomaka et al., 1993; Tomaka, Blascovich, Kibler, & Ernst, 1997), and for pleasant versus unpleasant affect (Cacioppo et al., 2000; Lang, Greenwald, Bradley, & Hamm, 1993), but do not robustly distinguish between traditional emotion categories.

Evidence from studies of facial behavior has yielded the same result. Facial electromyography measurements coordinate around positive versus negative affect (Cacioppo et al., 2000) or intensity of affect (Messinger, 2002), rather than discrete emotion categories. Participants can assign posed facial configurations to discrete emotion categories with some reli- ability, but these findings are open to alternative explanations (e.g., Russell, 1994; Russell, Bachorowski, & Fernandez-Dols, 2003), including that per- ceivers are imposing, rather than detecting, categorical distinctions in the facial configurations that they rate (I return to this point later).

Evidence from studies of instrumental behavior is similar. Instrumen- tal behavioral responses such as flight or fight correspond to situational demands (Bouton, Chapter 9), rather than to specific categories of emotion. Behaviors are specific, context-bound attempts to deal with a situation (Cacioppo et al., 2000; Lang, Bradley, & Cuthbert, 1990). Functional demands vary with situations, making it likely that instances of the same emotion can be associated with a range of behaviors. For example, Lang et al. (1990) note that the behaviors associated with fear can range from freez- ing to vigilance to flight. Not only are different behaviors associated with the same emotion category, but also one type of behavior can be associated with many categories. For example, there are several types of aggressive behavior, such as defensive, offensive, or predatory, each of which is assumed to be associated with a different type of stimulus situation caused by different neural circuitry (Blanchard & Blanchard, 2003).

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Many theorists assume that kinds of emotion have specific neural essences (e.g., Buck, 1999; Damasio, 1999; Dolan, 2002; Ekman, 1992; Izard, 1993; LeDoux, 1996; Panksepp, 1998). Yet two recent meta-analyses of neuroimaging studies (Murphy, Nimmo-Smith, & Lawrence, 2003; Phan, Wager, Taylor, & Liberzon, 2002) failed to find consistent evidence of par- ticular neural correlates for anger, sadness, disgust, and happiness. A fear– amygdala correspondence was noted across both analyses, but can be accounted for by alternative explanations (see Phan et al., 2002). Although there are a number of methodological and theoretical factors that presently limit our ability to draw inferences about the neural bases of emotional responses, the failure to find neural signatures for distinct emotions thus far is consistent with the behavioral evidence. Furthermore, although there is good evidence that specific behaviors (e.g., freezing) may depend upon specific brainstem and subcortical nuclei (e.g., Panksepp, 1998), there is lit- tle evidence to suggest that each behavior can be uniquely associated with any single emotion category (although we can effortlessly assign behaviors to categories).

Just as behavioral and biological findings have not produced strong evidence for “kinds” of emotions, there is no clear evidence for qualita- tively different “kinds” of experiences. Self-reports of experienced emotion take on a circumplex shape, rather than a simple structure configuration (with one factor or cluster for the report of each emotion; e.g., Barrett, 2004; Feldman, 1995a, 1995b; Russell, 1980). A circumplex shape indicates that reports of anger, sadness, fear, and so on, can be broken down into more elemental properties. Although there is some debate about the con- tent of those properties, valence (hedonic tone) and arousal (feelings of acti- vation and deactivation) are prime candidates (Russell, 2003; Russell & Barrett, 1999). It has been argued that the valence and arousal properties observed in self-reports of emotion experience reflect (1) people’s beliefs about what they feel (Dennett, 1991), (2) the contaminating influence of emotion language (i.e., the words used in the rating process; e.g., Frijda, Markam, Sako, & Wiers, 1995), or (3) evaluative processes that occur subse- quent to the experience of emotion (Charland, Chapter 10). Evidence is accumulating against these alternative explanations, however (Barrett, 2004; Barrett, Quigley, Bliss-Moreau, & Aronson, 2004; Barrett & Nie- denthal, 2004).

Most importantly, physiological, behavioral, and experiential outputs for each emotion category are not highly intercorrelated (Bradley & Lang, 2000; Lang, 1968; Mandler, Mandler, Kremen, & Sholiton, 1961), under- mining the claim that the various aspects of emotional responding ema- nate from a single common cause. Although no single study has yet mea- sured all possible outputs simultaneously, even two or three response

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channels fail to correlate when researchers induce anger, sadness, fear, and so on. Enough evidence has accumulated for some theorists to con- clude that the lack of coherence within each category of emotion is empirically the rule rather than the exception (Bradley & Lang, 2000; Russell, 2003; Shweder, 1994).

Although the instrument-based data do not cohere to reveal categories of emotion, they do show more consistency when measuring pleasant and unpleasant affects. Judgments of facial behaviors (for a recent review, see Russell et al., 2003), electromyographic (EMG) recordings of facial move- ments (for a meta-analytic review, see Cacioppo et al., 2000), autonomic physiology (for a meta-analytic review, see Cacioppo et al., 2000), and expressive behavior (for a review, see Cacioppo & Gardner, 1999) can all be described in terms of valence–arousal combinations. Emotion data are only confusing when scientists search for evidence of coordinated response pro- files for anger, sadness, fear, and so on. Of course, it is always possible to postulate inhibitory and modulating factors that interfere with coordinated outputs. Alternatively, it is possible to consider other plausible ways to account for the failure to observe the kind of response clusters that would confirm the existence of natural kinds of emotion.

Implications for Understanding the Experience of Emotion

Despite its intuitive appeal, research has not produced a strong evidentiary basis for the idea that there are kinds of emotion. A brief review indicates that after almost a century of searching, scientists still do not have strong, consis- tent evidence to support the idea that emotions have causal status and pro- duce the substrates for the experience of anger, sadness, fear, and so on. The only place scientists observe strong evidence for the existence of these emo- tion categories is in perceiver reports. People automatically and effortlessly assign anger, sadness fear, and so on to others on the basis of their behaviors, and they identify these emotions in themselves. How can scientists under- stand the experience of anger, sadness, fear, and so on, if there are no real emotion mechanisms producing distinct experiences? For the remainder of the chapter, I suggest one possible answer to this question.

THE EXPERIENCE OF EMOTION AS A PERCEPTUAL ACT

As people, we rely on our experiences to tell us about the world. Because immediate experience is so compelling, and because we do not have access to its generation, we believe that our experiences faithfully reveal things as

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they actually are. We conduct ourselves as if experience gives us direct access to the world around us, on the assumption that the world as we feel (hear, taste, see, or smell) it is identical to the physical world that exists apart from us. We see (at least, in Western cultures) anger, sadness, fear, and so on, in people’s behavior, and experience it in ourselves, leading us to assume that those emotions are actual causal entities lurking somewhere within the brain or body. Yet it is possible that we are naïve realists (Asch, 1952/1957; Jones & Nisbett, 1971) when it comes to emotion—we believe that our experiences of emotion reveal an unbiased, internal reality but they may not. Careful study has determined that we rarely experience things as they actually are. Perception is constructive, even at the most basic sensory level (Ramachandran, 1992, 1993). We cannot discern the causes of behavior from our experience, even though we believe that we can (Nisbett & Wilson, 1977). Our knowledge of people and situations unconsciously shapes what we “see” people doing and gives rise to how we explain that behavior (for a review, see Gilbert, 1998). Perhaps the same is true for emotion. In the pages that follow, I develop this idea, suggesting that emotions are perceptions (where perception is defined as assigning objects to meaningful categories so that we “see” an instance of a category). I suggest that the experience of emotion is a perceptual act, or an instance of categorization that involves what we know about emotion.

As an analogy, consider the experience of color. Although the light spectrum is a continuum of wavelengths, color perception is categorical. The English words red, green, blue, and so on, correspond to sets of wave- lengths that are experienced as qualitatively different categories. There are some embodiment constraints on color categorization, because at a sensory level, the human visual system constrains and shapes how we perceive and experience the light spectrum. We sense light at a particular wavelength in a way that is constrained by how the retina registers sensory information and the low-level visual processing that takes place. In the end, we experi- ence some color corresponding to that wavelength, and that color is in- fluenced by our conceptual knowledge of color (Davidoff, Davies, & Roberson, 1999; Özgen & Davies, 2002; Roberson, Davies, & Davidoff, 2000). In this culture people have knowledge about what constitutes the category red, including knowledge of different hues, what objects have them, what colors match, and so on. There is variability in this knowledge (both across individuals and across cultures), so the way I categorize the experience of a certain wavelength may differ from someone else. For example, when my husband and I look at a pillow in our front parlor, we both take in the same wavelengths of light that are bouncing off the pillow (and the rest of the room), and we both detect that wavelength as dictated by what our visual system produces in its early stages of sensory processing.

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Our experience of that pillow as red, or pink, or rose, depends on what we know about those colors and how we use what we know as we categorize the pillow’s color. Behavior toward this pillow, such as deciding what other objects we might match it with, is driven by our experience of its color. Fur- thermore, as we learn more about color (e.g., by taking an interior design course), the way we experience and act on the pillow, or other red-like objects, will change (Özgen & Davies, 2002).

I propose that something similar happens with the experience of emo- tion. At a sensory level, a continuous stream of homeostatic feedback from the body delivers affective information about each individual’s current rela- tionship to the world. It is not a specific interoceptive readout of autonomic activity or anything so precise. Rather, it is a core affective state that gives rise to feelings of displeasure (or pleasure) and activation (or deactivation) that results from ongoing automatic evaluations or primary appraisals of the world. This information is available to be felt or experienced. The way that people perceive this feeling will depend on the conceptual knowledge about emotion that they bring to bear when they categorize their affective state. A person might experience his or her core affective state as sadness, anger, or nervousness. In this view, emotion experience depends, in part, on what knowledge the person brings to bear at the moment of experience. Although the person’s initial behavior might be a function of his or her affective state, what comes next (how the person acts to change his or her current state) will depend, at times, on what is known about emotion and how that knowledge is used.

The basic premise is that the experience of emotion begins with effort- less, automatic perception—a perception of affect through the lens of cate- gory knowledge about emotion. It is not interoception—the simple sensory detection of an internal event. Instead, it is, as William James (1884, 1890/ 1950, 1894/1994) suggested, a self-perception. To be more specific, the experience of emotion is the categorization of core affect. The perceptual process proceeds according to the general principles of behavior identifica- tion that can be found in the social-psychological literature on person per- ception. The category knowledge brought to bear does not consist of sym- bolic representations but of sensory–motor representations that involve the body and are designed for action. So, like several other contributors to this volume (Niedenthal et al., Chapter 2; Atkinson & Adolphs, Chapter 7; Prinz, Chapter 15), I suggest that conceptual knowledge about emotion involves sensory, somatovisceral, and motor states, and that people use this knowledge both when perceiving someone else’s emotion and when per- ceiving their own feelings. Unlike those contributors, however, I assume that there is nothing privileged about such knowledge. We do not learn about anger and sadness and fear because they are real categories in nature.

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We learn about them the way we learn about other abstract concepts, and we integrate sensory and motor states into basic-level emotion categories based on the language that we speak.

Self-Perception

In the field of psychology the idea that emotion is a perception began with William James. In the most general terms, James (1884, 1890/1950, 1894/1994) suggested that the experience of emotion (which he merely called emotion) results from the self-perception of automatic processes. He focused primarily on the ways in which the peripheral nervous system acts on somatovisceral and voluntary muscle activation. A number of modern accounts are inspired by the idea that the experience of emotion is a self- perception (e.g., Damasio, 1994; Dolan, 2002; Laird & Bresler, 1992; Rus- sell, 2003), although they vary in the type and specificity of processes pro- posed.

A strict interoceptive account of the self-perception of emotion, such as that proposed by James and later by Schachter and Singer (1962), is untenable for several scientific reasons (Barrett, Quigley, et al., 2004). Peo- ple do not have automatic, immediate, and explicit access to autonomic and somatic activity, and there is considerable variation (both across persons and across contexts) in the ability to accurately perceive somatovisceral information. Moreover, and perhaps more important for the view being developed here, different categories of emotion are not associated with sig- nature visceral sensations, suggesting that feelings of anger, fear, and so on, do not derive uniqueness from interoceptive readouts of somatovisceral activity.

Nonetheless, James’s general idea—that the experience of emotion results from the self-perception of automatic processes—has some merit. I suggest here that when we experience an emotion, we are perceiving our core affective state at a given instance in time. Core affect is the ongoing, neurophysiological state that results from evaluations of the (internal and external) environment (Russell, 2003; Russell & Barrett, 1999). Core affect causes us to feel moved, compelled, or generally emotional. It can be char- acterized as having hedonic (pleasant or unpleasant) and arousal (activation and deactivation) properties, which are associated with the value of a stim- ulus situation (whether something is good or bad for us), as well as with the predictive certainty of this value (whether or not active coping or more information is required; but for an alternative view, see Charland, Chapter 10). Core affect alone does not produce feelings of anger, sadness, fear, and so on, but it is where these experiences begin. Perceiving core affect at a given moment in time is the first step to experiencing an emotion.

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Core Affect

All the neural processes by which an organism judges, represents, and responds to the value of objects in the world are central to what I mean when I say something involves affect (see also Cardinal, Parkinson, Hall, & Everitt, 2002). Organisms continually and automatically evaluate situations and objects for their relevance and value—that is, whether or not their properties signify something important to well-being (see Bargh & Fergu- son, 2000, but for a contrasting view see Clore, Storbeck, Robinson, & Centerbar, Chapter 16; Storbeck & Robinson, 2004). An object is valuable when it is potentially important to survival (Davis & Whalen, 2001), salient and meaningful (Phan et al., 2002), or relevant to immediate goals (Smith & Kirby, 2001). Objects rarely have intrinsic value or meaning (i.e., they rarely act directly on the nervous systems without involving prior learning; see Owren, Rendell, & Bachorowski, Chapter 8). Typically, meaning is determined by a particular person in a particular context at a particular point in time. This is the basic point made by appraisal models of emotion (e.g., Scherer, Chapter 13; Clore et al., Chapter 16). The result of this evaluative processing has a pervasive influence on a person’s core affective state at any given point in time.

There is a distributed network within the brain that performs evaluation, computes value, and produces changes in core affect. The amygdala is the centerpiece of this system. The evaluation of a stimulus begins when sensory information from the world reaches the amygdala (e.g., Lundqvist & Öhman, Chapter 5; de Gelder, Chapter 6; Atkinson & Adolphs, Chapter 7). According to work by Whalen and colleagues (Kim, Somerville, Johnstone, Alexander, & Whalen, 2003; Whalen, 1998; Whalen, Shin, McInerney, Fischer, Wright, & Rauch, 2001), the ventral lateral aspect of the amygdala (corresponding to the lateral nucleus) computes a quick, initial assessment of a stimulus’s predic- tive value (i.e., to what extent it will predict a subsequent threat). When a stimulus has a high predictive value (i.e., its threat value is certain), informa- tion is sent directly to various output systems so that the organism can respond appropriately. Potentially, this process allows a person to produce simple, evolutionarily tuned behaviors to deal with threat or reward (see Phelps, Chapter 3). Given the world in which humans live, it is rare to encounter stimuli with a certain predictive value, so that other processes are usually engaged to help determine the meaning of a stimulus when its pre- dictive value is uncertain. The ventral amygdala can disinhibit the dorsal amygdala (corresponding to the central nucleus) to marshal attention and other output systems to gather more information to better assess the predic- tive value of the stimulus (and to allow the person to better predict its stimu- lus value the next time it is encountered).

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In addition, value prediction can be improved by identifying that an object is present and recognizing what it is, both of which involve percep- tual processing. The available sensory information is extracted and matched with stored unimodal representations in perceptual memory. This process involves primary, secondary, and association areas of sensory cortex that are connected to the ventral region of the amygdala. When viewing a snake, for example, bottom-up (or stimulus-driven) processes extract information about perceptual features of the object. These features constrain one another during a matching process, leading to stimulus recognition, and the stimulus is recognized as familiar or not. Although the object is not yet named or identified as belonging to a specific category, this perceptual information contributes to predicting its value and helps the person to respond accordingly.

Evaluations can also be influenced by information from the later stages of perceptual processing when an object is interpreted. This is when con- ceptual knowledge begins to play a role in affective processing (involving left-inferior prefrontal areas). The stimulus is assigned to a category (e.g., the object is categorized as an instance of snake), can be named (e.g., “that is a snake”), although it need not be, and an action plan is generated to deal with it (e.g., the perceiver prepares to walk in the other direction).

Finally, when the predictive value of a stimulus is uncertain, informa- tion from the lateral nucleus of the amygdala is forwarded to the ventral medial aspect of the amygdala (corresponding to the basal nucleus), where information is combined with context-relevant information coming from the orbitofrontal and medial prefrontal cortices. Although some researchers consider this a form of regulation, I think of it as a later processing compo- nent of evaluation, in that contextual information can be brought to bear to determine whether or not a stimulus is threatening in a particular circum- stance (as in extinction and other forms of contextual conditioning; see Bou- ton, Chapter 9). So, although I would act on my propensity to walk away from the snake if it is across my path when I am hiking in the forest, I might actually approach the snake if I were visiting a zoo and the snake was behind glass. My 5-year-old daughter, on the other hand, would likely approach the snake regardless, because she is very curious about snakes. In this way, evaluations can also be influenced by more complex conceptual processing, which can alter the behavioral plan.

The neural consequences of evaluation have a neuromodulatory effect on a wide array of output systems, from those that are typically associated with emotional responding (e.g., autonomic and endocrine changes, volun- tary behavior, facial movements) to those that are not (e.g., selective atten- tion, memory). These output response systems are influenced by non- affective processes as well (e.g., autonomic changes occur with simple

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changes in posture, endocrine changes occur after eating, facial movements occur for social communication), such that there is no specific class of “emotional behaviors,” no specific “action tendency,” facial “expression,” nor autonomic nervous system “patterning” that is unique to each kind of emotion. The output of any given response system (behavior, attention, facial movements) is multiply determined and can be considered more or less affectively infused in a given instant, depending on the extent to which it is constrained by evaluation. Furthermore, the extent to which behavior can be thought of as “affective” versus “emotional” depends on the kind of conceptual knowledge that is brought to bear during evaluation (a point to which I return later). As a consequence, freezing may be an innate behav- ior, and it may be part of the Western script for fear such that we automati- cally categorize freezing as an instance of fear, but this is not evidence, in and of itself, that freezing behavior is caused by some module of fear responding or gives evidence of fear.

A person’s core affective state is an accounting of how events and objects are influencing the state of the organism at a given moment in time (cf. Russell, 2003). It is similar to what Lambie and Marcel (2002) refer to as “emotion state.” In a sense, core affect is a neurophysiological barometer of the individual’s relationship to an environment. Core affect, at a given moment in time, can be influenced by automatic evaluations of what is in the focus of attention, as well as what is in the periphery (one’s background environment; Russell & Snodgrass, 1987; see evidence on background con- ditioning, Phillips & LeDoux, 1994). Everything that has been said about “emotion” may be true of core affect. The hardwiring to support core affect is present at birth (Bridges, 1932; Emde, Gaensbauer, & Harmon, 1976; Spitz, 1965; Sroufe, 1979). It can be acquired and modified by associative learning (e.g., Cardinal et al., 2002), although the original learning is indeli- ble, and newer learning is controlled by the context (Bouton, Chapter 9). Core affect (i.e., the neurophysiological state) can exist and influence behavior without being labeled or interpreted, and can therefore function unconsciously (e.g., Berridge & Winkielman, 2003; Winkielman, Berridge, & Wilbarger, Chapter 14). Core affect (and corresponding behavioral responses) can exist alone or can be represented and reported as a feeling.

Whether because of extreme changes that capture attention or deliber- ate introspection (such as when a person is asked to report a feeling), peo- ple verbally represent core affect as feelings of valence (pleasure or displea- sure) and activation (feeling sleepy or excited). When people are asked directly about feelings of pleasure or displeasure, activation or deactivation, they can report them (e.g., Russell, Weiss, & Mendelsohn, 1989). When people are asked about their experiences of emotion, they also communi- cate their core affective feelings (Feldman, 1995b; Russell, 1980; for a

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review, see Barrett & Russell, 1999). In fact, core affective feelings are implicitly communicated in self-reports of emotion experience. The extent to which a conscious feeling is characterized by one or the other property varies within a person over time (Barrett, in press), across people (Feldman, 1995a; Barrett, 1998, 2004b), and across cultures (Mesquita, 2003).

Indeed, people most often report core affective feelings as part of an emotional episode—a short-lived response that corresponds to the collo- quial idea of “having an emotion.” Although emotion is experienced as a discrete act, core affect is in constant flow and flux. People are continuously in some state of core affect, constantly moving their faces and their bodies. The possibility pursued here is that the ebb and flow of core affect is parsed into discrete events during the process of perception, and it becomes per- ceptually bound to the object that is believe to have caused the feeling in the first place. As a result, a person becomes angry with someone, afraid of something, sad about something. I suggest that we perceive emotion in our- selves in a way that is similar to the way we perceive the behaviors of oth- ers, termed person perception or ordinary personology. The general idea is that people emit a stream of actions (perhaps facial actions that are caused by evaluative processing and associated with core affective states). Cate- gory knowledge shapes those actions into the perception of an emotional event in others—emotion identification, if you will. Similarly, I argue here that we engage in emotion identification when we use category knowledge about emotion in the perception of our own core affective states, producing the experience of emotion.

How Is Emotion Perception Achieved?

Social psychology has accumulated a large and nuanced body of research on how people perceive one another’s behavior and infer causes (for review of this literature, see Gilbert, 1998). Originally, it was believed that people, like physical objects (or emotions, for that matter), had real properties that could be observed, so that it was possible to quantify the accuracy of per- ceptions of those properties (Brunswick, 1947). Very quickly, however, the field shifted away from questions about accuracy because it was discovered that the person properties under investigation—traits—defied simple mea- surement and clear definition. Instead, researchers became interested in understanding how people infer the properties of others—in particular, why people see certain behaviors and how they come to understand what caused them (Heider, 1944). In a sense, ordinary personology is the study of theory of mind—how people attribute mental states to self and others in order to explain and predict the behavior that is perceived in others. It might prove helpful to follow a path set by attribution theorists almost half

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a century ago to focus on the judgment process as a way of understanding how people perceive an emotion in themselves—and therefore experience that emotion.

Person Perception

Person perception involves three processes (for a review, see Gilbert, 1998), but for the purposes of this chapter we are most concerned with the process of behavior identification—how an observer perceives what a tar- get person is doing. People are constantly moving and doing things (such as moving their facial muscles). Somehow, we partition that continuous move- ment into recognizable, meaningful, discrete acts (such as a facial expres- sion). Bob is contracting his facial muscles, and water is coming out of his eyes; we recognize this movement as the behavioral act of crying. Bob is moving his feet heavily as he walks; we recognize this movement as the behavioral act of stomping. Inferring an intention is part of the behavior identification stage because observers prefer to identify behavioral acts in terms of the target’s intentions (cf. Gilbert, 1998). The inference of inten- tion gives meaning to the behavioral act. If Bob is stomping, then he is behaving angrily. He is in an intentional state (i.e., his behavior is caused). Because his anger mechanism is triggered, Bob is angry at this moment in time. We have categorized an instance of anger in Bob.

It is a well-known finding in social and cognitive psychology that prior information structures incoming information. This dynamic is very clearly the case in person perception, where the knowledge that is active in our minds influences what behaviors we see and what causes we infer, often without our awareness. Person perception researchers have focused their investigations on how category knowledge about persons (based on their prior behavior, group membership, etc.) influences behavior identification. Just as stereotypes about people shape our perceptions of what they do and why, category knowledge about emotion may act like “emotion stereotypes” to shape our perceptions of emotion in others and in ourselves. The argu- ment, then, is that self-perception is an act of person perception when the target of perception is the self.

Emotion Perception

Just as behavior identification is shaped by category knowledge about per- sons, emotion identification may be shaped by category knowledge about emotion. Behavior identification involves parsing a stream of actions into discrete bits by assigning them an intention to render them meaningful. Similarly, emotion identification (the act of emotion perception) may in-

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volve parsing the stream of core affect—whether the internal state (acces- sible to the emoter) or its behavioral consequence (accessible to the observer)—into discrete emotional bits by assigning an intention to render it meaningful. Just as we interpret or imbue behavioral actions with inten- tion when we parse them into a discrete behavioral act, so we imbue core affect with intention or emotional “aboutness” when we parse it into dis- crete acts of feeling. When a person identifies his or her core affect as being about something, it becomes intentional, and the experience of emotion begins.

There is evidence that conceptual knowledge about emotion seam- lessly shapes the perception of emotion in others. Some of the initial research on behavior identification examined how emotion category infor- mation influenced the identification of emotion in photographs of facial configurations and in verbal descriptions of emotional reactions (Trope, 1986). Additional studies have replicated and extended these findings (Bouhuys, Bloem, & Groothuis, 1995; Carroll & Russell, 1996; Halberstadt & Niedenthal, 2001; Trope & Cohen, 1989). If processes that enable us to know one another also allow us to know ourselves, then conceptual knowl- edge about emotion may quickly and unconsciously shape our identifica- tion of our own emotions in much the same way that it serves to shape our perceptions of emotion in others. Early perceptual processing may extract sensory information from the internal context in much the same way that sensory information is extracted from the external stimulus environment during object recognition (to determine whether or not there is an object present). For example, in much the same way as bottom-up (or stimulus- driven) processes extract information about perceptual features of the face during face recognition, processing of the somatovisceral information (con- stituting a person’s core affective state at a particular moment in time) may allow people to recognize that a shift in core affect has occurred. Shifts in core affect are then available to be identified in a manner that is similar to object identification. Just as conceptual knowledge is necessary to catego- rize a set of facial behaviors as an instance of anger, so too this knowledge may influence the categorization of our own core affective state during a process of emotion identification. It is possible that the categorization pro- cess can also be the result of more deliberative processing, either during introspection or when core affect is intense enough to be represented in awareness (in a manner reminiscent of Mandler, 1975, or Schachter & Singer, 1962). The reason that our experiences of emotion have a given quality is that emotion identification occurs outside of our awareness the majority of the time.

The conceptual system might shape the categorization of core affect into the experience of emotion with several consequences. These ideas

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were inspired by Barsalou’s (1999, 2003) discussion of the ways in which conceptual information supports perceptual inferences. First, to the extent that conceptual knowledge performs some sort of figure–ground segrega- tion, the experience of an emotion will “pop out” as separate from the ebb and flow in ongoing core affect. Second, once an instance of core affect is categorized, a rich set of inferences is available that constitutes expertise about how to deal with the world (including our feelings) at that instant in time. Third, conceptual knowledge of emotion can help us anticipate other aspects of the emotional response that are (whether correctly or errone- ously) expected, either speeding their perception or going beyond the information present to fill them in at a given perceptual instance. This part of the process can, perhaps, result in illusory correlations between re- sponse outputs (helping to explain why researchers continue to search for coordinated autonomic, behavioral, and experiential aspects of an emo- tional response). Fourth, conceptual knowledge about emotion allows us to go beyond the information given in another way, in that it guides us to assume what happened before the instance of core affect and what will hap- pen next—we fit what we see into a script so as to better predict our own behavior. In the next section, I consider how conceptual knowledge about emotion might achieve these effects.

Conceptual Knowledge and Categorization

Whenever we selectively attend, with some consistency, to components of experience, knowledge of a category develops (cf. Schynn, Goldstone, & Thibaut, 1998). The human conceptual system contains a collection of cate- gory knowledge, including knowledge about kinds of emotion. Children acquire emotion concepts over time (Widen & Russell, 2003). Each time a parent labels a child’s behavior with an emotion term, or a child hears the emotion term being used to label someone else’s behavior, the child extracts information about that instance and integrates it with past informa- tion associated with the same term that is stored in memory. In this way, children acquire emotion categories that conform to their culture.

In most discussions of emotion categories, the basic unit of knowledge is an emotion concept. A concept of a particular emotion, say, anger, is thought to contain a feature list that includes what triggers an instance of anger, what it feels like to be angry, what relational theme is likely to be present, physiological changes to be expected, what voluntary movements, vocal cues, and facial movements are typically involved, and what are the social rules for expressing the emotion. To know the script for anger in your culture is to know what anger is (Fehr & Russell, 1984). In the past, researchers have argued over the structure and format of these conceptual

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representations (e.g., Russell, 1991; Clore & Ortony, 1991), but most have agreed that concepts are part of the semantic memory system— decontextualized distillations of invariant properties that are extracted from previous instances of the category. These representations are termed amodal because they are abstracted from sensory–motor events and stored in some sort of propositional form, such as in an encyclopedia (Barsalou, 2003). They are thought to be nomothetically and idiographically stable. For a given emotion category, different people within a culture share roughly the same representation, and the same person uses the same repre- sentation on different occasions. All cognitive processes operate on these redescriptions, as the original sensory–motor representations are no longer needed.

More recently, Barsalou and his colleagues (Barsalou, 1999, 2003, in press; Barsalou, Simmons, et al., 2003) have challenged these ideas, sug- gesting that static entities called concepts do not exist. Instead of viewing categories as represented by invariant concepts that can be retrieved intact from long-term memory, each category is represented by a large number of specific instances, called situated conceptualizations. These situated con- ceptualizations are not amodal, abstract exemplars; rather, they are partial reenactments or simulations of the sensory–motor states that occurred with previous instances of the category. No single situated conceptualization need give a complete account of the category. An instance of a category involves the sensory, motor, and introspective states that come together in working memory in a way that is tailored to the current situation. Niedenthal and colleagues (e.g., Chapter 2) have reinterpreted existing evi- dence from research on attitudes, social perception, and emotion to support the idea that social knowledge is grounded in sensory–motor representa- tions. Most important for the position advanced here is their suggestion that emotion categories, as situated conceptualizations, are implicated in emotion perception.

A situated conceptualization (i.e., an instance of conceptualizing a cat- egory) is produced by a simulator (or set of simulators). As discussed in Niedenthal et al. (Chapter 2), a simulator for a category of knowledge, such as anger, develops as sensory–motor and somatovisceral sources of informa- tion are encoded during instances when words for anger are used. Sensory information about the objects (e.g., people) that are seen as causing anger, motor programs for dealing with anger, the coincident interoceptive states (such as those associated with core affect or cognitive operations), the broader stimulus situation or context are all integrated into the simulator. Extending this view, it is possible that an instance of core affect (i.e., the person’s current homeostatic state resulting from evaluation), along with representations of concurrent objects in the focus of attention, actions

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taken, the relational context, the emotion label provided by others, and so on, bind together to form an instance of anger. Because core affect is a cate- gory of experience, it may have its own simulator or be represented by its own collection of simulations that is embedded in emotion category simula- tors (see Barsalou, Niedenthal, Barbey, & Ruppert, 2003, for a discussion of embedded simulators). Properties that are pointed out by parents (or other speakers) or those that are functionally relevant in everyday activities will bind with core affect to represent anger in that instance. As these instances accumulate, knowledge about anger develops as a distributed neural sys- tem that involves both modality-specific and association areas. These estab- lish the conceptual content for the basic-level category anger and can be retrieved for later simulations of anger when needed. As a result, a situated conceptualization view of emotion knowledge is consistent with the view that core affect is a necessary part of every instance of emotion.

At the simplest level, the central hypothesis outlined in this chapter— that conceptual knowledge shapes the identification of core affective events—becomes more plausible if emotion knowledge is simulated. Cate- gory representations are characterized as sensory–motor events. Core affect consists of sensory–motor information. Since the two share a repre- sentational format, they could be seamlessly integrated during an instance of perception. This integration may be especially likely because emotion categories are abstract, and introspective state information is particularly important to abstract concepts (Barsalou & Wiemer-Hastings, in press).

Furthermore, situated conceptualizations have several distinctive prop- erties (for a detailed discussion, see Barsalou, 1999, 2003, in press) that allow for specific predictions about how emotion perception should pro- ceed, as well as its consequences for the experience of emotion. First, and most importantly, the situation will influence what is felt. A situated concep- tualization (e.g., an instance of conceptualizing anger) is inherently bound to a particular context (Yeh & Barsalou, 2002). Context is particularly important to conceptualizations of abstract categories (Barsalou & Wiemer- Hastings, in press) such as emotion. Information about the relational con- text (Lazarus, 1991) or a situation’s meaning to a person at a particular point in time (Clore & Ortony, 2000) may constitute some of the background information contained in situated conceptualizations of an emotion cate- gory that, like objects, may serve to launch a simulation. An experience of emotion, then, may be shaped by the situation, such that the experience of a given emotion, such as anger, will show great heterogeneity across instances within a person and across people. There are a multitude of sensory–motor simulations that belong to anger, each one producing a dis- tinct feeling state. This view is similar to what James (1884) proposed but is clearly different from Damasio’s (1994) somatic marker hypothesis, which

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states that there are specific somatic markers for particular emotion catego- ries (Damasio et al., 2000).

Second, language can intrinsically influence the experience of emotion. To the extent that language drives category acquisition, words will deter- mine which simulations are available for use during emotion identification. Language might also shape experience via production of novel simulations (i.e., representations of things that have never been encountered together; Barsalou, 2003). People may integrate in LTM two representations from the same emotion category, even when their surface similarities differ (see Barsalou et al., 2003), because the label for the emotion links them in mem- ory (see Gelman & Markman, 1987). Highly different instances for the same category can become integrated over time and become available for simulation during emotion identification. As a result, people can simulate and experience new combinations that will add to the range of emotion experience. This generative feature of situated conceptualizations may help to explain why people perceive prototypical emotion episodes, even though those episodes seem impossible to capture with the use of scientific instru- ments.

Third, experience may shape subsequent behavior. Situated conceptu- alizations contain inferences about situated action (i.e., the actions needed in a given situation). Although some of the behavior that we typically think of as “emotional” may result from core affective processes, it is possible, even likely, that once conceptual knowledge about emotion is activated, it can direct subsequent behavioral responses. Across varied situations, dif- ferent situated conceptualizations of a given emotion category arise, each designed to optimize one particular type of situated action associated with that category. For example, you may have learned a host of different actions associated with the category anger. Sometimes it works to yell, sometimes to pound your fist, sometimes to cry or walk away, sometimes to hit. During a given act of conceptualizing, you are most likely to simulate whatever action will allow you to achieve yours goals for the given situation. As a result, situated conceptualizations deliver highly specific inferences tai- lored to particular situations regarding what actions to take.

Fourth, experiencing an emotion, like conceptualizing in general, may be a skill. Some people may be better than others at tailoring conceptual knowledge to meet the needs of situated action (Barsalou, 2003). The peo- ple who are better at tailoring their simulations to the needs of the particu- lar situation will be more functionally effective than those who are less able to do so. Similarly, constructing such an emotion experience may also be a skill. Presumably, there is no single experience of anger, but many, depen- dent on the content of the simulation. It is a skill to simulate the most appropriate or effective representation, or even to know when to inhibit a

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simulated conceptualization that has been incidentally primed (Barrett et al., 2004).

Finally, the importance of situated action in situated conceptualizations may help explain why people perceive a prototypical emotional episode (i.e., what most people consider the clearest cases of emotion characterized as having all the necessary component parts; Russell, 2003; Russell & Barrett, 1999), even though such episodes are quite rare. Barsalou (2003) has argued that people are goal achievers who organize knowledge in catego- ries to support acting in the most functionally effective way. Over time, goal-directed categories become well established in memory (Barsalou & Ross, 1986), such that the most typical members of the category are those that maximize goal achievement (not those that are most frequently en- countered). If emotion categories are goal-directed categories, then the most typical instances of a category will not contain properties that appear most commonly as instances of the category, but those that represent the ideal form of the category—that is, whatever is ideal for meeting the goal around which the category is organized. This may be one reason that scien- tists typically theorize about and focus their empirical efforts on, prototypi- cal emotional episodes, even though the nonprototypical cases are more frequent in our everyday lives.

WHAT IS THE EXPERIENCE OF EMOTION?

In this chapter I have argued that the dominant scientific paradigm for explaining the experience of emotion assumes that there are natural kinds of emotion mechanisms that cause behavior and experience. Despite the lack of strong, compelling instrument-based evidence, many scholars con- tinue to hold this view, believing that there are real behaviors that can be called angry, fearful, sad, and so on. As a challenge to this view, I have out- lined the equally plausible model that to experience an emotion is to per- ceive it. In this view, emotions are not causal entities. They, themselves, are caused. Emotions do not explain anything. They are the things to be explained. My model of emotion experience involves three propositions. First, I proposed that core affect, as the neurophysiological state resulting from assessing the predictive value of a stimulus, is one basic substrate of experience. Core affect is available to be felt, although it need not be felt in any given instance. Second, I argued that the experience of emotion is psy- chologically constructed via the same processes with which we experience color, and each other. Knowledge of emotion categories shapes the percep- tion of core affect into an experience of emotion in much the same way that knowledge of color categories shapes the experience of a continuous wave-

276 THE EXPERIENCE OF EMOTION

length light spectrum, or how category knowledge about people shapes our perceptions of other people’s behavioral actions into meaningful acts. Third, I have suggested that the content and structure of category knowl- edge about emotion determines which emotion is perceived and, poten- tially, even what we feel. Because conceptualizing involves sensory–motor representations, conceptual knowledge about emotion can seamlessly shape the perception of core affect into the experience of an emotion.

The model that I have proposed clearly builds on key ideas from the psychological literature on emotion. Most clearly, my view owes a debt to social-constructivist models in which emotional states are culture-bound descriptions that are differentiated, defined, and labeled via schemas or mental representations of emotion concepts (e.g., Averill, 1980; Harre, 1986; White, 1993). It bears some resemblance to Schachter and Singer’s (1962) two-factor theory and to Scherer’s (e.g., Chapter 13) level of process- ing view, although there are notable differences. It is also broadly consis- tent with an appraisal perspective on emotion, in which appraisals are not so much a set of processes for generating emotion but the rules for describ- ing which emotions are felt when (Clore et al., Chapter 16). My view also is clearly inspired by William James, who, contrary to popular belief, did not argue that anger, sadness, and so on, have specific and unique patterns of somatovisceral changes in the entitive sense; rather, he argued for the het- erogeneity of instances within each emotion category. According to James, there can be variable sets of bodily symptoms associated with a single cate- gory of emotion, making each a distinct feeling state and therefore a dis- tinct emotion. By the term emotion, James was referring to particular instances of feeling, not to discrete emotion categories. What differentiates my model from these other perspectives is the emphasis on categorization processes as a core mechanism driving emotion experience.

It also seems important to point out that the view of embodied emo- tion knowledge discussed here can in principle be consistent with the idea of emotions as causal entities. People may have situated conceptualizations, not because they acquired emotion categories through language and label- ing, but because they learned about emotion mechanisms that already exist in the brain and body. Even the idea that emotion knowledge allows people to know emotions in others can be consistent with the idea that emotions exist as causal entities. Ontology is not identical to epistemology. Anger, sadness, fear, and so on, may be real mechanisms that cause behavior and experience, and people may perceive them accurately or inaccurately. Of course, this position assumes that there is some clear empirical criterion for judging the accuracy of emotion perceptions, which currently there is not. At best, the empirical glass is half full.

Of course, the value of the perspective that I have outlined in this chapter will rest or fall with empirical evidence. Undoubtedly, a major

Feeling Is Perceiving 277

research initiative is required to test these ideas. For now, it is reasonable to point out that there is scientific precedent for taking this point of view. Many psychological constructs that scientists once thought of as fixed, uni- tary causal entities with an identifiable essence (e.g., memory, personality, concepts, attitudes) are now thought of as emergent properties or byprod- ucts of distinct but interacting systems (Barsalou et al., 2003; Johnson, 1992; Johnson & Hirst, 1993; Mischel, 1984; Mischel & Shoda, 1995; Schacter, 1996). Furthermore, there is recent evidence from artificial intel- ligence research indicating that language shapes the acquisition of category knowledge (Steels & Belpaeme, in press). People come to know what the color blue is because other people (parents, other adults, etc.) teach them, as children, to associate objects that reflect particular wavelengths with words for blue. Recent research on the categorical perception of color (Özgen, 2004; Özgen & Davies, 2002) suggests that language influences perception by shaping the boundaries of specific color categories. There is also good scientific evidence for the idea that conceptual knowledge influ- ences perception, whether about physical objects (e.g., Palmer, 1975), phe- nomenal contents such as color (Davidoff, 2001), or people (Gilbert, 1998). And then there is evidence that conceptual knowledge is embodied (Barsalou, 1999; Barsalou et al., 2003), that emotion knowledge, in particu- lar, may be embodied (see Niedenthal et al., Chapter 2) and have a role in shaping perception (for a review, see Niedenthal & Halberstadt, 2003). If conceptual knowledge has pervasive effects on perception, then perhaps it is involved with perceiving emotion in the self and others. Why should we assume that the perception of emotion is different from the perception of anything else?

ACKNOWLEDGMENTS

Many thanks to Larry Barsalou, Paula Niedenthal, and Piotr Winkielman for their helpful comments on an earlier draft of this chapter. Preparation of this chapter was supported by National Science Foundation Grant Nos. SBR-9727896, BCS 0074688, and BCS 0092224, and by National Institute of Mental Health Grant No. K02 MH001981.

NOTES

1. Feeling does not necessarily serve as evidence of the causal mechanism to observers, however. For the observer (observing the emoter), an emotion is revealed by expressive behavior, over and above anything else (including the emoter’s verbal report).

2. Admittedly, the neural systems involved in early sensory processing of faces and

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core affective information would be somewhat different, however. Early per- ceptual processing of somatovisceral information associated with core affective state may involve posterior aspects of the insula. This information is re- represented in the anterior insular cortex and other parts of a larger system (including anterior cingulate cortex, limbic motor areas, and orbital frontal cor- tex) thought to be responsible for the subjective experience of feelings in humans (Craig, 2002).

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PART V

Perspectives on
the Conscious–Unconscious Debate

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TEHmEotiConONanSdCDIOuaUl-SP–rUocNeCssOMNoSdCelIsOUS DEBATE

CHAPTER 12

Emotion Processes Considered from the Perspective
of Dual-Process Models

ELIOT R. SMITH ROLAND NEUMANN

For at least two millennia, people seeking to explain their own and others’ behavior have resorted to explanations in terms of two distinct and often conflicting inner mechanisms. For example, St. Paul, in his Epistle to the Romans, lamented:

I can will what is right, but I cannot do it. For I do not do the good I want, but the evil I do not want is what I do. Now if I do what I do not want, it is no lon- ger I that do it, but sin which dwells within me. . . . I see in my members another law at war with the law of my mind and making me captive to the law of sin which dwells in my members. (Rom. 7:15–23)

This same core insight—that our thoughts and behavior are driven by two separate and often conflicting mechanisms—has recently become part of social-psychological theories of phenomena as diverse as stereotyping (Devine, 1989), attitude–behavior relations (Fazio, 1986), and persuasion (Petty & Cacioppo, 1986). These dual-process models, of course, do not use labels such as “the law of sin” and “the law of my mind,” but refer to the two processes as heuristic and systematic (e.g., Chaiken, 1980) or associative

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1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

Emotion refers to a bundle of loosely related processes (involving appraisal, affect, motivation, expressive behaviors, activation and use of semantic knowl- edge, subjective feelings, and self-regulation), not to a single “thing.” In para- digm cases all these processes may unfold in parallel in reaction to the same event, but dissociations among the processes are also common (because each process has many potential causes). This definition is similar to the one we would give for cognition, which also refers to a bundle of loosely coupled pro- cesses involving information transformation, representation, etc., rather than to a single conceptual entity.

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

A useful and at least somewhat precise term is preconscious, which refers to processes that are (a) generally automatic, given relevant stimulus input, and (b) whose results are accessible to conscious awareness. Examples are recognizing a familiar face or accessing the meaning of a written word in one’s native lan- guage, which are automatic in that one cannot simply decide not to perform these processes. Preconscious processes constitute our subjective experience, allowing us to see a world of meaningful objects and events. In contrast, fully conscious processes involve effortful, controlled search for and use of relevant or appropriate information, with the process itself as well as its result being available to awareness.

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

Our theory deals with two types of processing (which we term associative and rule based) that are correlated with, but not identical to, the preconscious– conscious distinction.

and rule based (Sloman, 1996). Recently, Smith and DeCoster (2000) reviewed a number of such dual-process models that have been formulated in different topic areas, making the argument that despite differences in detail, they all essentially rest on the same distinction between two basic processing systems. They adopted Sloman’s (1996) labels, associative and rule based, for the systems. Since Smith and DeCoster’s review, still other models sharing the same family resemblance have appeared (Strack & Deutsch, 2004; Lieberman, Gaunt, Gilbert, & Trope, 2002). Except for a few who adhere to single-process models (e.g., Kruglanski, Thompson, &

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Spiegel, 1999), it seems that dual-process models represent mainstream thinking within wide areas of social psychology, particularly social cogni- tion, today.

However, although emotion theorists have addressed several related ideas, explicit application of dual-process models to the processes involved in the elicitation and control of emotion is only beginning. This chapter begins by summarizing the general features of existing dual-process mod- els, including brief comments on the two recent ones just referenced. Like Smith and DeCoster (2000), we emphasize their similarities rather than their points of difference. The core of the chapter then describes thoughts and hypotheses about how emotion fits into the general dual-process framework. We conclude with comments on a number of implications aris- ing from this way of thinking.

DUAL-PROCESS MODELS Review of Dual-Process Models

In their review and integration, Smith and DeCoster (2000) draw on evidence from cognitive and neuropsychological sources as well as from existing dual-process models in social psychology. Their starting point is dual-memory-system models, discussed by numerous theorists in re- cent decades (e.g., Tulving, 1983; Sherry & Schacter, 1987; McClelland, McNaughton, & O’Reilly, 1995). These models hold that humans have two interacting but separate memory systems. The rationale for a dual-system model is that the adaptive demands on memory inherently conflict and are difficult or impossible to satisfy within a single memory system. One demand is to record information incrementally, slowly building up repre- sentations based on a large sample of experiences, so that stable knowledge and expectancies about the environment can be recorded in an enduring fashion. A conflicting demand is to record information quickly, so that events that occur only once can be recorded and used to direct adaptive action in the future. But if each passing event leaves a strong and lasting trace in memory, the resulting disruption will make it impossible to build up a stable record based on a multitude of experiences. This conflict has been termed the “stability/plasticity dilemma.”

This logical argument about the conflicting demands of slow and rapid learning is paralleled by neuropsychological evidence (reviewed in McClelland et al., 1995) that points to the existence of two memory systems that serve these adaptive demands. A slow-learning system (based in corti- cal regions) records information slowly and subserves learning of cognitive skills based on extensive practice, as well as learning of general regularities,

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covariations, or associations in input stimuli, possibly across many sensory modalities. After they are learned, these regularities are used to generate expectations and fill in unobserved details in new input information, a func- tion that has often been termed schematic processing in cognitive and social psychology. A fast-learning system, mediated by the hippocampal region of the brain, records episodic memories of events that occur only once. Proba- bly the strongest evidence for the independence of the two memory sys- tems is that the latter system is selectively impaired by hippocampal lesions that leave the slow-learning system relatively unimpaired (e.g., Squire, 1992). Because the fast-learning system requires attention and other cogni- tive resources for its operation, it can be disrupted by distraction, compet- ing task demands, etc.

Two processing modes depend on the respective properties of the two memory systems, according to Smith and DeCoster (2000). Associative pro- cessing is based on the properties of the slow-learning system. When new stimulus information is encountered, this type of processing uses knowl- edge that has been acquired from a large number of previous experiences to fill in information that is unobserved in the current situation, quickly and automatically. The process can be aptly characterized as a preconscious “pattern completion” mechanism (see Niedenthal, Barsalou, Ric, & Krauth- Gruber, Chapter 2). That is, suppose one has encountered dogs on many occasions, leading to the development of a multimodal representation in the slow-learning memory system that involves dogs’ visual appearance, barking sounds, their typical behaviors, the sound of the word for dog, as well as one’s typical affective and behavioral responses to the presence of a dog (whether fearful withdrawal or joyful playfulness). This entire repre- sentation can be reactivated (i.e., the pattern can be completed via memory retrieval) by an encounter with any sufficiently distinctive subpart—such as the sound of a bark. Importantly, distinct representations could be built up for dogs encountered in separate contexts (e.g., household pets vs. dogs running wild outside) or for separate types of dogs (e.g., large German shepherds vs. small poodles), and then the context-specific version could be reactivated on a future occasion, depending on the perceptual cues. Associative processing is shared with nonhuman animals, for it does not de- pend on linguistic or other abilities that are unique to humans. There is lit- tle or no conscious awareness of the retrieval or pattern-completion pro- cess, only of its results (thus the process is termed preconscious).

In contrast, rule-based processing uses symbolically represented knowledge (such as logical inference rules) to direct processing. For exam- ple, suppose someone from a different culture treats one in a way that seems disrespectful. An immediate (associative) response may be anger. But an attributional search involving effortful consideration of all the sur-

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rounding circumstances may lead to the conclusion that the offense was inadvertent, caused by the person’s ignorance of local cultural norms. This conclusion might dissolve the anger. Rule-based processing is unique to humans (and, perhaps, a few of our closest primate cousins). Rules may be stored in either memory system, depending on whether they have been encountered only a few times or many times over an extensive period (in which case they could be stored in the slow-learning system). Rule-based processing is more effortful and less automatic than associative processing, so it can be selectively disrupted by distraction, cognitive load, and the like. Rule-based processing is also generally available to conscious awareness at each step of the processing (e.g., each potential attribution for a person’s behavior that is considered), not only the final result.

One of the key points emphasized by Smith and DeCoster (2000) is that the two processing modes draw on partially independent memory sys- tems or “databases” of stored knowledge. Associative processing depends on associations, built up by repeated experiences over time, through which a person might form a representation (for example) linking yellow-striped insects and painful stings. Such a representation may not be verbalizable or accessible as explicit knowledge. Smith and DeCoster describe how associative learning and pattern completion can be accomplished by a connectionist network.1 In contrast, rule-based processing depends on lin- guistically encoded propositions, structured by logical relations rather than by simple repeated co-occurrence. Such a rule could be learned from a sin- gle exposure. Interestingly, associative and rule-based knowledge might conflict. In fact, social-psychological studies using dual-process approaches have often focused on exactly that issue. For example, dual-process models have been widely applied to help understand stereotyping processes. Researchers assume that many people have learned associations of stereo- typic traits to various social and ethnic groups (based on a long history of exposure to cultural stereotypes in the media, etc.) but also maintain explicit propositional beliefs that reject those stereotypes (e.g., Devine, 1989). Given adequate time and attentional capacity, people may be able to use their explicit beliefs to override the automatically (associatively) acti- vated stereotypic information.

Most of the dual-process models that have been formulated with- in specific topic areas in social psychology (e.g., Fazio, 1986; Petty & Cacioppo, 1986; Chaiken, 1980; Brewer, 1988) and in cognitive psychology (e.g., Sloman, 1996) fit quite well within this general framework. The mod- els use different terminology, of course, and they differ in some details, notably regarding whether the two types of processing proceed in parallel or sequentially (associative followed by rule based)—Smith and DeCoster (2000) hold that processing is parallel. But all the reviewed models share

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the general theme that one processing mode operates automatically and preconsciously to structure people’s conscious experience, with little de- pendence on attention or cognitive resources. For example, people may evaluate a persuasive message without much explicit thought if easily noticed features (e.g., its length or the attractiveness of the communicator) are associated with positive or negative evaluations; such an association allows the perceiver to arrive at a quick favorable or unfavorable impres- sion. Or people may respond negatively to an individual who is a member of a particular group if negative stereotypic features associated with that group are automatically activated upon encountering the individual. The second processing mode operates optionally, uses more powerful inferen- tial means, and requires attention and subjective effort. Using this mode, people may scrutinize the persuasive arguments in a message in detail, comparing them to their general knowledge to arrive at a reasoned judg- ment about the message. Or they may examine the individual’s personal attributes, effortfully seeking to go beyond the simple group-membership information (and associated stereotypes) to determine the individual’s true characteristics.

Newer Dual-Process Models

Strack and Deutsch (2004) recently advanced a new dual-process model that has some innovative features but also shares the same general assump- tions. Briefly, Strack and Deutsch distinguish an impulsive system (similar to the associative system discussed above) from a reflective system (similar to rule based). Their discussion emphasizes the role of the two systems in governing overt behavior, such as approach or avoidance of an object, and not just processing within the head. They also propose that the reflective system, as part of its ability to process propositional representations, can represent and use negations, whereas the impulsive system cannot do so. In fact, a frequently encountered negation (e.g., “Nixon is not a crook”) may lead to an association between the concepts and therefore the automatic activation of crook whenever Nixon is encountered—despite the fact that the propositionally based reflective system can produce judgments or behavior indicating correct comprehension of the negation.

Lieberman et al. (2002) also recently advanced a dual-process model that again fits the same general outline. Their terms are reflexive (x) for the associative system and reflective (c) for the rule-based system. Like Smith and DeCoster (2000), they hold that the reflexive system rests directly on the properties of a connectionist memory system that slowly builds up asso- ciations over time and uses them as a pattern-completion mechanism. Their unique contribution is to emphasize the way the reflexive system

Emotion and Dual-Process Models 293

structures our conscious experiences of the world, whereas the operation of the reflective system is experienced as our reflections, thoughts, or reac- tions to the perceived world. They also devote attention to the “alarm” functions that call the reflective system into activity when the more auto- matic (but less powerful) reflexive system gets into trouble or reaches an impasse. Finally, they hypothesize linkages of the distinct processing sys- tems to separate brain structures. They follow McClelland et al. (1995), on whom Smith and DeCoster (2000) also rely, in linking the reflective system to hippocampal areas (see also Phelps, Chapter 3), as well as to the anterior cingulate and prefrontal cortices.

Despite these differences in emphasis, overall, the processing modes described by Strack and Deutsch and Lieberman et al. seem to be readily identifiable with those of the other models discussed in Smith and DeCoster’s (2000) review.

EMOTION PROCESSES FROM THE PERSPECTIVE OF DUAL-PROCESS MODELS

Our main purpose in this chapter is to discuss processes involved in the elicitation and control of emotion within this dual-process conceptual framework. Several emotion theorists have advanced ideas that can be directly related to this framework, and we briefly review these before dis- cussing a conceptual integration in more general terms. We begin, though, by noting that important classes of emotion models have not explicitly incorporated the notion that humans possess two distinct modes of mental processing.

Ambiguity of the Term Appraisal

Highly influential approaches to emotion, such as appraisal models and related theories (e.g., Weiner’s attributional model of emotion, 1986) sought to specify the cognitive processes that determine the quality and the intensity of emotions. However, these approaches were often unclear on whether appraisals are conscious/reflective or not. Some researchers explicitly proposed that appraisal processes are relatively automatic and inflexible, whereas others suggested (either explicitly or by implication) that appraisal processes that have more of a flavor of reflective reasoning might be responsible for eliciting emotions (e.g., Weiner, 1986).

From the dual-process perspective, it appears that the term appraisal has been used to label fundamentally different types of information that are processed in fundamentally different ways. (In a similar way, the term infer-

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ence has been used to refer to both automatic/associative and reflective forms of processing, despite their different properties; see Lieberman et al., 2002). Many emotion theorists have recognized this point (e.g., Smith & Kirby, 2001; Scherer, 2001), which was also central in the “affective pri- macy” debate between Zajonc and Lazarus (see Schorr, 2001, for a sum- mary). Appraisals can include relatively low-level perceptual features (e.g., an object rapidly looming in the field of vision) that produce affective reac- tions. But equally, high-level conceptual features resulting from sophisti- cated reasoning and inferential processes, such as attributional inferences, can also produce emotional responses. In summary, the widespread use of the single term appraisal in these very different ways may have subtly dis- couraged application of dual-process thinking in the area of emotion pro- cesses.

Dual-Process Ideas in Emotion Theory

Several emotion theorists have advanced ideas that overlap in important ways with dual-process models of the sort reviewed above. Keltner and Haidt (2001) distinguish two classes of emotions. Primordial emotions are universal, biologically based patterns of appraisals and responses observed across species and cultures, whereas elaborated emotions are packages of meanings, social practices, and norms that are built up around emotions in a particular culture. The authors emphasize that the elaboration process loosens the link between a primordial emotion and its original evolutionary function. For example, the primordial emotion of disgust, originally serving to compel the organism to avoid ingestion of contaminated food, comes to be applied to norm violators or holders of unpopular ideas, who might met- aphorically contaminate the social group. The distinction drawn by Keltner and Haidt has obvious relevance to dual-process ideas, but with two impor- tant caveats. First, we would refer to distinct processes (i.e., associative vs. rule based) that give rise to emotion, rather than distinct classes of emotion. In other words, and consistent with some of these authors’ own points, a given emotion such as disgust may, at times, be produced by one type of process and, at times, by another, so it seems imprecise to talk of two classes of emotions. According to our point of view, a similar outcome (e.g., a simple affective response or a fully self-aware emotional experience) may be produced by either type of process (Nisbett & Wilson, 1977). Second, we would emphasize that elaborated emotions (as well as primordial ones) could be experienced frequently enough over time that they too could come to be elicited through associative processes, given a relevant situa- tion.

Ochsner and Barrett (2000) describe emotion as resulting from interac- tions between automatic, nonconscious processes and more deliberative

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processes, using an overall framework that has much in common with social-psychological dual-process models. Automatic bottom-up processes classify events or objects as positive or negative in valence and initiate gen- eral affective responses and preparations for generic bodily actions such as approach or avoidance. Top-down reflective processes can operate flexibly, directing attention to specific aspects of an event, regulating or inhibiting overt actions, or applying complex knowledge (including general knowl- edge about emotions), often in the service of self-understanding or self- regulatory goals. For these writers, a consciously experienced emotion occurs only when both types of processes are engaged and produce an affective response that is accompanied by the activation of semantic knowl- edge, including a verbal label for the emotion. We would add that an emo- tion label (such as fear) may become associated with a particular situation (the sight of a large dog) and affective responses (negative arousal), so that the entire package of responses, including not only affective changes but also activation of a verbal label, may be generated fairly automatically by associative pattern-completion processes.

Leventhal and Scherer (1987) distinguished three forms of information processing that can lead to affective responses, two automatic and one more deliberate. On a first level of information processing, sensory–motor pro- cesses can lead to affective responses. For example, loud and abrupt sounds can trigger fear responses. Second, learned associations (such as that between weapons and aggression; Berkowitz, 1993) mean that an encoun- ter with such a cue (a weapon) can activate schematic representations that in turn elicit affect (see Teasdale, 1999, for a similar idea). Both of these more automatic and inflexible forms of information processing are exam- ples of associative processes, in our view. Leventhal and Scherer (1987) distinguish these two automatic forms of processing from conceptual pro- cessing, a more deliberate form of information processing that involves propositionally organized memory structures (similar to our rule-based processing).

Clore and Ortony (2000) use the same terms as Smith and DeCoster (2000), associative and rule based, to describe two processing modes that can result in emotion elicitation. Associative processing is regarded as a form of memory retrieval in which a prior affective response to an object is reactivated or reconstructed, in a fast and automatic but relatively inflexible way, when the object is encountered again. Rule-based processing, in con- trast, is driven more by sensory inputs and “computes” an appropriate affective response, taking more time but allowing great flexibility of re- sponding. These theorists differ from Keltner and Haidt (2001) in postulat- ing two types of processes that can produce the same set of emotions, rather than two distinct sets of emotions. Overall this view is similar to our own.

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Similar emphases are evident in the discussion by Matthews and Wells (1999) of automatic and controlled processes in emotion. Focusing on nega- tive stimuli, they postulate that a stimulus-driven network automatically generates affective responses to threat stimuli. A separate supervisory sys- tem maintains and regulates processing with regard to specific goals. The authors emphasize that the attention-demanding quality of negative stimuli may result from either type of processing: automatic attentional demands arising from the lower-level system, or the activation in the supervisory sys- tem of specific goals leading to attentional focusing (on the self or on the environment, monitoring for threats), which lead to rumination or worry.

LeDoux (e.g., 1996) provides a broadly similar analysis, but with the addition of significant neurophysiological detail (see also Teasdale, 1999). Focusing on threat-related stimuli, LeDoux notes that cognitive analyses (of what the stimulus is) are distinct from affective analyses (of what the stimulus means for the individual’s safety). These affective computations are generally performed in the amygdala, which receives inputs from many different areas of the sensory cortex, and lead to multiple behavioral and autonomic responses (e.g., increased heart rate, preparation for flight). Other inputs flow to the amygdala from the hippocampus, facilitating affec- tive responses based on episodic memories of previously experienced events—in other words, associative reactivation of an affective response. These latter pathways also allow for the cognitive modulation of amygdala activity based on larger situational contexts, such as the recognition that a specific stimulus poses a threat in one class of situations but not in another. However, the ability to carry out such modulations requires repeated prac- tice; one cannot simply cognitively “decide” not to be afraid of a given type of stimulus and have that decision become immediately effective. In our model this requirement of considerable repetitions marks the “cognitive modulation” process as part of the associative processing mode.

Toward Conceptual Integration

A paradigm example of the application of dual-process thinking in social cognition involves the stereotyping processes. Upon encountering a mem- ber of a stereotyped group, well-learned stereotypic attributes are automat- ically activated through associative processes in the perceiver. If the perceiver is processing minimally, the stereotype will likely control behav- ior (leading, e.g., to avoidance of the target). In contrast, given time and cognitive capacity, the perceiver can effortfully call to mind more symboli- cally represented beliefs and personal standards against using stereotypes and try, in various ways and with varying degrees of success, to control or override the effect of the automatically activated material on judgments and behavior.

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Applying similar thinking to a central example of emotion processing, phobias, we would say that upon encountering a trigger stimulus (per- haps a snake or a large dog) that has frequently been associated with fear in the past, affective responses are automatically reactivated in the phobic person. If the perceiver is processing minimally, the affective response will control behavior. In contrast, with time and cognitive capacity the perceiver can remind him- or herself that the stimulus is not actually dangerous and try, in various ways, to control or override the effects of the automatically activated feelings. These efforts may be more or less successful (Gross, 1998).

Associative Processes in the Elicitation of Emotions

To flesh out different aspects of the overall similarities between these accounts, we begin by discussing the associative activation of emotion. In standard dual-process models several points are similar to the associative processing mode. First, frequent pairing in the past of a specific stimulus with an emotional response (as with a social stereotype) leads to the devel- opment of an association, which can reactivate the response when the stim- ulus is again encountered. Thus a child who has been burned by a fire sev- eral times may come to fear the sight or sound of a fire even if no heat can be felt. In the development of panic disorders, it is assumed that exposure to panic attacks causes the conditioning of anxiety to exteroceptive and interoceptive cues (Bouton, Mineka, & Barlow, 2001). The resulting net- work of associations allows the cues to activate the whole network, includ- ing the different emotional components. This formulation explains why behavioral responses such as emotional expressions can influence emotions (for an overview, see Adelman & Zajonc, 1989). In a similar vein, for an individual suffering from a posttraumatic stress disorder (PTSD), a single cue such as a smell or the shape of an object can reactivate the whole pat- tern of associations, which in turn trigger the emotional response. The operation of the pattern-completion mechanism explains why a degradation of the perceptual input can nevertheless activate the same response. Evi- dence for such a mechanism comes from a study by Bradley, Codispoti, Cuthbert, and Lang (2001). In this study pictures generated essentially the same affective responses—both self-reported emotion and physiological reactions—whether they were presented in color or black and white. Thus a reduced version of the presented information might nevertheless be suffi- cient to elicit affective responses. According to Dimberg, Thunberg, and Elmehed (2000), subliminal exposure to facial expressions elicits congruent facial responses. Lundqvist and Öhman (Chapter 5) suggest that this effect might be due to some specific patterns of facial features, such as the eye- brows.

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In sum, it has been shown that many different types of cues have the potential to activate various experiential, physiological, and behavioral aspects of emotion. We emphasize that this is (in our view) due to the oper- ation of an associative pattern-completion mechanism. Once an entire pat- tern involving multiple components is experienced many times, any one of the components becomes capable of reactivating the entire pattern. One implication of this perspective is that arguments about the “true” causal sequence between different components of emotion (e.g., appraisals and subjective experience, or experience and expressive behaviors) are point- less, because any of these components can be causally effective in reactivat- ing any other.

Second, the associative reactivation of a well-learned pattern is fast and automatic in the sense that a simple cognitive decision cannot prevent it (i.e., deciding that the dog is not dangerous or that the stereotype is incorrect). In other words, associative responses are not “cognitively pene- trable.” For example, Rozin, Millman, and Nemeroff (1986) reported that people exhibited disgust at the sight of chocolate in the shape of feces, despite their knowledge that the material was simply chocolate. The speed of an associative response might be adaptive, but on the other hand, it makes this process relatively inflexible.

Third, associative reactivation can occur without conscious awareness of the stimulus that triggers the reactivation. This point has been amply established in many studies demonstrating that subliminal stimuli (of which the perceiver is not consciously aware) influence both social–cognitive judgments and affective responses (Bargh, Chen, & Burrows, 1996; Murphy & Zajonc, 1993). For example, Öhman and Soares (1994) showed that peo- ple with phobias experience elevated skin conductance responses to sub- liminally presented pictures of spiders or snakes. Aside from laboratory presentations of stimuli in highly controlled brief flashes, this process may have much relevance in everyday life. An affectively laden past experience may be reactivated by a stimulus that receives little conscious attention (perhaps because it is but one element in a crowded scene), leading to a “mood” for which the perceiver is unable to assign a cause.

Despite these similarities, one salient point regarding associative pro- cesses and emotion differs from other areas in which dual-process models have been applied. In general such models have assumed that frequent co- occurrences are necessary to build up an association between a stimulus and response. However, it is well known that specific stimuli are orders of magnitude easier to associate with particular affective responses (e.g., snakes with phobic responses) compared to arbitrary stimuli. One or a few experiences with such a biologically relevant stimulus may suffice to create an association that would otherwise take much repetition to develop.

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A major component of such quick associative responses may be the creation of simple linkages between the fundamental dimension of evalua- tion and various other responses, including behavioral approach or avoid- ance. Evaluation has been shown to influence many types of responses, early in processing. For example, smiles can be generated faster in response to positive words and frowns faster for negative words (Neumann, Hess, Schulz, & Alpers, in press). Not only facial expressions but also approach and avoidance movements are closely linked to the processing of valence (Strack & Deutsch, in press; Neumann, Foerster, & Strack, 2003; Winkielman, Berridge, & Wilbarger, Chapter 14). For example, bodily movements inter- preted as avoidance are faster in response to negative words, whereas movements interpreted as approach are faster in response to positive words (Chen & Bargh, 1999).2 It is likely that a few experiences suffice to create an association between the valence of an object and the representation of behavioral approach or avoidance responses. Of course, it is possible to engage in action that is opposite to these automatic behavioral tendencies, but only by exercising effortful control.

Rule-Based Processes in the Elicitation of Emotions

Emotion can be elicited by thoughtful, reflective processing. For example, anxiety can result from thinking about what other people might think of me (reflective or rule-based processing) as well as by the mere perception of a snake (associative processing). Disgust can be elicited not only by the visual qualities of an object (as just mentioned) but by what one explicitly knows about the object—for example, by the knowledge that an insect had crawled over tasty-looking food (Rozin et al., 1986). Fear can be elicited by actual exposure to a fearful object or by the anticipation of threats in the future. Anger can be induced by aversive stimuli such as cold or hot tem- peratures or by considering whether someone deliberately violated a norm (Berkowitz, 1993).

Thus rule-based processing allows for a more flexible activation of emotional response, in ways that are more sensitive to the social context. For example, foods that are eaten with gusto in some cultures are viewed as disgusting in others. Similarly, cultural norms can influence the situations and events that elicit emotions such as shame or pride (Mesquita, 2001; Neumann & Steinhäuser, 2003). However, this higher sensitivity of rule- based emotional responses to potentially shifting circumstances and cul- tural norms has its price: Reflective or rule-based processes are more effortful and can thus be undermined by a lack of cognitive resources. Therefore, distraction is sometimes successful in regulating emotions. For example, anger can be generated by an effortful analysis of the motives

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behind another person’s action. In such cases counting to 10 might be a successful (distraction) strategy to prevent socially inappropriate behavior because it redirects one’s attention, thereby (ideally) preventing the at- tributional analysis that gave rise to the angry feelings.

Emotion Regulation

Rule-based processing is important not only in the initial evocation of emo- tion but also when people attempt to control or regulate emotions. The examples that opened this section both dealt with intentional control (of activated stereotypes or of an affective response viewed as inappropriate). It seems clear that the very automaticity of associatively generated re- sponses makes their direct suppression difficult and costly at best, and inef- fective at worst (stereotypes: Macrae, Bodenhausen, & Milne, 1995; emo- tions: Richards & Gross, 2000). Under what conditions can associatively driven responses be controlled or overridden by more reflective processes?

According to the approach presented in this chapter, rule-based con- trol should be successful to the extent that an event or situation has not already triggered associative processes. Recent research has shown that smiles can be produced faster in response to pleasant words, whereas frowns are faster in response to unpleasant words (Neumann et al., in press). This finding suggests that although one can exert voluntary control over one’s emotional expression (e.g., smiling when processing negative information), associative processes are faster in supplying a congruent response than an incongruent response.3 Moreover, suppression of already activated responses requires cognitive resources and may therefore impair other processes essential for social interaction and memory encoding (But- ler et al., 2003; Richards & Gross, 2000).

More successful control uses one of three strategies. One can attempt to reinterpret or recategorize the original stimuli—in other words, to think of them in new ways (i.e., reappraisal strategies; Gross, 1998). Whether this strategy is possible when the emotion is due to associative processing is currently unclear. One can direct attention to different (less affectively evo- cative) aspects of the overall stimulus situation (analogous to directing one’s attention to a stereotyped target’s unique individual attributes rather than to the target’s group membership). However, this approach might not be feasible in highly evocative circumstances: for example, the would-be ski- jumper who suffers from fear of height, or a tunnel-phobic person con- fronted with spelunking.

Finally, in a longer-range sense, control is possible by repeatedly pair- ing the stimulus with a different, incompatible affective response. This approach recognizes that a single experience cannot have much impact on

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the slow-learning memory system on which associative processing is based, but that repeated experiences can build up new representations over time. Thus, in the treatment of phobias, people are exposed to the nondangerous stimulus time after time, without experiencing any harm. As an effect of the frequency of exposure, the phobic response gradually weakens (Bouton, Chapter 9; Bouton et al., 2001; Foa & Kozak, 1986; Quigley & Barrett, 1999). In a similar way, the sight of blood or saliva evokes disgust in most people. It is therefore an important part in the training of physicians to overcome their immediate emotional response toward these classes of stim- uli. From the perspective of the dual-process model, the need for repeated exposures is clear evidence that these emotional responses are due to asso- ciative processing rather than to reflective processing. In contrast, an emo- tional response that hinges on rule-based processing, such as fear in response to hearing that a dangerous criminal is on the loose in one’s neigh- borhood, should evaporate immediately upon learning that the criminal has been captured by the police.

Relation to Core Affect Theory

For insights into the ways that associative and rule-based or reflective pro- cessing interact to shape an entire emotion episode, we turn to core affect theory. Russell (2003; Barrett & Russell, 1999) recently advanced this inte- grative model of emotion. In this model, affect states that are describable within a two-dimensional space whose axes are pleasantness and arousal, are at the core of all emotions (as well as moods). Core affect changes in response to many types of external stimuli as well as internal processes (such as diurnal rhythms) and is assumed to be subjectively perceptible (leading to a sense of feeling good, bad, energized, tired, etc.). A change in core affect that is consciously experienced and attributed to some cause constitutes the beginning of an emotional episode. This attribution marks the transition between feeling an amorphous, unpleasant activation and feeling that way because of a snake, or between feeling vaguely unpleas- antly deenergized and feeling that way about a just-ended relationship. As Russell (2003, p. 149) writes, “Sometimes the cause is obvious; sometimes a search is required; sometimes mistakes are made.” The attribution is func- tional in directing attention and behavior with regard to the object that is responsible for the emotion.

In the next stage of the core affect model various components of the emotional episode, including the core affect and the perceived cause, as well as situational factors, overt behaviors, and bodily experiences (such as physiological changes), form input to a perceptual process that gives rise to the experience of emotion (Barrett, Chapter 11), or to what Russell

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(2003) terms “emotional meta-experience.” In effect, the person con- sciously notices or recognizes that he or she is afraid, sad, guilty, or experi- encing any of numerous other emotions. Thus the perception of emotions is composed of many different inputs, and the mechanisms involved are anal- ogous to those that have been well studied in the area of person perception (Barrett, Chapter 11).

Note that the core affect model inverts the causal ordering assumed in the naïve or common-sense model of emotion, which says that some event (e.g., danger) causes an emotion (fear) that is assumed to be a unique inner state, which then causes subjective feelings (being afraid), nonverbal expressions, autonomic changes, and instrumental actions. This idea im- plies that all these types of changes should generally covary, contrary to the findings of emotion researchers (Russell, 2003; Barrett, Chapter 11). In core affect theory, as noted earlier, these various factors are used to catego- rize the emotion perceptually based on the extent of resemblance between these factors and a mental representation of a given emotion’s prototype.

How does the core affect model fit with the dual-process framework? Quite well. We assume that the changes in core affect caused by some external events may be hardwired (e.g., fear at the visual appearance of great height) or learned from previous encounters (e.g., fear at the sight or smell of a fire). Other reactions closely linked to core affect (such as expres- sive nonverbal behaviors or increases in physiological action readiness) may also occur automatically. Automatic responses take place within the associative processing mode, without any necessary participation by rule- based or reflective processing (Barrett, Chapter 11). Notably, these pro- cesses can occur in nonhuman species as well. The identification of a cause may also often be automatic and associative: The sight of a snake triggers both the affective reaction and the recollection of previous encounters with frightening snakes.

Other processes within the core affect model invoke the type of sym- bolic/propositional reasoning that is a uniquely human power. Sometimes this is the case for causal identification. Identifying the cause may require an effortful, intentional search, and occasionally misattributions are made. A person may come home and snap at his or her spouse, not realizing that the true cause of the annoyed feelings is an abrasive encounter with a coworker that occurred earlier in the day. Similarly, Neumann, Seibt, and Strack (2001) showed that positive feedback about one’s performance in an intelligence test leads to stronger feelings of pride if a positive rather than a negative mood state was unobtrusively induced previously. Apparently, participants in a positive mood identified the positive feedback as the source of their feeling state, although their feelings stemmed, in part, from the prior mood induction. Thus, whenever feelings are induced in quick

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succession, which might be common in everyday life, much more effort is needed to identify with precision the contribution of each emotion-eliciting event.

Sometimes reflective processing can help people identify the true cause of the emotion in such cases. And “emotional meta-experience,” the categorical knowledge that one is experiencing a discrete emotion (e.g., annoyance, guilt, anxiety), is clearly in the province of reflective thought (for an alternative view, see the section on “Functional Modularity of Emo- tion” in Barrett, Tugade, & Engle, 2004). Moreover, core affect can be input to reflective processing and thereby form the basis for conscious decisions—in effect, affective states can inform the individual about signifi- cant events (Keltner & Haidt, 1999; Schwarz & Clore, 1983). Reflective processing about one’s emotions can also lead to meta-emotions, such as shame at feeling angry.

These linkages to dual-process thinking yield testable predictions. Dual-process models in other areas of social psychology have often been tested by manipulating cognitive load or distraction, which is believed to selectively impair rule-based processing while having little impact on asso- ciative processing (see Barrett et al., 2004). In the area of emotional pro- cesses, cognitive load or distraction ought to make it more difficult for peo- ple to identify which emotion they are experiencing (meta-experience), even though it should not greatly reduce the core affect changes. Load or distraction also should interfere with people’s ability to accurately identify the cause of the emotion, at least in cases where it is not overwhelmingly obvious. Tentative support for this assumption comes from a study by Siemer and Reisenzein (1998). Consistent with the mood-as-information approach (Schwarz & Clore, 1983), in this study moods were more likely to affect subsequent judgments when participants were under time pressure or when their processing capacity was reduced by a secondary task. This study suggests that cognitive load indeed interferes with the ability to iden- tify the cause of a core affect state, making it more likely for the affect to be misattributed to irrelevant sources. Importantly, however, and consistent with our predictions, the core affect state itself (the mood state) was not influenced by the secondary task. However, further research is needed to explore whether reduced processing capacity exerts similar influences on the ability to identify the causes of emotions.

IMPLICATIONS

Several interesting implications arise from the distinction between the associative and rule-based or reflective processes that underlie emotions.

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Modes of Emotion Regulation

Whereas emotions that are due to reflective processes might be changed by a reconsideration or reappraisal of the situation, emotions that are due to associative processes are likely to change only if the stimulus input is interrupted—because they are more or less automatically activated by per- ception of the stimulus. This proposition has implications for emotion con- trol. In order to avoid perceptual input that elicits fear, people might try to avoid the whole situation or shut their eyes (as a child might do at a scary part of a movie). On the other hand, distraction might be appropriate to control, for example, fear of public speaking.

Selective Effects of Misattribution

The core affect model leaves open the possibility of misattribution (i.e., being mistaken about the cause of an emotion) and also of misidentifying the specific emotion that one is experiencing. This aspect of the model reflects the well-known idea that people have access to their experiences but not to the causes and processes underlying these experiences (Nisbett & Wilson, 1977). Especially if distinct emotions are evoked in quick succes- sion, it is likely that affective responses may carry over from one event to the next, making it more difficult to identify the correct causes of one’s emotion. Research has shown that, in principle, people are able to correct judgments about their emotion (Neumann et al., 2001). However, despite efforts to correct for unwanted influences (e.g., persuading oneself that the current feeling of anger is not due to the remark of one’s partner but rather to a prior frustration), behavioral responses such as facial expression never- theless reflect these influences (e.g., more frowning toward the partner). The facial component of an emotion may be more influenced by associative processing and less by conscious (rule-based) control (Neumann et al., 2001). In other words, although one can make efforts to find out the correct cause of all emotion, one’s feelings and facial expression might nevertheless reflect the influence of prior events.

Dissociations from Cognitive Beliefs

Dissociations can occur when the associative system produces a specific emotion that the reflective system views as inappropriate. As Sloman (1996) emphasized in his discussion of dual-process models, perceptual illusions such as the Müller–Lyer illusion persist and are subjectively compelling even though one explicitly knows they are false in appearance (e.g., the arrows are the same length). Blascovich (personal communication, August, 2002) reports that people often are afraid to walk over a “pit” they can see

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in virtual reality goggles, even though they know they are on a safe, stable floor. Russell (2003) captured this same type of dissociation in his “virtual reality” principle, which says that people will experience emotions in response to fictional accounts, movie portrayals, etc., even if they know that the depicted events are untrue. This is an interesting finding, given that some emotion researchers (Frijda, 1988; Ortony, Clore, & Collins, 1988) argue that the object of an emotion needs to be construed as real before it can elicit emotional responses. No doubt, knowing that the object of one’s emotion is real can intensify emotional responses, and the belief that the object is not real dampens emotional responses (Gross, 1998; Lazarus & Alfert, 1964). We suggest, however, that this pattern should be true only to the extent that the emotion is evoked by reflective process. Knowing that a pit that visually appears before one’s feet is unreal should have little impact on the affective response, assuming that it is generated by associative pro- cesses.

Dissociations Due to Input Stimuli

The associative and rule-based systems are most effectively activated by different types of input. Associative processes can be most directly acti- vated by visual or other actual sensory inputs (e.g., the sight of a charging bear) (see Lundqvist & Öhman, Chapter 5; de Gelder, Chapter 6; Atkinson & Adolphs, Chapter 7). Rule-based processes, with their heavy linguistic component, are directly activated by symbolic input (e.g., reading “The bear charges at you”). This point has many implications (see Lieberman et al., 2002). One is methodological: Researchers often use verbal or symbolic stimuli for their convenience, but should understand that results may not be equivalent to those resulting from images, movies, etc. Nevertheless it is obvious that people can respond emotionally to words. How does this response occur? One potential route is that people can transform symbolic stimuli into vivid images that, in turn, trigger emotion through associative processing. Consistent with this suggestion, Lang (1977) has shown that good imagers are more likely to respond affectively to degraded input (short phrases) than poor imagers. In short, the experiential quality of the internal representation influences whether the associative mode of process- ing is activated (see also Niedenthal, Barsalou, Ric, & Krauth-Gruber, Chapter 2, for a related view).

Implications of Emotions for Dual-Process Theories

We have been discussing implications of dual-process thinking for under- standing processes relevant to emotion, but emotions also have implica- tions for dual-process models. As Lieberman et al. (2002) explain, one func-

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tion of negative emotions is as an alarm or wake-up call for the reflective system, indicating that more automatic (associative mode) regulatory pro- cesses have failed. Berkowitz (1993) demonstrates that negative affect can be automatically elicited by a variety of different factors (e.g., heat, foul odors, loud noises). The evoked negative feeling might, in turn, activate the reflective system to understand whether and why the individual’s goals are blocked. If the resulting causal search identifies another person’s actions as the source of the negative situation, subjectively experienced anger may result. Accordingly, ruminative thoughts might be able to transform a mild shudder into a full-blown panic attack (Bouton, Chapter 9; Martin & Tesser, 1989). Thus the two processing modes can have parallel effects in emo- tional responses.

Attributions for Emotional Responses

We advance one more speculative suggestion concerning the way in which emotional reactions are subjectively experienced. Processing in the associa- tive mode is automatic and preconscious, becoming subjectively part of the experience of the perceived object itself, as Lieberman et al. (2002) empha- size. For this reason, emotions based on the associative processing system may be seen as intrinsic to the object itself: The fire or the storm cloud is experienced as inherently frightening (for a similar point, see Barrett, Chapter 11). In contrast, responses generated by rule-based or reflective processes are subjectively experienced as one’s own thoughts or reactions to events (Lieberman et al., 2002) rather than as inherent in the object. We may say “I feel upset” or “I feel guilty,” attributing the emotional response to ourselves, rather than assuming that the emotion is inherent in the object and that everyone else would feel the same in the same situation. Still, the determinants of the outward or inward “focus” of emotions are multiple and complex (see Lambie & Marcel, 2002), and this hypothesis based on the properties of dual-processing modes is speculative and requires further elaboration and empirical test.

CONCLUSIONS

Dual-process approaches have become common in many topic areas across social and cognitive psychology (Smith & DeCoster, 2000). In this chapter we have attempted to sketch the outlines of a dual-process approach to pro- cesses involved in the elicitation and control of emotion, and to review some of the implications of such a model. In general, we believe that this integrative theoretical effort makes good sense. Our dual-process approach

Emotion and Dual-Process Models 307

makes sense of facts such as the following: (1) some affective responses are evidently shared by nonhumans, whereas others rest on types of verbal/ propositional reasoning that are more uniquely human; (2) some emotions are easily altered by changing high-order knowledge or beliefs, whereas others are recalcitrant and cannot be changed by beliefs (e.g., disgust felt at a disgusting-looking object that one knows is a wholesome food); (3) emo- tions can be misattributed (linked to an incorrect cause) and misidentified (given an incorrect label), suggesting that the more automatic processes that generate the emotion are distinct from the more thoughtful processes involved in causal search and emotion labeling; (4) sometimes emotions are generated by preconscious processes, so that we are conscious only of a sudden onset of affect, and sometimes by conscious processes, in which we are aware of each step in a chain of reasoning that leads us to an emotion- ally evocative conclusion. The success and empirical fruitfulness of dual- process thinking in other domains suggest that as this approach to emotion processes is carried further, it may well lead to important conceptual and empirical insights.

NOTES

1. A connectionist network is a large number of simple yet richly interconnected processing units (loosely analogous to neurons), in which a flow of signals across the connections allows the network to perform the basic functions of informa- tion transformation and representation. Each experience leads to small changes in the strengths of the connections between units. The result of many such changes is that the network becomes able to reconstruct patterns that it had previously generated in response to similar patterns of inputs.

2. Recent research suggests that it is not the movement direction that is associated with the processing of valence but rather the increase (withdrawal) or decrease (approach) of distance between the self and an object (Neumann, Seibt, & Levy-Sadot, 2004). Thus, if the reference point of a movement is the self, push- ing a lever away is executed faster (increasing the distance to the self). However, if the reference point is the object, moving the hand away from the object is executed faster (increasing the distance to the object).

3. From that point of view it might not be surprising that the timing of facial responses seems to be a critical variable in lie detection (Ekman, 1986).

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TUHncEonCsOciNouSsCPIrOocUeSss–eUsNinCEOmNoStiCoInOUS DEBATE

CHAPTER 13

Unconscious Processes in Emotion

The Bulk of the Iceberg

KLAUS R. SCHERER

This chapter reviews some of the central emotion processes and the respec- tive role of consciousness (or its absence). Contrary to what seems to be current practice, I attempt to refrain from classifying phenomena into con- scious and unconscious, which implies a divide between two separate cate- gories. Rather, I assume that a large majority of emotion processes func- tions in an unconscious mode and that only some of these processes (or their outcomes) will emerge into consciousness for some periods of time. I like Freud’s metaphor of an iceberg, the bulk of which is invisible (the unconscious) with only a small tip above the surface (the conscious). If we assume that the fluid in which the emotion iceberg floats (the mental soup) can vary in consistency, buoyancy will determine the degree of emergence (the buoyant force is equal to the weight of the liquid that the object dis- places. If the liquid is denser, the buoyant force is greater. Steel sinks in water but floats in mercury). Similarly, increases in density of mental pro- cessing may result in a greater emergence of processing into consciousness.

The major purpose of this chapter is to analyze theoretically the con- scious and unconscious processes in emotion elicitation and differentiation. Specific research is cited as illustration, but no coherent, let alone exhaus- tive, review is intended. To identify contrasting positions and to stimulate

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Unconscious Processes in Emotion 313

1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

In this chapter, I present a comprehensive component process model of emo- tion that defines emotion as an episode of interrelated, synchronized changes in the states of all or most of five organismic subsystems (cognition, neurophysiological support, motivation, motor expression, subjective feeling)
in response to the evaluation of an external or internal stimulus event as rele- vant to major concerns of the organism. Emotion-constituent evaluation is described as recursive sequences of appraisal at several levels of processing (sensory–motor, schematic, conceptual) based on a set of universal criteria. This account allows for an almost unlimited number of differentiated emotional qual- ities to emerge, depending on the respective appraisal profile and sequence (for further details, see Scherer, 2001a, 2004a). Verbal labels such as fear, joy, or anger are seen as language-based categories for modal emotions, i.e., frequently and universally occurring events and situations that generate similar appraisal profiles (Scherer, 1994).

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

It would be inappropriate to attempt to define “consciousness,” given the extraordinary multiplicity of definitions currently in existence. Thus, a generic core of understanding of consciousness and unconsciousness is presupposed. However, I suggest separating these notions from assumptions made about the nature of cognitive processing, such as automatic, effortful, or implicit.

3. Does your theory model with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

Importantly, it is assumed that a large majority of emotion processes function in an unconscious mode and that only some of these processes (or their outcomes) will emerge into consciousness for some periods of time. This process is seen as linked to the degree of synchronization between organismic subsystems pro- duced by emotion elicitation and the attention generated by a monitoring system. A process whereby parts of an integrated representation of the underly- ing component processes emerge into consciousness, as a prerequisite for verbal labeling and communication, is suggested and illustrated in this chapter (see Scherer, 2004a, for further details).

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debate, some issues are presented in an exaggerated fashion. Most impor- tant, the spirit in which the chapter is written is exploratory, as is appropri- ate for the vast and largely uncharted territory of the conscious and the unconscious in emotion.

Given the rampant terminological confusion in the area of emotion theorizing and research, it may be useful to start with a definition of emo- tion. I have suggested seven different types of affective states in the form of a design feature analysis (see Figure 13.1), with examples of each: Preferences, utilitarian emotions, aesthetic emotions, mood, interpersonal stances, attitudes, and affective personality traits. These different con- structs are compared on the basis of a set of design features (see Scherer, 2004b) that includes (1) typical intensity, (2) duration, (3) the degree of syn- chronization or coordination of different organismic systems during the state, (4) the extent to which the change in state is triggered by, or focused on, an event or a situation, (5 and 6) the extent to which the differentiated nature of the state is due to a process of antecedent appraisal or evaluation (either intrinsic, i.e., determined by the object, or transactional, i.e., deter- mined by the object in interaction with the needs/goals of the appraiser), (7) the rapidity of change in the nature of the state, (8) the degree to which the state affects behavior, and (9) the relative importance for emotion induction via art or music. Specifically, emotion is defined as an episode of massive, synchronous recruitment of mental and somatic resources to adapt to, or cope with, a stimulus event that is subjectively appraised as being highly pertinent to the needs, goals, and values of the individual.

In this chapter, I focus on three major processes directly determined by the reactive nature of emotion that commonly occur during an emotion episode: (1) the detection and evaluation of the significance of a stimulus event for the individual; (2) the preparation of response tendencies; and (3) the integration of evaluative and proprioceptive information, resulting in subjective feeling states. A number of issues pertinent to consciousness and elaboration is explored for each of these processes. Researchers working on unconscious phenomena in affect and emotion have their preferred terms to distinguish conscious and unconscious processes in a larger sense. This is not the place for a detailed historical overview and assignment of respon- sibility for the definition and use of certain terms via conscientious citation. Even a cursory overview of the literature in this domain (Bargh, 1994; Bargh & Ferguson, 2000; Cohen & Schooler, 1997; Fazio, 2001; Greenwald & Banaji, 1995; Hameroff, Kaszniak, & Scott, 1996; Kihlstrom, 1994; Lambie & Marcel, 2002; Leventhal, 1984; Shallice, 1972; Schneider & Shiffrin, 1977) suggests a number of adjectival pairs, in addition to con- scious and unconscious, that are regularly used: explicit versus implicit, controlled versus automatic, effortful versus effortless, and conceptual/

                

315

Intensity Duration

Synchronization

Event/situation focus

Intrinsic appraisal

Transactional appraisal

Rapidity of change

Behavioral impact

Induction
via art/music

Type of affective state: brief definition (examples)

Preferences: evaluative judgments of stimuli in the sense of liking or disliking, or preferring or not, over another stimulus (like, dislike, positive, negative)

L M H L

VL VH VH M VL VH VH M VH VH

MH VH H

Utilitarian emotions: relatively brief episodes of synchronized response of all or most organismic subsystems to the evaluation of an external or internal event as being of major significance for personal goals and needs (angry, sad, joyful, fearful, ashamed, proud, elated, desperate)

Aesthetic emotions: evaluations of auditory or visual stimuli in terms of intrinsic qualities of form or relationship of elements (moved, awed, surprised, full of wonder, admiration, bliss, ecstasy, fascination, harmony, rapture, solemnity)

L–M L

M H VH L VH

L VH

Mood: diffuse affect state, most pronounced as change in subjective feeling, of low intensity but relatively long duration, often without apparent cause (cheerful, gloomy, irritable, listless, depressed, buoyant)

M H

LLMLH

H M

Interpersonal stances: affective stance taken toward another person in a specific interaction, coloring the interpersonal exchange in that situation (distant, cold, warm, supportive, contemptuous)

M M

L H L L VH

H L

Attitudes: relatively enduring, affectively colored beliefs and predispositions toward objects or persons (loving, hating, valuing, desiring)

M H L VH

VL VL L L L VL VL L VL VL

L M L L

Personality traits: emotionally laden, stable personality dispositions and behavior tendencies, typical for a person (nervous, anxious, reckless, morose, hostile, envious, jealous)

Design feature

FIGURE 13.1. Design feature definitions for major types of affect. VL, very low; L, low; M, medium; H, high; LH, very high. From Scherer (2004b). Copyright 2004 by the Journal of New Music Research (www.tandf.co.uk). Reprinted by permission.

316 THE CONSCIOUS–UNCONSCIOUS DEBATE

propositional versus schematic. Although individual authors may make sharper distinctions, there is a common tendency to assume a high degree of overlap between unconscious, implicit, automatic, effortless, and sche- matic, on the one hand, and conscious, explicit, controlled, effortful, and conceptual/propositional, on the other. In addition, there is a tendency to view these pairs as binary, dichotomous alternatives rather than as opposite poles on an underlying dimension. Both of these assumptions seem to require more extensive debate (see also Clore & Ketelaar, 1997).

To what extent are these modalities interrelated? It is likely that there is a high degree of empirical covariation between some of the modalities. But these relationships are probably much too complex to justify treating the terms unconscious, implicit, automatic, and effortless as synonyms. For example, on the one hand, an automatically triggered reflex may require lit- tle effort and could remain opaque to consciousness unless it is externalized as overt behavior, as in the case of the knee jerk. On the other hand, reflexes should, by definition, be explicit. Implicit processes should be effortful because they require a lot of inference to determine the behavioral meaning. If attention is one of the required resources, it is unlikely that the process will be automatic and remain entirely unconscious. The lack of appropriate conceptual distinctions may actually hinder the careful analysis of the precise nature of the processes involved in the emotion mechanism. Thus the modalities or dimensions discussed earlier should be treated as independent, continuous dimensions in a multidimensional space. In con- sequence, the processes under study in a particular research project should be qualified, at least roughly, with respect to their position on each of these dimensions separately. Although difficult and necessarily speculative, such an approach could produce interesting insights into the nature of the men- tal processes that underlie emotion. It would certainly force us to be more precise in the conceptualizations and potentially even in the operation- alizations used in this research.

THE DETECTION AND EVALUATION
OF THE SIGNIFICANCE AND IMPLICATIONS OF A STIMULUS EVENT FOR THE INDIVIDUAL

The presence of an emotion is an indicator that the individual has detected an event that is likely to have significant consequences for his or her needs, goals, and values. The reason that we can be confident of this statement is that the principle of economy underlying much of evolution would not per- mit an important investment of resources, as constituted by a massive, syn- chronized response across several organismic systems, unless there were a

Unconscious Processes in Emotion 317

real need for adaptation. The better we understand the process of signifi- cance detection and evaluation, the better we understand emotion. The sig- nificance of a stimulus event resides in its meaning, and its meaning, in its behavioral (as compared with semantic) sense, is defined by potential con- sequences for the individual’s needs, goals, and values. There seem to be two major mechanisms for meaning assignment: pattern matching and rule- based inference (see also Smith & Neumann, Chapter 12).

It is generally assumed that, from an individual’s past experience, the matched schemas or the inferences from specific features will produce a certain type of behavioral meaning. For example, if one has had negative experiences with doctors, a negative attitude may be activated each time one sees a man in a white coat, independent of the context. However, in many cases, the current context, and particularly the current motivational state of the person, contributes massively to the emergence of the behavior- al meaning of an event (and the consequent emotional reaction). In other words, behavioral meaning is, in large part, constituted by an individual’s assessment of the probable consequences of a particular stimulus event occurring at a particular time, and this assessment is determined by the individual’s motivational state, available resources, and the respective socionormative context. This point is so important that it bears restating: Although some of the behavioral meaning of a schema or an inference is stored in memory in the form of association with other memory and knowl- edge content as well as past affective reactions, much of the behavioral meaning in a particular situation is determined by an interaction between these stored meaning components and their evaluation in the light of the cur- rent motivational state and available resources for outcome control.

To my knowledge, until recently (see Ekman, 2004), neither basic emotion theorists nor dimensional theorists have been centrally concerned with the nature of the processes that detect pertinent events, evaluate their consequences and meaning for the individual, and thus differentiate the resulting emotions and their behavioral effects (Scherer, 2000b). In con- trast, this evaluation is the major focus of interest in componential appraisal theories of emotion (see Ellsworth & Scherer, 2003; Scherer, 1999; Scherer, Schorr, & Johnstone, 2001, for overviews), which attempt to conceptualize the behavioral meaning of an event for the individual (and thus the result- ing emotion) on the basis of profiles of evaluation criteria such as novelty, agreeableness, goal conduciveness, coping potential, and norm compatibil- ity (see Scherer, 2001a). For example, appraisal theorists might describe the behavioral meaning of an event, such as being threatened by a mugger, as novel, disagreeable, goal obstructive, difficult to cope with, and immoral. The predicted emotion would be a variant of a fear–anger blend. Impor- tantly, appraisal theorists consider the evaluation and the resulting emotion

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as a continuous and constantly changing process. The variability is due to situational changes as well as to reappraisals of the consequences. Further- more, the motivational state of the individual as well as his or her resource supply are likely to change, sometimes rather abruptly. In consequence, behavioral meaning must be an emergent quality, subject to constant and often sudden change.

In consequence, all stimulation impinging on the organism must be constantly monitored for dynamic behavioral meaning. This meaning is emergent, based on an interaction between the nature of the event, its con- sequences, and the individual’s motivational state. Given the complexity and changeability of the factors involved, it is unlikely that behavioral meaning can be constituted simply by matching situational features with schemas stored in long-term memory. The only exception might be power- ful stimuli that have an unconditional impact, such as evolutionary threat, or other unconditioned stimuli that represent powerful aversive (pain) or appetitive (food, sex) functions. Yet even these might be mediated by moti- vational states. Thus it seems that pain sensitivity is mediated by both dispositional and state differences (Coderre, Mogil, & Bushnell, 2003).

In general, the ongoing evaluation of most day-to-day stimulus events will require comparative evaluation of an event with the current motiva- tional and resource state. These operations go far beyond simple feature detection or even schema matching and are thus likely to be effortful. How- ever, they must be largely automatic, given that they operate almost con- stantly. It would hardly be feasible to imagine a higher-order monitoring system controlling this process in any depth. For the same reason, much of this process is likely to operate outside of consciousness, because the attentional resources mobilized by conscious processing could not be invested in a continuous fashion. Because the significance-evaluation mechanism is on all the time, one might expect a shallow filter to operate to screen incoming stimulation for significant consequences, on the basis of a particular tuning or setting of the organism’s motivational state. Only stim- uli that are not filtered out as inconsequential will elicit deeper processing.

How does this process work? The enormous amount of research on the amygdala that has been stimulated by the pioneering work of LeDoux (2000) and Davis (1998; Davis & Whalen, 2001) suggests some beginning answers. There is much evidence to suggest that direct projections from the sensory thalamus to the amygdala serve to activate rudimentary defense reactions to powerful threats such as evolutionarily prepared stimuli (e.g., snakes, facial anger expression) or conditioned stimuli based on painful unconditioned stimuli (Lunsqvist & Öhman, Chapter 5; de Gelder, Chapter 6; Atkins & Adolphs, Chapter 7; Dolan & Morris, 2000; Vuilleumier, Armony, Driver, & Dolan, 2001; Vuilleumier & Schwartz, 2001; Whalen,

Unconscious Processes in Emotion 319

1998; Whalen, Curran, & Rauch, 2001; Whalen, Shin, et al., 2001). From this evidence, there is reason to believe that the amygdala plays an impor- tant role in the filtering process referred to earlier. This role is all the more probable because, contrary to popular opinion, the amygdala does not seem to be exclusively focused on the recognition of threat- or fear-relevant stim- ulation. In a careful review of the literature, Sander, Grafman, and Zalla (2003) have accumulated evidence that suggests that the amygdala is a gen- eralized device for the low-level detection of significance or pertinence in a general sense. In other words, the amygdala seems capable of deciding, on the basis of rather rudimentary information conveyed directly from the sen- sory thalamus, that a particular stimulus is potentially significant for the needs and the well-being of an organism. The baffling question is, of course, how the amygdala does it. Could it be that a certain number of per- tinent schemas, “the most significant of . . . , ” are stored in this subcortical structure, and if so, in which form? Or does the amygdala, which is highly connected to most subcortical and cortical regions, rely on schemas stored in a distributed fashion? Is the inventory of the schemas that reflects vital behavioral meaning the same for every individual, that is, genetically deter- mined by evolutionary preparation? Or does the experience and the moti- vational makeup of the individual influence the target patterns stored in this central gatekeeper structure? Does the information processing that takes place in the amygdala take into account the current motivational and resource state of the organism, implying some kind of comparison, or at least tuning, or is it limited to matching the input features to invariant schemas? The research agenda for affective neuroscientists specializing on the amygdala should keep the discipline busy for some time.

Most important, despite the fascinating demonstration of the existence of a “low road” (direct thalamo–amygdala projections) and a “high road” (via the cortical association areas) of information processing by LeDoux and others, one should not forget that the process is generally integrated. Acti- vation triggered by external stimulation speeds along both roads, and although the more rapid lower road may start producing some generalized autononous nervous system (ANS) efference after 80 milliseconds of stimu- lus onset, travel on the high road is not far behind, and the first results of cortical processing will arrive at the amygdala 50–100 milliseconds later. Thus it cannot be a question of either/or but rather of how processing along the two routes is integrated and coordinated. One can assume that this inte- gration and coordination can take many different forms, ranging from pre- dominance of the lower road, with only minor involvement of the higher level (as in the case of stimulation to which satisfactory adjustment can be made on the basis of low-level regulation), to almost exclusive involvement of the cortical level (as in the case of logical deductions in a philosophy

320 THE CONSCIOUS–UNCONSCIOUS DEBATE

seminar). In addition, it is not only the level but also the quality of process- ing that is at stake. Is simple schema matching sufficient or are inference and comparison required? Is the process highly routinized and able to unfold automatically or is an active, effortful, and controlled search required? How many tasks have to be dealt with at the same time and how much attention is available for each? As suggested earlier, we can expect that the quality of the respective evaluation process must be described as a trajectory through a multidimensional space formed by the dimensions of effort, automaticity, explicitness, and consciousness. Leventhal and Scherer (1987) have suggested that the type of processing with regard to content (types of appraisal) and level (sensory–motor, schematic, and conceptual) is determined by the need to arrive at a conclusive evaluation result (yielding a promising action tendency). If automatic, effortless, unconscious pro- cesses do not produce a satisfactory result, more controlled, effortful, and possibly conscious mechanisms are brought into play to determine the behavioral meaning of a stimulus event and prepare an adaptive response.

THE PREPARATION OF RESPONSE TENDENCIES

The function of emotion is to prepare adaptive behavioral reactions. In con- sequence, one of the most important processes is the preparation of appro- priate action tendencies. The conceptualization of this essential set of processes varies considerably over the three theoretical traditions. Dimen- sional theorists, in line with their emphasis on valence, mostly discuss the preparation of approach or avoidance tendencies (Carver, 2001). Discrete or basic emotion theorists assume highly integrated response patterns for each of the basic emotions, particularly with regard to motor expression and physiological response specificity (Ekman, 1972; Izard, 1971). In con- trast, many appraisal theorists postulate that response preparation depends directly on the results of the appraisal process (Roseman, 2001; Scherer, 1984, 2001a; Smith & Scott, 1997). I have postulated that each significant result on an appraisal dimension triggers a response in all components of emotion and that these sequential changes are cumulatively integrated. Each result of a particular check in the cognitive component is expected to affect every other component of the emotion process (even though the effect may be slight in many cases). The effects of subsequent checks cumu- latively add to the pattern of change (see Scherer, 2001a, Fig. 2). Given the theoretical prediction of a fixed but recursive, sequence and of detailed response characteristics in different peripheral domains (e.g., motor ex- pression and physiological responding), these claims can be empirically investigated (for a discussion, see Barrett, Chapter 11). This is particularly

Unconscious Processes in Emotion 321

interesting with regard to the temporal unfolding of these processes, for which there is currently little evidence in the literature. Electroencephalo- graphic work in progress in our lab (Grandjean & Scherer, 2003) provides the first evidence for the assumption that the checks underlying the appraisal process are not simultaneous but occur sequentially, as predicted. For example, the cerebral processes at the cortical level related to the experimental manipulation of novelty, investigated with electroencepha- lographic methods, seem to occur earlier than the processes related to the relevance appraisal.

THE INTEGRATION OF EVALUATIVE
AND PROPRIOCEPTIVE INFORMATION AND THE EMERGENCE OF SUBJECTIVE FEELING STATES

As suggested earlier, an emotion episode essentially consists of synchro- nized processes of event evaluation and response preparation involving several components. Each of these processes can be expected to have its own projections and proprioceptive feedback loops, allowing for rudimen- tary, largely automatic regulation. However, if these processes are to be controlled and regulated at a higher level, the information needs to be cen- trally represented and, at least in part, to emerge into consciousness. The reason is that the complete process of central evaluation and peripheral responses is unlikely to be centrally stored over an extended period of time, both because of capacity limitations and the need for meaning analysis on a macro level that can guide control and regulation efforts. In consequence, we need to model the process that underlies the emergence of integrated representations of central processing and proprioceptive feedback into con- sciousness.

Figure 13.2 illustrates these notions. A Venn diagram with a set of overlapping circles represents the different aspects of monitoring (see also Kaiser & Scherer, 1997; Scherer, 1994). The first circle (A) represents the raw reflection or representation of changes in all synchronized compo- nents in a monitoring structure in the central nervous system, integrat- ing the representation of central processing and somatosensory feedback (Iwamura, 1998). This structure is expected to receive massive projections from both cortical and subcortical central nervous system (CNS) structures (including proprioceptive feedback from the periphery). Even though this representation will only become partly conscious, the information repre- sented here is of central importance for response preparation (and thus behavioral adaptation), learning, and rudimentary coping and regulation. One might call the content of the circle integrated process representation.

322 THE CONSCIOUS–UNCONSCIOUS DEBATE

FIGURE13.2. Threemodesoftherepresentationofchangesinemotioncompo- nents: unconsciousness, consciousness, and verbalzation.

The second circle (B), only partially overlapping with the first, repre- sents that part of the integrated process representation that enters aware- ness (possibly when a high degree of component synchronization requires a high level of controlled regulation and social communication) and thereby becomes conscious. This circle represents the quality and intensity of the conscious feeling state generated by the eliciting event. It would seem that the content of this circle is close to what philosophers and psychologists have referred to as qualia.

The third circle in Figure 13.2 represents the individual’s ability (which may or may not be realized) to verbally report the subjective experi- ence during the emotion episode and thus share it with significant others (including emotion researchers). The fact that this verbalization circle over- laps only partially with the conscious feeling circle is meant to suggest that we can verbalize only a small part of our conscious experience, as a result of (1) the limited availability of appropriate verbal categories (in a particular language and/or to a particular individual), and (2) the individual’s inten- tions to control or hide some of his or her innermost feelings. Most impor- tant, the constant flow of consciousness cannot be completely described by a discrete utterance. Thus verbal report must, by necessity, be an approxi-

Unconscious Processes in Emotion 323

mation that identifies the most salient elements of the experience in the form of a state definition that uses concepts provided by the emotion- related semantic concepts in a language (for a more complete description of the Venn diagram, see Scherer, 2004a; for an alternative view, see Barrett, Chapter 11).

Admittedly, this schema does not do much to advance our understand- ing of the processes involved, but it may help us ask appropriate research questions concerning (1) the nature of the integration of information from different modalities into a coherent representation, (2) the conditions for emergence of this representation into consciousness, and (3) the encoding of conscious representations into verbal statements.

The central projections from both the cognitive processing and the motor and physiological responding need to be integrated within each domain, across the different domains, and over time. I believe that these extremely complex dynamic integration processes have been severely neglected by past work on emotion. They constitute a major challenge for investigators in this area, because the processes of integration are likely to be largely unconscious but result in a holistic, phenomenal experience or feeling that is at least, in part, conscious. In what follows, I briefly sketch the integration processes that seem to be required: (1) the integration of appraisal results, (2) the integration of peripheral component effects, and (3) integration across components and time.

Integration of Appraisal Results

In trying to predict the emotions resulting from different patterns of appraisal, theorists in this tradition have generally used profile matching or regression analysis (for a review, see Scherer, 1999) without paying too much attention to the problem of the integration of the appraisal results with regard to both the different evaluation criteria or dimensions and the changes over time. In my own model, I have proposed a recursive sequence of stimulus evaluation checks, with an accumulation of the expected efferent effects (see Scherer, 2001a, Figure 2). What remains to be done is to specify the nature of the integration functions that must underlie these cumulative processes. I have suggested attacking this issue by start- ing from a suggestion made by Anderson (1989), who postulates different types of integration functions based on the current goals of the organism, which transform subjective appraisal results into an implicit response (see Scherer, 2004a). It would be a major breakthrough to be able to model information integration in appraisal and to predict integration rules for combinations of specific appraisal criteria. For example, we found empiri- cally (van Reekum et al., 2004) that the perceived coping potential has a dif-

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ferent effect on psychophysiological responses as a function of goal condu- civeness. As one might expect, coping ability is of less relevance and has less of an impact on the ANS when things are going according to plan. In Anderson’s approach, this pattern would be modeled by a configuration rule, which predicts that the importance of one of the criteria depends on the level of another.

To what extent are these processes available to consciousness? Ap- praisal theorists are often chided for relying on verbal report in order to study event evaluation (Parkinson, 1997). The argument is that, given the rapidity and complexity of the underlying inference processes, individuals are unlikely to have access to the inner workings of the process. This is quite likely. However, it does not rule out that the individual is aware of the outcome of the inference process, for example, the realization of being faced with a goal obstruction that he or she is powerless to remove. This issue is related, of course, to the even more complex issue of what the objects of consciousness are. It is unlikely that the results of evaluations on individual appraisal dimensions enter awareness directly, in raw form, so to speak, because it is probably the interaction between different dimensions that is central rather than the nature of the individual ingredients. Despite this complexity, we may need to be more specific about these objects if we want to advance our understanding of the nature of emotion-antecedent evaluation processes. In order to address these issues in research, we obvi- ously need to rely on self-report (heeding the problems of incomplete over- lap of circles B and C in the schema described earlier). However, if we want to get at the integrated representation of the appraisal results, we may need to change our instruments and procedures, which, so far, have focused on individual appraisal dimensions.

Integration of Peripheral Component Effects

Proprioceptive feedback information is available from different response components such as vocal and facial expression or psychophysiological symptoms. The question of how different patterns of feedback from the so- matic nervous system (SNS) and the ANS are integrated and when they enter consciousness has not been extensively studied to date. One possibil- ity is that integration is, in part, predetermined by major functional circuits that underlie peripheral responding. For example, in Gellhorn’s (1964) the- ory of ergotropic and trophotropic systems (or the more general notion of sympathetic and parasympathetic systems), individual responses are syn- chronized by the activation of the superordinate systems. One could assume that feedback integration reassembles those functional interrela- tionships. Although such a form of autoorganization might be a feasible

Unconscious Processes in Emotion 325

mechanism for ANS integration (albeit there is increasing doubt as to the unity of such large-scale systems), such a mechanism is unlikely to be oper- ative in somatic integration, in particular, facial expression and action- related movement. In the case of adaptive behavior, the underlying deter- minant, and possibly the focus of integration, may be some form of motiva- tional urge, such as an action tendency (Frijda, 1986). In the case of facial expression, there is much debate between theorists who suggest that the face expresses basic emotions (Ekman, 1972; Izard, 1971), a “social message” point of view (Fridlund, 1994; see also Owren, Rendall, & Bachorowski, Chapter 8), and appraisal theorists, who suggest that ele- ments of facial expression might be directly triggered by the results of eval- uation on particular combinations of appraisal dimensions (Scherer, 1992; Smith & Scott, 1997). Each of these assumed functions seems to imply a different type of integration process.

How do these processes enter awareness? Although we know that interoception, that is, the conscious proprioceptive representation of inter- nal physiological changes, does not accurately reflect the physiological parameters (Barrett, Chapter 11; Vaitl, 1996), there might be more precise nonconscious representations that provide input to the process of integrat- ing the various response domains in the ANS and SNS. In other words, raw proprioceptive feedback from peripheral physiological responses may not project directly to brain structures that underlie the emergence of con- sciousness but, rather, may contribute to a representation that integrates the changes in several response components. This integrated representa- tion, in turn, may then reach consciousness without allowing the specifica- tion of details for individual classes of responses.

One of the problems with studies of interoception (or, for that matter, of emotion-specific physiological response patterns, in general) is that, to the best of my knowledge, not a single study has studied interoception dur- ing serious emotional upheavals, such as trying to flee from a terrorist bomb attack, being enraged by an unbearable insult, or experiencing extreme joy in seeing one’s baby. Much of the experimental research, to date, has induced mild emotional states, if any, and it is not surprising that people are not good at verbally indexing subtle variations in physiological parameters. Nor is it surprising that it is difficult to find emotion-specific patterns in physiological responding if no specific emotions have been induced. Thus the issue remains open until more representative emotional states with higher specificity and higher intensity have been studied (if this will ever be possible). From the standpoint of evolutionary architecture, it seems functional that humans should not have a detailed conscious repre- sentation of minor adjustments of ANS parameters, because minor regula- tion should be performed automatically without taxing the control center.

326 THE CONSCIOUS–UNCONSCIOUS DEBATE

In contrast, in the case of a strong emotion with massive, highly synchro- nized deviations from baseline across several response modalities, one would expect the changes to be represented in consciousness to allow high- level coping and regulation. The question is whether that emergence into consciousness happens in the form of an integrated representation (e.g., becoming aware of high arousal or excitation) or in the form of domain- specific representations (e.g., increased heart rate, short breath, perspira- tion, etc.). Most likely, both processes operate. People often do report spe- cific symptoms in connection with an emotional experience (and, as sug- gested earlier, there is little evidence that strong symptoms during intense experiences cannot be accurately reported). At the same time, people also readily evaluate the degree of their arousal or excitation (to name but one possible integrated representation). So far, few studies have been con- ducted to evaluate the correlation between these impressions and objective indicators. Past research has shown, however, that there does not seem to be a single indicator of arousal. This is as it should be if, as one would expect, arousal or excitation reflects an integrated representation across several modalities.

As this brief overview suggests, an important effort of conceptualiza- tion and much basic research are needed to better understand the underly- ing feedback and integration mechanisms and the specificity of each domain. It is to be hoped that neuropsychological research on the projec- tion and organization of proprioceptive feedback in different domains can provide fresh insight on these complex phenomena.

Integration across Components and Time

Although the issue of integration and the form in which raw or integrated representations reach consciousness are difficult to address, they are even harder to conceptualize and study across domains. If emotional episodes are subjectively experienced as an integrated whole, as one may assume from the way in which people normally talk about their emotions, there must be some kind of overall integration and representation across the dif- ferent components and across time. Although we can focus on micro- momentary changes of feeling and particular cognitive processes or periph- eral responses, it seems that we more typically become aware of our feelings in experiential chunks. In other words, there is some phenomenal unity to the feeling in a particular emotion episode, possibly linked to a cause–effect chain as well as to some type of closure. In consequence, there must be a powerful process of integration across components and over time. What is the structure of this integration, its gestalt or organizing prin- ciple? Here I again contrast the different suggestions made by dimensional

Unconscious Processes in Emotion 327

theories, discrete emotion theories, and my own version of componential appraisal theory.

Dimension theorists suggest that subjective experience is integrated along the dimensions of valence and arousal. Recently, Russell and Barrett (Russell, 2003; Russell & Barrett, 1999) have suggested that the representa- tion of feeling in this two-dimensional space, prior to further elaboration, is the primitive core affect (see also Barrett, Chapter 11). This idea has a ven- erable history, having been first articulated by Wundt (1874), who proposed a tension–relaxation dimension in addition to valence and activation. The assumption is that the feeling constituted by these dimensions is a con- scious phenomenon and accessible to introspection.

Basic emotion theorists have not felt the need to extensively discuss the issue of feeling and the role of consciousness, because the assumption of homogeneous emotion patterns entails the existence of feeling states that correspond to the patterning provided by the respective basic emotions. These states are accessible to consciousness and labeled by the respective verbal emotion labels. Thus, in this tradition, feeling states are integrated with regard to basic emotion families.

The position of appraisal theorists is less clear and possibly less homo- geneous. Therefore, I describe my own position in greater detail (summa- rized from Scherer, 2004a). I have argued earlier (Scherer, 1984) that there are as many different emotions as there are distinguishable patterns of appraisal results. This explanation translates directly into the issue of inte- gration and feeling. Briefly put, I suggest that multidomain integration is unique to the specific stimulus event and the appraisal results it generates. These results, and the proprioceptive feedback of the response patterns they produce, are integrated across components and over time, in the form of qualia—specific emotional experiences that are unitary, indivisible phe- nomena. I further suggest that it is the very process of synchronization, which I have proposed as the hallmark of emotion as an affective phenome- non, that elicits and organizes this process of integration. It seems safe to assume that this integration occurs outside of awareness. As Anderson (1989, p. 147) suggested earlier: “What does attain consciousness is often, perhaps always, a result integrated across different sense modalities at pre- conscious stages.”

What processes might mediate the emergence into consciousness of preconsciously integrated content? In a chapter urging the use of nonlin- ear dynamic systems theory for the description of emotion processes (Scherer, 2000a), I suggested that this point might be marked by a quali- tative change in a monitor system that reacts to a degree of coupling or synchronization of the subsystems that surpasses the normal baseline fluctuations.

328 THE CONSCIOUS–UNCONSCIOUS DEBATE

What is the justification for claiming that emotional experience is inte- grated in the form of qualia, or myriad different representations? Claiming such a mechanism seems to contradict the postulate for efficiency and par- simony I have advocated in several places earlier. However, if feelings rep- resent a monitoring system that serves to regulate, it seems appropriate to assemble as much detailed information as possible in a central represen- tation to fine-tune regulation attempts. Specifically, the integration of proprioceptive information from response components should maintain a maximal amount of detail in unconscious short-term memory (as symbol- ized by circle A in Figure 13.2). Many low-level regulation processes are likely to operate at this level and can benefit from a comprehensive repre- sentation of the behavioral meaning of the eliciting event and the response profile that was produced by the associated appraisal process.

When part of the unconscious representation becomes conscious or is to be stored in long-term memory (e.g., passing from circle A to circle B in Figure 13.2), further integration will be required. One could argue that it is at this point that integration along the lines of dimensions or basic emotion categories occurs. Yet based on the fact that we can obtain self-report on appraisal patterns, or experienced symptoms, or expression patterns in addition to emotion labels, it is likely that even at this level, detailed infor- mation is retained in less integrated form. Self-report is certainly biased by social representations concerning emotions, including stereotypes, but it is highly likely that individuals do have conscious access to central represen- tations of their appraisals and response patterns, at least in the sense of out- come consciousness (as compared with process consciousness).

Further integration occurs when conscious experience is verbalized (the intersection of circles B and C in Figure 13.2). Although the common path for integration is constituted by the semantic field for emotional phe- nomena in the respective language, this does not mean that the integration necessarily occurs along the lines of discrete emotion categories, as repre- sented by single words or concepts or by valence and arousal dimensions. Verbal report is not limited to simple naming; it can use complex expres- sions and even analogies or metaphors (Lakoff & Kövecses, 1987). Clearly, if respondents are forced to respond to a limited number of categories, as identified by labels or dimensions, they will integrate the information retrieved from memory in a form that allows them to decide among the alternatives or determine the overall valence or arousal level. However, this form of report does not constitute evidence that preformed categories or dimensions determine the integration early on in the process. Functionally, it makes sense to keep as much detailed representation as possible and to perform only as much integration as necessary.

Unconscious Processes in Emotion 329

The conceptualization of conscious affective feeling suggested here does not contradict the proposals made by dimensional or discrete emotion theorists but, rather, integrates these proposals. Although I would continue to hold that there are as many different emotional states as there are poten- tial appraisal patterns, it is true that some appraisal profiles occur much more frequently than others, producing what I have called modal emotions (Scherer, 1994). These emotions correspond to the basic emotion categories that exist in all languages, reflecting the well-known fact that discrete ver- bal labels reflect objects, events, or concepts for which there is a strong need to communicate. Most likely, conscious feeling states corresponding to frequently encountered appraisal profiles form already coherent qualia even before verbalization (circle B in Figure 13.2). The act of verbal encod- ing probably serves to focus the feeling further and structure it around social and individual schemas.

With respect to dimensional theories, I suggested many years ago that the Wundtian dimensions of feeling might reflect underlying criteria of emotion processing (Scherer, Abeles, & Fischer, 1975, p. 138). Translated into the more recent notion of stimulus/evaluation checks, this means that (1) the valence dimension reflects appraisal of intrinsic pleasantness and goal conduciveness, (2) activation reflects pertinence and urgency, and (3) power/control reflects coping potential (see also Scherer, 2004a; Scherer, Dan, & Flykt, in press). Here I would disagree with Russell and Barrett’s view that the valence and activation dimensions are somehow primary or reflect a primitive “core” of affective feeling. Rather, I see them as deriva- tive or secondary in the sense that the individual is able to synthesize or project more complex feeling states onto those dimensions when required to do so. However, the issue is open to debate and focused empirical inves- tigation.

CONCLUSION

It is common knowledge that the relationship between emotion and con- sciousness is extremely complex. The current contribution renders the issue even more complex by (1) insisting on multiple dimensions, facets of consciousness, and associated processes, and (2) highlighting the impor- tance of the neglected phenomena of subsystem synchronization and inte- gration as decisive determinants of the emergence of feeling into con- sciousness. The latter processes, which have rarely been addressed in the literature, are central features of emotion. I do not tire of suggesting that multicomponent synchronization is the essential feature that distinguishes

330 THE CONSCIOUS–UNCONSCIOUS DEBATE

emotional from nonemotional states, and I have speculated that the emer- gence of conscious feeling may be related to the degree of synchronization, which is related to the need for high-level controlled regulation (Scherer, 1984, 2001a). In discussing neuroscience approaches of relevance to cur- rent debates in emotion psychology (Scherer, 1993), I suggested that Damasio’s (1990) model of time-locked or synchronized multiregion activa- tion as a potential mechanism for memory recall might be an interesting example of CNS-based synchronization. Over the last 15 years, the notion of neural synchronization as a basis for multimodal temporal binding (Treisman, 1996) has become extremely popular. Partly because of an influ- ential paper by Crick and Koch (1990), there have been several attempts to link neural synchronization to the emergence of awareness and conscious- ness. In a comprehensive overview of this literature, Engel and Singer (2001) point out that any theory about the neural correlates of conscious- ness must explain how multiple component processes can be integrated and how large-scale coherence can emerge within distributed neural activ- ity patterns (see Dennett, 1991, for an alternative view). This is exactly what is required to understand emotion as conceptualized by the compo- nent process model. Engel and Singer review evidence showing that cross- system coherence and dynamic response selection can be achieved through dynamic binding of distributed information via temporal synchronization of neuronal discharges (with precision in the millisecond range). Concretely, Engel and Singer (p. 23) suggest that synchrony may be ideally suited to promote access of selected contents to working memory (“Synchronized assemblies may stabilize in some reverbatory state, endowing them with competitive advantage over temporarily disorganized activity”), thus be- coming conscious. According to Engel and Singer (p. 24), the process of neural synchronization also explains integration: “Temporal binding may establish patterns of large scale coherence, thus enabling specific cross- system relationships that bind subsets of signals in different modalities.”

To date, most of the empirical work has been done on perceptual and somatosensory processes in animals, apart from some pioneering work on human perception (Tallon-Baudry, Bertrand, Delpuech, & Pernier, 1996). However, the general framework is extremely pertinent to the issue of emo- tion emerging into consciousness, as discussed in this chapter. I hope that the effort to disentangle different aspects of consciousness and to start speculating about underlying processes may help, in the long run, to pose more specific questions, amenable to systematic experimental research. It seems obvious to me that progress in understanding the underlying mecha- nisms critically depends on the development of a truly interdisciplinary domain of affective sciences and effective collaboration with the behavioral neurosciences.

Unconscious Processes in Emotion 331

ACKNOWLEDGMENTS

I gratefully acknowledge helpful comments and suggestions by David Sander Didier Grandjean, and Ursula Scherer.

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CHAPTER 14

Emotion, Behavior, and Conscious Experience

Once More without Feeling

PIOTR WINKIELMAN KENT C. BERRIDGE JULIA L. WILBARGER

This chapter focuses on the relation of unconscious components of emo- tion to conscious feeling. By conscious feeling we mean the experiential, phenomenological, “what-it’s-like” aspect of emotion. We ask whether valenced states—affect and emotion—can exist as well as drive the organ- ism’s behavior without participation of conscious feeling. The question is controversial because, as we will see shortly, there is a tradition in the human emotion literature to view conscious feeling as central for emotion.

The chapter is structured as follows. First, we summarize the tradi- tional view on emotion and conscious feeling. Second, we argue for the idea of unconscious or unfelt emotion. Third, we address some of the empirical and philosophical challenges of this idea. Fourth, we address the relation between conscious and unconscious components of emotion.

EMOTION WITH FEELING

Definitions

An old line says there are more emotion definitions than emotion research- ers. However, if there is one definition on which most researchers agree, it

335

336 THE CONSCIOUS–UNCONSCIOUS DEBATE

1. What is the scope of your proposed model? When you use the term emotion, how do you use it? What do you mean by terms such as fear, anxiety, or happi- ness?

We think of emotion as a state in which several systems of the organism are directed toward a specific valence. As we discuss in the section titled “Defini- tions,” it is typically assumed that emotion is characterized by loosely coordi- nated changes in several components, including (a) conscious feeling, (b) perception and cognition, (c) action tendency, (d) bodily expression, and (e) physiology. Our chapter examines whether the conscious feeling component is indeed necessary for emotion in human and nonhuman animals. We conclude that it is not.

2. Define your terms: conscious, unconscious, awareness. Or say why you do not use these terms.

One important aspect of consciousness is the potential of the organism to intro- spect about a state and to express it verbally or nonverbally. As we argue in the chapter, sometimes an emotion state can be principally unconscious, that is, unavailable to the systems responsible for expression and introspection, even under proper motivational and cognitive conditions.

3. Does your model deal with what is conscious, what is unconscious, or their relationship? If you do not address this area specifically, can you speculate on the relationship between what is conscious and unconscious? Or if you do not like the conscious–unconscious distinction, or if you do not think this is a good question to ask, can you say why?

The relation between conscious and unconscious aspects of emotion involves a complex set of psychological and neural factors. Conscious aspects of emotion probably emerge from a hierarchy of unconscious emotional processes, imple- mented by interactive brain systems that form reciprocal connections across subcortical and cortical networks. Some specific factors are discussed in our section “What Makes Emotion Unconscious or Conscious?”

is probably close to this. Emotion is a state characterized by loosely coordi- nated changes in the following five components: (1) feeling—changes in subjective experience; (2) cognition—changes in attentional and perceptual biases, low-level appraisals, and high-level beliefs; (3) action—changes in the predisposition for specific responses and the general behavioral direc- tion; (4) expression—changes in facial, vocal, postural appearance; and (5) physiology—changes in the central and peripheral nervous systems. This definition is presented in several classic textbooks on emotions and is used throughout this volume (e.g., Atkinson & Adoplphs, Chapter 7; Scherer, Chapter 13; but for a critical position, see Barrett, Chapter 11).

Emotion, Behavior, and Conscious Experience 337

It is also useful to distinguish between affect and emotion. The term affect describes a state that can be identified primarily by its positive– negative valence. The term emotion describes a state that can be identified by more than its valence and includes specific types of negative states (e.g., fear, guilt, anger, sadness, disgust) and specific positive states (e.g., happi- ness, love, pride). Throughout this chapter we primarily use the term emo- tion because we believe that our arguments also apply to specific emotion states, even though the empirical evidence for our position has been obtained primarily in the domain of affect. We return to this issue later.

Theories of Emotion: Feeling as a Central Component

Theorists have long recognized that there are many components of emo- tion. Typically they have considered feeling as a central or even a neces- sary component. Consider some of the influential theorists. In “What Is An Emotion?” William James proposes that conscious feeling, generated through the perception of bodily changes, is exactly what distinguishes emotion from other mental states. Without it, “we find that we have noth- ing left behind, no ‘mind-stuff’ out of which the emotion can be consti- tuted” (James, 1884, p. 193). Similarly, Freud, though often portrayed as the father of the unconscious, specifically excluded emotions from the realm of states that can exist without being experienced. Freud believed that emo- tions are always conscious, even if their underlying causes sometimes are not: “It is surely of the essence of an emotion that we should feel it, i.e. that it should enter consciousness.” (Freud, 1950, pp. 109–110). These assump- tions are shared by contemporary theorists. Clore (1994) titled one of his essays “Why Emotions Are Never Unconscious” and declared subjective feeling as a necessary (although not a sufficient) condition for emotion (see also Clore, Storbeck, Robinson, & Centerbar, Chapter 16). In defining affect, Frijda says that the term “primarily refers to hedonic experience, the experience of pleasure and pain” (1999, p. 194; emphasis added). In short, past and present theorists of human emotion emphasize the centrality of conscious feeling.1

Emotion Research: Feeling as a Central Agenda

The feeling component is emphasized not only in theories but also in research on human emotion. In social-psychological studies, for example, the presence of an emotion is typically determined by self-reports of feel- ings (e.g., mood questionnaires, affective checklists, interviews). When studies collect multiple measures of emotion, including the cognitive, behavioral, expressive, or physiological components, the self-report is often

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considered as the “gold standard” for determining whether emotion had occurred (Larsen & Fredrickson, 1999). There is also a lot of substantive interest in the nature of feelings. For example, some of the debates in emo- tion literature concern the contribution of bodily responses to feelings (Niedenthal, Barsalou, Ric, & Krauth-Gruber, Chapter 2; Prinz, Chapter 15), the dimensional structure of feelings (Russell, 2003), individual differ- ences in the valence versus arousal component of feelings (Barrett, Chapter 11), the role of culture in type and frequency of feelings (Mesquita & Markus, 2004), and the simultaneous coexistence of positive and negative feelings (Cacioppo, Larsen, Smith, & Berntson, 2004).

Most important, conscious feeling is seen as a central causal force in emotional impact on behavior. One example comes from research on judg- ment. A dominant model, tellingly called “feeling-as-information,” pro- poses that emotions influence judgment via changes in conscious feelings, which people use as a shortcut to judgment, following the “how-do-I-feel- about-it-heuristic” (Clore et al., Chapter 16; Schwarz & Clore, 2003). The feeling-as-information model has received strong empirical support and certainly captures many cases of affective influence on judgment. However, most studies testing this model relied on manipulations designed to pro- duce conscious feeling states, using stimuli such as music, movies, recall of autobiographical memories, etc. Yet the model is silent on the mechanism by which emotional stimuli that do not change feelings could influence judgments and behavior.

EMOTION WITHOUT FEELING

As we have just shown, conscious feeling has a central place in both the theoretical thinking and empirical practice of human emotion research. However, do emotions always require consciousness? Can one meaning- fully talk about “unfelt” or “unconscious” emotions? Over the last several years, researchers have increasingly started to consider these possibilities.

Unconscious Elicitation of Emotion

The first challenge to the role of consciousness in emotion came from dem- onstrations that subliminal stimuli trigger emotional reactions. These dem- onstrations are now widely accepted in the emotion research community. In fact, in a recent Emotion Researcher, newsletter of the International Society for Emotion Research (2004), on the issue of “unconscious emo- tion,” no contributor expressed doubts that emotion can be elicited outside of awareness or attention.

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An example of a subliminal elicitation of positive affect comes from research on the mere-exposure effect, or the increase in preference to repeated items (Kunst-Wilson & Zajonc, 1980). In one study, participants were first subliminally exposed to several repeated neutral stimuli consisting of random visual patterns. Later those participants reported being in a better mood than participants who had been subliminally exposed to different nonrepeated neutral stimuli (Monahan, Murphy, & Zajonc, 2000). An exam- ple of a subliminal induction of negative affect comes from studies in which subliminal stimuli, such as gory scenes embedded in a movie or pictures of snakes presented to phobic participants, led to an increase in self-reported anxiety (Öhman & Soares, 1994; Robles, Smith, Carver, & Wellens, 1987).

Note, however, that in these studies only the affect-triggering stimulus is unconscious; the affective reaction itself is conscious. Indeed, the very presence of the affective reaction is determined by asking people to self- report. Thus it is useful, instead, to look at other studies that tested the presence of an affective reaction using physiological measures. For exam- ple, skin conductance response, an indicator of sympathetic arousal, can be triggered by subliminally presented emotional words (Lazarus & McCleary, 1951) and by pictures of fear-relevant objects (Lundqvist & Öhman, Chap- ter 5). Similarly, subliminal facial expressions activate the amygdala, a structure involved in assigning affective significance to stimuli (Whalen et al., 1998), and elicit facial reactions detectable with electromyography (Dimberg, Thunberg, & Elmehed, 2000) (for a review, see Lundqvist & Öhman, Chapter 5; de Gelder, Chapter 6; Atkinson & Adolphs, Chapter 7; and Öhman, Flykt, & Lundqvist, 2000). Unfortunately, these studies are not conclusive on the question of unconscious emotion. First, the physio- logical measures used in these studies cannot distinguish between the arousal and valence components of a response, or may reflect other pro- cesses such as facial mimicry. Thus it is not clear if a valenced reaction actu- ally occurred. Second, in these studies self-reports of emotion were either not collected or collected after the physiological measure of affective reac- tions, so it is not clear if the reaction registered in physiology was itself con- scious or not. Third, because these studies did not measure behavioral con- sequences, it is possible that any emotion reaction was extremely weak and possibly inconsequential. Still, the physiological studies are suggestive and raise the possibility that under right conditions, people could have genuine affective reactions that are not manifested in their conscious experience.

Unconscious Emotion

Over the last several years we have offered theoretical arguments and empirical support for the idea of unconscious emotion (Berridge & Winkiel-

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man, 2003; Winkielman & Berridge, 2004). Our views are in agreement with several other authors. For example, Kihlstrom (1999) suggested that the term implicit emotion could be used to refer to “changes in experience, thought or action that are attributable to one’s emotional state, independent of his or her conscious awareness of that state” (p. 432). Damasio (1999) and LeDoux (1996) described how deep brain structures participate in generat- ing an unconscious stage of fear, anger, happiness, and sadness reactions. Lambie and Marcel (2002) suggested that there are “several kinds of unawareness of genuine concurrent emotion” (p. 220), including “an en- tirely nonconscious emotion state” (p. 229).2

In the next several sections we review the main theoretical and empir- ical arguments for the idea that emotion may exist independent of con- scious experience. First, we present functional and evolutionary consider- ations. Second, we review evidence from research on the emotional brain. Third, we discuss relevant psychological studies. Fourth, we address theo- retical and empirical challenges to the notion of unconscious emotion and address outstanding issues.

Functional and Evolutionary Considerations

Does the capacity for emotional behavior evolutionarily precede, follow, or co-occur with the capacity for conscious feeling? This is a difficult question as it involves making historical assumptions about the conjunction of two complex mental faculties: emotion and consciousness (Heyes & Huber, 2001). It is more manageable to ask whether basic affective reactions require conscious processing. Consider simple positive/negative reactions that animals produce to stimuli such as predators, prey, strangers, con- specifics, food, drink, or mates (Konorski, 1967). The function of these affective reactions is to allow animals to react appropriately to favorable or unfavorable events by adjusting sensory apparatus (e.g., prioritizing certain stimuli), physiology (e.g., cardiovascular and hormonal changes), and action (e.g., priming of motor programs). From a design standpoint, it would be disadvantageous if performing this basic function required the organism to possess a cognitive apparatus capable of consciousness (Cosmides & Tooby, 2000). Though little is known about the exact mechanisms of consciousness, it is unlikely it can be implemented by the computational architecture of simple organisms (Dennett, 1991; Prinz, Chapter 15). Further, even in humans, conscious mechanisms are often too slow and imprecise to coordi- nate an emotional response (Smith & Neumann, Chapter 12). Most impor- tant, consciousness is often unnecessary. After all, many relatively complex coordination functions in organisms are efficiently performed without

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experiential representation (e.g., coupling between the cardiovascular, respiratory, and digestive systems, Porges, 1997). In short, it is reasonable to assume that at least basic affective reactions can be performed without engaging mechanisms responsible for conscious feelings (LeDoux, 1996).

One standard challenge psychologists sometimes offer to the above arguments is that positive/negative reactions of simple organisms should not be called affective. For example, paramecia can approach a variety of stimuli, but it makes little sense to use the term positive affect for an organ- ism that does not even have neurons. Further, even in more complex organ- isms, many reactions to favorable or unfavorable stimuli are more aptly classified as reflexes, than affective behaviors. For example, when a spider jumps to kill a prey, it makes little sense to explain this behavior by propos- ing an underlying negative affect state. We agree, and along with most authors, require that to count as affective, the behavior should meet several criteria (Scherer, Chapter 13). First, the organism must be able to assess the input in terms of valence. Second, this assessment must lead to a temporary state that involves several synchronized components (i.e., perceptual, hor- monal, cardiovascular, muscular). Importantly, these criteria do not require the organism to explicitly represent its goals or explicitly make emotional “judgments”—only to respond in a coherent way to challenges and oppor- tunities in their environment (see Prinz, Chapter 15).

Given these criteria, affect perhaps should not be assigned to reflexes or to creatures such as paramecia. However, it should be assigned to organ- isms that respond in a coherent, multisystemic fashion to challenges and opportunities, even if these organisms have little cognitive capacity for con- sciousness. For example, under these criteria, reptiles are capable of affect because they show coherent cardiovascular, hormonal, perceptual, and behavioral responses to favorable and unfavorable stimuli (Cabanac, 1999). In fact, there are many structural homologies between the reptilian and the mammalian limbic system (Martinez-Garcia, Martinez-Marcos, & Lanuza, 2002), and there are also remarkable similarities in the affective neuro- chemistry in reptiles, fish, birds, and mammals (Goodson & Bass, 2001).

In short, the available data suggest that vertebrates are capable of coordinated, multisystemic responses to emotionally relevant stimuli, via homologous neural circuitry that regulates these responses across a diver- sity of vertebrate groups. Thus, while it seems inarguable that the neural substrates required for conscious experience are quite different across these groups, there is nonetheless remarkable consistency in other compo- nents of affective response. It therefore seems reasonable to propose that neural components of emotional processing can function in a way that is largely uncoupled from the neural components of consciousness.

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Neuroscientific Considerations

These evolutionary arguments are consistent with research on modern mammalian brains. As we discuss next, both subcortical and cortical struc- tures participate in affective processes. However, as many have suggested, the “old” subcortical structures might be especially important for basic affective reactions, whereas the “new” cortical structures might be espe- cially important for conscious feelings. The locations of the most important structures of the generalized emotional brain are indicated in Figure 14.1. Below we provide a brief overview of what is known about the roles of these structures in generating positive and negative affect. However, we remind the reader that our presentation here is very simplified and does not capture the multiple roles these structures play in both affect and cog- nition, and their complex neuroanatomy and neurochemistry (see Berridge, 2003).

FIGURE 14.1. Approximate location of brain structures important for emotion. The figure does not show the relative depth of any structure and shows only one of each pair of bilateral structures.

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Subcortical Networks and Basic Affective Reactions

The subcortical structures involved in causing basic affective reactions range from the “mere” brainstem to the complex network of the “extended amygdala” (Berridge, 2003). Let us illustrate the critical role of these struc- tures in both positive and negative affect with a few examples.

Brainstem. Though some view it as a merely reflexive structure, almost every physical pleasure or pain must climb its way up through the brainstem. Research shows that in both animals and humans basic affective responses are modulated by structures in the brainstem. For example, in the domain of positive affect, research highlights the importance of the parabrachial nucleus (PBN). The PBN receives signals ascending from many sensory modalities, including visceral signals regarding internal bodily functions, and also taste sensations from the tongue.3 Not surpris- ingly, PBN plays a role in generating positive responses to tasty foods. For example, when a rat’s PBN is tweaked by microinjections that activate its benzodiazepine/gamma-aminobutyric acid (GABA) receptors, the rat pro- duces greater “liking” reactions to sugar, such as tongue protrusions and lip licking (Berridge & Pecina, 1995). In the domain of negative affect, research highlights the importance of the periaqueductal grey (PAG). In animals, the PAG mediates defensive reactions to threatening stimuli (Panksepp, 1998), and in both animals and humans, the PAG mediates responses to pain (Willis & Westlund, 1997). Importantly, the PAG does not simply compile incoming information to relay to the forebrain, but forms reciprocal connections with subcortical forebrain structures, thereby pro- viding an anatomical basis by which sensory stimuli can be processed by the PAG in a context-dependent and coordinated fashion (Panksepp, 1998).

A particularly poignant demonstration of the importance of the brain- stem to basic affective reactions is offered by a cruel experiment of nature. As a result of a birth defect, some infants have a congenitally malformed brain, possessing only a brainstem but no cortex and little else of the forebrain (i.e., no amygdala, nucleus accumbens, etc). Yet in these an- encephalic infants, the sweet taste of sugar still elicits facial expressions that resemble normal “liking” reactions, such as lip sucking and smiles, whereas bitter tastes elicit facial expressions that resemble “disliking” reac- tions, such as mouth gapes or nose wrinkling (Steiner, 1973). In this con- text, it is also interesting that positive facial expressions to sweetness are emitted by chimpanzees, orangutans, gorillas, various monkeys, and even rats (Berridge, 2000; Steiner, Glaser, Hawilo, & Berridge, 2001). The pat- tern of positive facial expression becomes increasingly less similar to

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humans as the taxonomic distance increases between a species and us. But all of these species share some reaction components that are homologous to ours, suggesting common evolutionary ancestry and a similar neural mech- anism that might be anchored in the brainstem.

Extended Amygdala. The term extended amygdala designates a con- figuration that includes the amygdala, nucleus accumbens, ventral pal- lidum, bed nucleus of the stria terminalis, and other structures. Recent years have witnessed an explosion of research highlighting the role of the extended amygdala in basic affective reactions.

Amygdala. The amygdala consists of a pair of almond-shaped struc- tures located in the medial temporal lobe, just anterior to the hippocampus. The amygdala is reciprocally connected to a variety of areas, including the visual thalamus and visual cortex, allowing for affective modification of per- ception; the dorsolateral prefrontal cortex, allowing for upstream and downstream regulation of affect state; and subcortical structures, allowing for affective influence on sympathetic and parasympathetic regulation of cardiovascular activity, respiration, hormone levels, and basic muscular reactions. The role of the amygdala in perceptual and learning aspects of emotion has been confirmed in animal research as well as human neuro- imaging and lesion studies (Phelps, Chapter 3; Atkinson & Adolphs, Chapter 7). Thus patients with congenital or acquired amygdala damage show impairments in conditioned fear responses, fear-potentiated startle responses, and arousal-enhanced perception and memory. Remarkably, patients with damage to the amygdala show little, if any, impairment in their subjective experience of emotion, at least as measured by the magni- tude and frequency of self-reported positive and negative affect assessed by the positive and negative affect schedule (PANAS) (Anderson & Phelps, 2002). This finding suggests a relative independence of the amygdala from the mechanisms underlying the generation of feelings.

There is also evidence that the amygdala can modulate emotional responses independent of any conscious evaluation of the stimulus. Some of this evidence comes from observations that the amygdala can be acti- vated with facial expressions that are not consciously perceived, presum- ably via a direct pathway from the visual thalamus (see Atkinson & Adolphs, Chapter 7). Thus amygdala activation has been observed with expressions of fear and anger presented subliminally (Morris, Öhman, & Dolan, 1999; Whalen et al., 1998), under condition of binocular suppression (Williams, Morris, McGlone, Abbott, & Mattingley, 2004), or to a patient’s blind visual field (de Gelder, Chapter 6).

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Additional evidence for the independence of basic affective reactions and conscious stimulus evaluation comes from autism—a neurodevelop- mental disorder characterized by deficits in communicative and social skills, restricted interests, repetitive behaviors, and impairments in emo- tional abilities (Hobson, 1993; Kasari, Sigman, Yirmiya, & Mundy, 1993). There are several reports of amygdala abnormalities in people with autism (Baron-Cohen et al., 2000). Thus one can expect individuals with autism to be impaired in their basic affective responses, which are dependent on the amygdala, and relatively unimpaired on affective responses that rely on more deliberate, conscious strategies. We have recently obtained such evi- dence in studies of affective startle modulation (Wilbarger, McIntosh, & Winkielman, 2004) which refers to a phenomenon that when individuals are startled by a loud noise, their defensive reflexes, such as the eyeblink, are larger in the context of negative than positive stimuli. This penomenon presumably reflects the modulation of an aversive versus approach re- sponse system (Lang, 1995). The amygdala is critical for such modulation, as suggested by the finding that electrical stimulation of the amygdala enhances startle amplitude, whereas lesions diminish it (Davis, 1997; Funayama, Grillon, Davis, & Phelps, 2001; Phelps, Chapter 3). In our stud- ies the individuals without autism replicated the classic startle modulation pattern: potentiation of an eyeblink response to a loud noise after negative pictures and reduction of the eyeblink after positive pictures. In contrast, the individuals with autism spectrum disorder (ASD) showed startle po- tentiation after both negative and positive stimuli. Importantly, the ASD individuals did not differ from typical individuals on conscious, explicit evaluation of the stimuli, as reflected in self-reports of valence and arousal (Wilbarger et al., 2004). In sum, these data again suggest that the impact of affective stimuli on basic behavioral responses can be dissociated from con- scious responses to the same stimuli.

Ventral Pallidum. The ventral pallidum borders on the lateral hypo- thalamus at its front and lateral sides and is a part of the extended amygdala. In rats, this structure is involved in producing positive reactions to tasty foods, as suggested by the facts that (1) ventral pallidal neu- rons fire to tasty rewards, (2) behavioral “liking” reactions to sweetness are increased by opioid drug microinjections in the ventral pallidum, and (3) excitotoxin lesions of the ventral pallidum abolish hedonic reactions and cause aversive reactions (e.g., gaping and headshakes) to be elicited even by normally palatable foods (Cromwell & Berridge, 1993; Tindell, Berridge, & Aldridge, 2004). The ventral pallidum may also be crucial to sexual and social pair bonding in rodents (Insel & Fernald, 2004). Less is

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known regarding the role of the ventral pallidum in affect mediation for humans, because the structure is too small to study via brain imaging. How- ever, there are a few intriguing observations. For example, electrical stimu- lation of the adjacent structure, the globus pallidus, has been reported to sometimes induce bouts of affective mania that can last for days (Miyawaki, Perlmutter, Troster, Videen, & Koller, 2000). In addition, the induction of a state of sexual or competitive arousal in normal men was found to be accompanied by increased blood flow in the ventral globus pallidus (Rauch et al., 1999).

Nucleus Accumbens. The nucleus accumbens, which lies at the front of the subcortical forebrain and is rich in dopamine and opioid neurotrans- mitter systems, is as famous for positive affective states as the amygdala is for fearful ones. The accumbens systems are often portrayed as reward and pleasure systems. In fact, activation of dopamine projections to the ac- cumbens and related targets has been viewed by many neuroscientists as a neural “common currency” for reward. There is actually evidence that the accumbens reflects not “pleasure” or “liking” of the stimulus, but rather an incentive salience, or “wanting,” of the stimulus (Berridge & Robinson, 1998). However, for the purpose of our argument here it is only important to highlight the role of the accumbens in positive affective reactions. For example, in rats, brain microinjections of drug droplets that activate opioid receptors in the nucleus accumbens cause increased “liking” for sweetness (Pecina & Berridge, 2000). In humans, the accumbens activates to drug cues and to other desired stimuli, including foods, drinks, and even money (Knutson, Adams, Fong, & Hommer, 2001).

Cortical Networks and Subjective Experience

We cannot talk about the emotional brain of mammals without discussing the cortex. In fact, when human subjects spontaneously recall emotional events, a host of cortical structures activate, including the prefrontal cor- tex, the insular cortex, the somatosensory cortices, and the cingulate cor- tex (Damasio et al., 2000). The approximate location of these structures is shown in Figure 14.1. Several chapters in this volume address the role of cortical structures in more detail (Niedenthal et al., Chapter 2; Phelps, Chapter 3; Gray, Schaefer, Braver, & Most, Chapter 4; Atkinson & Adolphs, Chapter 7; Prinz, Chapter 15; other chapters suggest it: Barrett, Chapter 11; Clore et al., Chapter 16). Here we only mention research most relevant to the proposition that the cortex mediates conscious expe- rience by hierarchically monitoring and rerepresenting subcortical pro- cesses.

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Prefrontal Cortex. The prefrontal cortex lies, not surprisingly, at the very front of the brain. The ventral or bottom one-third of the prefrontal cortex is called the orbitofrontal cortex and is the most elaborately devel- oped in humans and other primates. There is some evidence that sub- cortical projections to the prefrontal cortex contribute to conscious affec- tive experience. For example, the intense feeling of pleasure experienced by heroin users appears to involve accumbens-to-cortex signals that are relayed to cortical regions via the ventral pallidum and thalamus (Wise, 1996). In another example, self-reports of excitement in typical participants are related to the degree of activation in the nucleus accumbens and prefrontal cortex (Knutson et al., 2004). The prefrontal cortex is important not only for conscious feelings; it also participates in affective reactions by modulating lower brain structures via descending projections (Damasio, 1999; Phan, Wagner, Taylor, & Liberzon, 2002). For example, the orbito- frontal cortex projects back to the accumbens (Davidson, Jackson, & Kalin, 2000), and the dorsolateral prefrontal cortex projects back to the amygdala (Ochsner & Gross, 2004).

Somatosensory Cortex and Insula. The primary (S1) and secondary (S2) somatosensory cortices are located behind the central sulcus and are responsible for monitoring the state of the body, including sensations (e.g., touch) and proprioception (i.e., state of muscles and joints), and for creating the internal “image” of the body (Ramachandran & Blakeslee, 1998). The insula is located near the bottom of the somatosensory cortices, almost at the intersection of the frontal, parietal, and temporal lobes, and receives inputs from limbic structures, such as the amygdala, and cortical structures, such as the prefrontal and posterior parietal cortices and the anterior cingulate. It appears to be particularly important for introception: monitor- ing the state of internal organs (Craig, 2003; Critchley, Wiens, Rothstein, Öhman, & Dolan, 2004).

There is evidence that the somatosensory cortices and the insula might jointly contribute to emotional experience by generating a model of the current body state. The neuropsychological evidence for this mechanism is extensively discussed by Atkinson and Adolphs (Chapter 7), and psycholog- ical evidence is reviewed by Niedenthal et al. (Chapter 2). For example, neuroimaging studies show that recall of emotional memories is associated with extensive activation of the somatosensory cortices (Damasio et al., 2000). In another example, lesions to the right somatosensory cortex are associated with both impaired perception of facial expressions and im- paired touch perception (Adolphs, Domasio, Tranel, Cooper, & Domasio, 2000). Finally, human studies show involvement of the insula in pain (Peyron, Laurent, & Garcia-Larrea, 2000), disgust (Wicker, Keyers, Plailly,

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Royet, Gallese, & Rizzolatti, 2003), and appreciation of sweet tastes and related rewards (O’Doherty, Deichmann, Critchley, & Dolan, 2002).

Cingulate Cortex. The cingulate cortex consists of a longitudinal strip running front to back along the midline of each brain hemisphere. It is a richly interconnected structure thought to interface between the limbic system and the prefrontal cortex. The cingulate cortex has been implicated in human clinical conditions such as pain, depression, anxiety, and other distressing states (Davidson, Abercrombie, Nitschke, & Putnam, 1999; Peyron et al., 2000). Interestingly, some research suggests that a conscious experience of emotion, per se (e.g., “I’m angry”), is associated with the dor- sal anterior region of the cingulate cortex, whereas more reflective parts of the emotional awareness (e.g., “I know I’m angry”), are associated with the rostral anterior region (Lane, 2000).

Interactions of Cortical and Subcortical Networks

As our brief review indicates, both subcortical and cortical systems partici- pate in emotion as a complex network connected in multiple loops. Within those loops, however, the subcortical systems seem essential for triggering basic affective reactions, whereas the cortical systems seem essential for supporting conscious affective experience. Specifically, the conscious expe- rience appears to emerge from the interaction between the cortical and subcortical loops, as the cortex hierarchically rerepresents and feeds back on the causally active subcortical processes. Importantly, we are not dimin- ishing the causal role of the cortex in emotion; as obviously, for humans, many events trigger an emotional response after extensive cortical process- ing. We are simply suggesting that in order to have a conscious emotional experience, the cortical networks may need to receive and reprocess input from subcortical networks.

Is it possible that conscious feelings exist subcortically, perhaps in structures as deep as the brainstem’s periaqueductal grey (PAG)? For exam- ple, Panksepp argued that “the most basic form of conscious activity . . . arises from the intrinsic neurodynamics of the PAG” (1998, p. 314) and sug- gested that “it is the PAG that allows creatures to first cry out in distress and pleasure” (p. 314). We agree that it is logically possible that brainstem circuits generate a rudimentary but real consciousness. This possibility can never be conclusively disproved. For now, it seems more likely that these subcortical circuits simply instantiate unconscious affective process. Those processes do not give rise to conscious feelings by themselves. They are not even directly accessible to conscious introspection in a normal brain, as evi- denced by people’s inability to report subliminally induced affect (dis-

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cussed shortly). Accordingly, we propose that the isolated brainstem is capable of unconscious “likes” and “dislikes,” which it reflects behaviorally, but not of conscious feelings of pleasure or displeasure.

Finally, it is worth highlighting that our point really is not about ana- tomical separation—a neat division of labor in which subcortical networks instantiate unconscious processes, whereas cortical networks instantiate conscious processes. Our point is that the mechanisms of consciousness are computationally demanding and require ability to rerepresent the input, integrate across multiple sources of input, and probably create some rudimentary representation of the self (Dennett, 1991). On that view, different mechanisms could be mixed together in the same brain divisions, or the same brain divisions could have both conscious and unconscious modes.

In sum, the multiplicity of loops and levels within brain networks raises the possibility for functional decoupling, possibly producing emo- tional reactions without conscious feelings, as well as conscious feelings without emotional reactions reflected in physiology or behavior. In fact, some research reviewed earlier could be interpreted as showing a double dissociation (A occurs without B, and B occurs without A). For example, “liking” responses in anacephalic babies represent the preservation of basic affective reactions after damage to mechanisms supporting consciousness (Steiner, 1973), whereas intact conscious feelings in patients without the amygdala (Anderson & Phelps, 2002) represent preservation of conscious experience after damage to subcortical mechanisms supporting basic affec- tive reactions. This possibility is consistent with research in experimental psychology, as we review next.

Experimental Psychology

All statements about whether emotion can or cannot be divided into con- scious versus unconscious are mere speculations. Without actual evidence of unconscious emotion, even positing its existence is a matter of taste. Neuroscientific evidence by itself is suggestive, but not enough—it could be consistent with either possibility. Further, much of neuroscientific evidence comes from animal studies and studies of brain-damaged patients. What is needed is an unambiguous demonstration of unconscious emotion— if it indeed exists—in typical individuals who are not brain damaged, not drug addicted, not under hypnosis, not under extreme circumstance, and not lacking in verbal or intellectual skills. If evidence could actually be obtained, then the discussion would shift from whether unconscious emo- tion is possible to how it is possible and what it means for psychology and neuroscience. So—is there any clear evidence?

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Uncorrected and Unremembered Affective Reactions to Facial Expression

An initial approach to the question of whether participants can be unaware of their affective responses was made in a study that asked participants to rate novel and neutral stimuli, such as Chinese ideographs (Winkielman, Zajonc, & Schwarz, 1997). Unbeknownst to the participants, some ideo- graphs were preceded by subliminally presented happy or angry faces. As mentioned earlier, neuroimaging studies suggest that subliminal angry and fearful faces activate the amygdala and related limbic structures, and are particularly likely to trigger unconscious affective reactions. As participants were making judgments of the ideographs, some were asked to monitor changes in their conscious feelings and told not to use their feelings as a source of their preference ratings. Those participants were also given instructions containing plausible alternative explanations for why their feel- ings might change, such as music playing in the background, or, closer to the truth, participants were told about invisible subliminal stimuli that might influence their mood. In effect, these instructions encouraged cor- rective attributions that typically eliminate the contaminating influence of conscious feelings on evaluative judgments (Clore, 1994). However, even for participants who knew to disregard their “contaminated” feelings, the subliminal happy faces increased, and the subliminal angry faces de- creased, preference ratings. Most relevant to the question of unconscious emotion, participants did not remember experiencing any changes in their mood when asked after the experiment about their emotions. Still, these studies are subject to criticism. Affective memory is not infallible. A skeptic could well argue that participants had a conscious emotional experience when exposed to subliminal affective faces, but simply failed to remember it later. Further, misattributional manipulations can fail for a variety of cog- nitive and motivational reasons.

Unconscious Affective Reactions Strong Enough to Change Behavior

We agree that stronger evidence is needed. Such evidence would show that cognitively able and motivated participants are unable to report a conscious feeling at the same time that their behavior reveals the presence of an affective reaction. Ideally, the affective reaction should be strong enough to change even behavior that has real consequences for the indi- vidual. To obtain such evidence, we assessed consumption behavior, requiring ingestion of a novel substance, after exposing participants to several subliminal emotional facial expressions (either happy, neutral, or angry). Each of the subliminal expressions was masked by a clearly visi-

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ble neutral face on which participants performed a simple gender detec- tion task (Winkielman, Berridge, & Wilbarger, 2005). Immediately after the subliminal affect induction, some participants rated their feelings (mood and arousal) and then consumed a fruit beverage. Other partici- pants performed consumption behavior and feeling ratings in opposite order. In Study 1, the consumption behavior involved pouring themselves a cup of a novel drink from a pitcher and then drinking it. In Study 2, participants were asked to take a small sip of the drink and rate it on dif- ferent dimensions (e.g., monetary value). In both studies, there was no evidence of any change in conscious mood or arousal, regardless of whether participants rated their feelings on a simple scale from positive to negative or on a multi-item scale asking about specific emotions. That is, participants did not feel more positive after viewing subliminal happy expressions, nor did they feel more negative after angry expressions. Yet participants’ consumption behavior and drink ratings were influenced by those subliminal affective stimuli, especially when participants were thirsty. Specifically, thirsty participants exposed to subliminal happy faces poured significantly more drink from the pitcher and drank more from their cup than those exposed to subliminal angry faces (Study 1). Thirsty participants were also willing to pay about twice as much more for the drink after exposure to happy, rather than angry, expressions (Study 2). That is, subliminal emotional faces evoked affective reactions that altered participants’ consumption behavior and evaluation of the beverage, but produced no mediating change in their conscious feelings at the moment the affective reactions were caused. Since participants rated their feelings of mood immediately after the subliminal affect induction, these results cannot be explained by the failure of affective memory. Thus we propose that these results demonstrate unconscious affect in the strong sense—an affective process strong enough to alter behavior, but of which people are simply not aware, even when attending to their feelings.

CHALLENGES TO UNCONSCIOUS EMOTION

Findings such as the one just described constitute some evidence for the independence of affect and conscious experience. But there are several challenges to be met.

How Does Unconscious Affect Work?

One challenge involves specifying the mechanisms by which affect can influence behavior toward an object without eliciting conscious feelings.

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One possibility is that unconscious affect directly modulates the object’s ability to trigger affective and motivational responses via a “front-end” or perceptual–attentional mechanism (Phelps, Chapter 3). That is, instead of triggering feelings, the affect could modify the position of relevant target objects on the organism’s “incentive landscape.” For example, in our bever- age studies, the exposure to subliminal happy or angry expressions could transiently multiply up or down the incentive value of the drink, leading to differential behavior and ratings. To give a neuroscientific account of a possible mechanism, we speculate that subliminal facial expressions might activate the amygdala, which then might activate the adjacent accumbens and related structures responsible for processing natural incen- tives (Berridge, 2003; Rolls, 1999; Whalen et al., 1998). Altered neuronal activity in the nucleus accumbens (constituting unconscious “liking”) could then change the human affective reaction to the sight and taste of a drink, leading to differential behavior and ratings, all without eliciting conscious feelings. In other words, we propose a mechanism that is not unlike what happens when a morphine microinjection into a rat’s shell of accumbens enhances the rat’s affective reaction to sweetness and leads to behavioral reaction of greater “liking.” This proposal awaits empirical testing.

Affect or Emotion?

Some skeptics accept unconscious affect but deny unconscious emotion (e.g., Barrett, Chapter 11). They point out that much of the evidence con- cerns basic unconscious positive–negative or liking–disliking reactions, and not the categorically different states associated with emotion (e.g., fear, anger, disgust, sadness, joy, love, pride). However, note that subcortical cir- cuitry is capable of at least some qualitative differentiation. For example, animals, even reptiles, show some categorical reactions to situations de- manding different emotional response (Panksepp, 1998). In another exam- ple, human neuroimaging studies reveal different patterns of amygdala activation to consciously presented facial expressions of fear, anger, sadness, and disgust (Phan et al., 2002; Whalen, 1998). If future research shows that masked expressions of fear, anger, disgust, or sadness can create different physiological reactions with different behavioral consequences, all without eliciting conscious feelings, then there might indeed be processes fully deserving the label “unconscious emotion.” Studies that measure psycho- physiological, behavioral, and self-report manifestations of emotion with- in a single design could be particularly useful to address such issues (Winkielman, Berntson, & Cacioppo, 2001).

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Affect or Cognition?

A critic may challenge the idea of unconscious affect by explaining the rele- vant empirical phenomena using a cognitive framework (e.g., Clore et al., Chapter 16). For example, the critic could argue that in our beverage stud- ies, facial expressions influenced behavior via cognitive reinterpretation of the consumption situation. In general, note that such an explanation is divorced from the larger animal and human literature suggesting involve- ment of subcortical mechanisms in the processing of facial expressions and consumption stimuli. More specifically, note that the cognitive account can- not explain several findings from the beverage studies. First, the cognitive account predicts that all evaluations should be influenced by subliminal facial expressions. However, subliminal expressions influenced only ratings related to the incentive value of the drink, as predicted by our account, but not ratings of mood or ratings of the drink that were irrelevant to its incen- tive value (e.g., sweetness), as would be predicted by the cognitive account. Second, a cognitive account cannot easily explain why the influence of facial expressions was selectively amplified by a motivational state (thirst), whereas that prediction naturally follows from our incentive value account. In short, our proposed explanation in terms of unconscious affect changing the drink’s incentive value is more consistent with the literature as well as the obtained data.

Unnoticed, Unverbalized, or Unconscious Affect?

Yet another challenge comes from the difficulty of conclusively establishing the absence of feelings. For one, there is the pesky problem of “proving the absence.” This problem can be addressed, however, through converging replications, such that the presence of conscious feelings is established as unlikely (just as Santa Claus cannot be proven nonexistent, but can be proven unlikely to exist). A more substantive problem involves the very nature of reporting on phenomenal states. Several writers point out the difference between primary “experiencing” or “raw” consciousness and secondary “reflecting” or “meta” consciousness (Charland, Chapter 10; Lambie & Marcel, 2002; Schooler, 2002). This distinction suggests that people can “feel” without being “aware that they feel.” Thus, perhaps in our drinking experiments, angry facial expression did indeed elicit “raw” anger, but our participants never reached a conscious, reportable belief that they “feel angry.” Or perhaps participants’ feelings were too subtle to be reflectively appraised. Or perhaps participants’ attempts to reflect destroyed their fleeting feelings. These are all interesting possibilities.

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However, we find them unlikely. First, the impact of the unconscious affect was sufficiently strong to change our participants’ behavior, so it should have been sufficiently strong to change their reports of experience. Second, our participants were able to self-report on other aspects of their mood and sensations, as reflected in individual differences in reports of their base- line mood states and in their precise reports of drink experience (see Winkielman et al., 2005). Still, future research should examine to what extent the absence of self-reported feelings in human studies represents a genuine absence of phenomenology or an inability to reflect on that phe- nomenology. Several writers have suggested that these questions could be addressed by providing participants with training in (1) introspection, (2) use of beepers, ratings scales, or momentary affect dials, and (3) alternative, nonverbal ways of expressing emotion (Bartoshuk, 2000; Lambie & Marcel, 2002; Nielsen & Kaszniak, in press; Schooler & Schreiber, 2004). Finally, neuroscience may be of help. If it is possible in the future to reliably iden- tify a neural correlate of subjective experience, the presence of conscious feelings could be suggested by changes in relevant neural activation.

CONSCIOUS AND UNCONSCIOUS EMOTION

In the preceding section we have presented a variety of arguments for the existence of “unfelt” affect and emotion. So are feelings just “icing on the cake”—nice, but not necessary? Are they the “red herring” of emotion research? We do not believe so. In the following section we offer specula- tion on the role of conscious feelings in emotion and the relation between conscious and unconscious components in emotion.

What Good Is Conscious Feeling?

Just like it makes functional sense that emotion can be “unfelt,” there are good reasons why at least some creatures are capable of conscious feelings. In general, there are several benefits for a mental state, whether emo- tional or cognitive, to be conscious (see Gray et al., Chapter 4; Smith & Neumann, Chapter 12; Prinz, Chapter 15). Consciousness allows flexibility and depth. The organism can go beyond simple, habitual reactions and design novel, complex, context-sensitive forms of responding (Dennett, 1991; Rolls, 1999). Consciousness also allows control. The organism can stop undesirable responses and promote the desirable ones, deciding how and when to respond (Ochsner & Gross, 2004). On top of these standard perks of consciousness, the capacity for conscious feelings may give emo- tion a specific communicative and motivational function. Conscious feel-

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ings give internal feedback about how well the organism is doing with the current pursuits, telling it to maintain or change its path (Clore et al., Chap- ter 16). Feelings also come with psychological immediacy and urgency, making the organism “care” about its fate in a way that may not available to any other mechanism (Searle, 1997). This immediacy and urgency applies to simple hedonic states, such as pain and pleasure, and to complex emo- tions. Thus, pangs of guilt propel us to make amends, whereas green eyes of jealousy make us watch for trespasses of our mates (Frank, 1988).

What Makes Emotion Unconscious or Conscious?

Given the many benefits of consciousness, why then are humans sometimes unaware of their emotion? We suppose that a variety of neuroscientific and psychological factors play a role. Most of these factors probably apply regardless of whether the process is emotional or cognitive. Earlier we speculated that under some circumstances, relevant neural processes could simply bypass the circuitry for subjective experience and feed directly into behavioral circuitry. That is, sometimes emotion can be unconscious for the same reason why vision can be unconscious. As documented in research on “vision for perception vs. vision for action” (Goodale & Milner, 2004) and in research on “blindsight” (de Gelder, Chapter 6; Weiskranz, 1996), the rele- vant information can feed into the action system without ever reaching brain areas responsible for subjective experience. Further, sometimes rudi- mentary affective processes may be like other neural processes, such as thermoregulation or fluid regulation which can run unconsciously and elicit conscious experience (e.g., feeling cold, or feeling thirsty) only when there is a need for conscious intervention. Another important factor might be the brain’s inability to construct a coherent percept, as when alternative sources of activation compete for interpretation (Crick & Koch, 2003).

Still other factors preventing the emergence of conscious representa- tion are more psychological. The input might be too weak or too brief, as amply demonstrated in the work on backward masking (Enns & DiLollo, 2000). Or the input may be strong but inconsistent with the perceivers’ expectations and thus escape attentional processing, as demonstrated in research on change blindness (Simons & Chabris, 1999). Or the input may not make sense in the context of the current situation (Dennett, 1991). Yet, in all these cases, the input may be sufficient to influence behavior.

Unfortunately, there is little empirical work on factors that determine the emergence of conscious emotional feelings. Future work could make some progress by, for example, systematically examining what determines whether subliminal stimuli elicit conscious mood. As we discussed earlier, in our research, exposure to subliminal facial expressions did not elicit feel-

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ing (Winkielman et al., 2005). However, other studies observed feeling changes after subliminal bloody pictures (Robles et al., 1987) or mere- exposed ideographs (Monahan et al., 2000). These findings suggest that perhaps simple or highly practiced stimuli, such as happy and angry faces used in our studies, are less likely to elicit feelings than more complex or novel stimuli, such as visual scenes or ideographs. The impact on feelings could also depend on the individual’s sensitivity to a particular emotion inducer. For example, subliminally presented snakes increased conscious anxiety in phobic but not typical participants (Öhman & Soares, 1994). Sim- ilarly, introspectively sensitive participants are better at detecting the impact of subliminal stimuli and use their own reactions in behavior (Katkin, Wiens, & Öhman, 2001). Another interesting factor is the salience of the self representation. That is, when the self is salient, a change in an affective state might be channelled to a conscious feeling, rather than a rep- resentation of an external object (Clore et al., Chapter 16; Lambie & Mar- cel, 2002). Finally, motivational factors could also channel the affect to the representation of the external object or to the conscious feeling. For exam- ple, in our drinking studies, the only hint of change in subjective experi- ence as a result of subliminal expression was observed among nonthirsty participants (for discussion, see Berridge & Winkielman, 2003). In sum, the emergence of conscious feelings may be determined by a host of stimulus, personal, and motivational factors. Though little is known at this point, it seems clear that the question of when and how emotion becomes conscious can be fruitfully investigated in an empirical manner, especially given all the new experimental and neuroscientific techniques now available.

CONCLUSION

In this chapter we argued for the existence of verifiable but unconscious emotional reactions. These reactions may be grounded in the oldest part of the emotional brain and may be similar in humans and animals. Neverthe- less, they can be powerful enough to guide even human behavior and judg- ments. Thus emotion researchers should not limit themselves to subjective experiences when theorizing about emotion and conducting relevant em- pirical research. However, we also believe that conscious feelings are criti- cal for understanding the mechanisms of emotion and its impact on behav- ior. Thus self-reports of feelings and other techniques that tap subjective experience have a major place in emotion theory and research. In fact, we see some of the most exciting topics in emotion research as understanding how and when emotion becomes conscious. Investigations of implicit emo- tional processes, techniques from human and animal affective neurosci-

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ence, and refinements in self-report methodology all can help us better understand the relation between conscious and unconscious emotions.

ACKNOWLEDGMENTS

We thank Jerry Clore, Lisa Feldman Barrett, Jim