The Neuroscience of Emotion: A New Synthesis

by Ralph Adolphs, David J. Anderson

Overview

A new framework for the neuroscientific study of emotions in humans and animals

The Neuroscience of Emotion presents a new framework for the neuroscientific study of emotion across species. Written by Ralph Adolphs and David J. Anderson, two leading authorities on the study of emotion, this accessible and original book recasts the discipline and demonstrates that in order to understand emotion, we need to examine its biological roots in humans and animals. Only through a comparative approach that encompasses work at the molecular, cellular, systems, and cognitive levels will we be able to comprehend what emotions do, how they evolved, how the brain shapes their development, and even how we might engineer them into robots in the future.

Showing that emotions are ubiquitous across species and implemented in specific brain circuits, Adolphs and Anderson offer a broad foundation for thinking about emotions as evolved, functionally defined biological states. The authors discuss the techniques and findings from modern neuroscientific investigations of emotion and conclude with a survey of theories and future research directions.

Featuring color illustrations throughout, The Neuroscience of Emotion synthesizes the latest in neuroscientific work to provide deeper insights into how emotions function in all of us.

Product Details

ISBN-13:	9780691174082
Publisher:	Princeton University Press
Publication date:	06/05/2018
Edition description:	New Edition
Pages:	376
Product dimensions:	6.00(w) x 9.30(h) x 1.20(d)

About the Author

Ralph Adolphs is the Bren Professor of Psychology, Neuroscience, and Biology at the California Institute of Technology (Caltech) and Director of the Caltech Brain Imaging Center. He is the coeditor of Living without an Amygdala. David J. Anderson is the Seymour Benzer Professor of Biology and Director of the Tianqiao and Chrissy Chen Institute for Neuroscience at the California Institute of Technology and an Investigator with the Howard Hughes Medical Institute.

Read an Excerpt

CHAPTER 1

What Don't We Know about Emotions?

The greatest enemy of knowledge is not ignorance, it is the illusion of knowledge.

— Ralph J. Boorstin

If you are like most people, you feel convinced that, because you have emotions, you know a lot about what emotions are, and how they work. We believe you are almost certainly wrong. In the field of emotion, as in most fields, familiarity is not the same as expertise. After all, you have a heart, but that doesn't make you an expert on hearts. You leave that to your cardiologist.

Yet the science of emotion is fraught with this problem: everyone seems to think they know what an emotion is. This is because we all have strong, and typically unjustified, intuitive beliefs about emotions. For instance, some people are absolutely certain that animals have emotions; others are absolutely certain that animals could not have emotions. Neither camp can usually give you convincing reasons for their beliefs, but they stick to them nonetheless.

We cannot emphasize enough the pervasive grip that our commonsense view of emotions has on how we (that is, researchers in the field) frame our scientific questions. We need to free ourselves of our commonsense assumptions — or at least question all of them — if we want to ask the right questions in the first place. This chapter introduces the topics of this book through this important premise and concludes by listing what we ideally would want from a mature science of emotion, and what entries in this list we will tackle in this book.

We wrote this book for two overarching aims. The first aim is to motivate the topic of emotion, to note that it is of great interest not only to laypeople but also to many scientific fields of study, and that it is a very important topic as well. At the same time, we emphasize that we currently know remarkably little about it yet — in particular, we know a lot less than we think we know. This is good news for scientists: there is work to be done, interesting and important work.

The second aim is to provide a summary of what we do know and to sketch a framework within which to understand those empirical findings and within which to formulate new questions for the future. This process is in practice very piecemeal: we need to have a little bit of data even to begin thinking about what emotions are, but then we discover problems with the way prior experiments were done and interpreted. In the dialectic of actual scientific investigation, both conceptual framework and empirical discovery are continuously revised, and inform each other. However, we have not written our book this way. Instead, we begin with some of the foundations for a science of emotion (chapter 2) — what kinds of ontological and epistemological commitments it requires, what kind of structure an explanation takes — and then work our way toward a list of features or properties of emotions (chapter 3), which then finally are the things we look for, and discover, through empirical research (chapters 4–9). We return to the foundations and the questions again in chapters 10 and 11 by contrasting our views with those of others, and by suggesting some experiments for the future.

Emotions According to Inside Out

What is it about emotions that we would like to understand? And what do we think we understand, but in fact don't (or are mistaken about)? Because emotions are ubiquitous in our lives, and integral to our experience of the world, it is dangerously easy to come up with simplistic views that do not stand up to closer scrutiny, and instead impede scientific progress because they create "the illusion of knowledge."

The film Inside Out, which won the 2016 Academy Award for Best Animated Feature, as well as a Golden Globe, provides a good example of many common but incorrect assumptions about emotion. As you watch the film, you get a fanciful view of how emotions are supposed to work inside a twelve-year-old girl, how those emotions are supposed to be integrated with memory and personality, and how they are supposed to be expressed as behavior. If Inside Out's view of emotion were right, you would be tempted to conclude that we understand an enormous amount about how emotions work — and, more generally, about how the mind and brain work. But Inside Out's view of how emotions work is wrong. In examining what, exactly, is wrong with it, we can highlight some of the gaps in our current understanding of emotion. If you've seen the film and you already find the view of emotion portrayed by Inside Out silly, you are ahead of the game — but bear with us as we use it as an example for uncovering problematic beliefs about emotion.

Inside Out's view of emotion takes as its starting premise the idea that all our emotions boil down to a few primary ones: in the film, they are joy, anger, fear, sadness, and disgust. These five emotions are animated as different characters, charming little homunculi that live in the brain of the little girl and fight with each other for control of her behavior and mental state. These homunculi sit at a control panel and watch the outside world on a screen. They react to the outside world, and in response they manipulate levers and switches that control the little girl's behavior. They are also affected by memories that are symbolized by transparent marbles; moreover, a series of theme parks provide a mental landscape symbolizing different aspects of the girl's personality. The five emotion characters fight over access to the memory marbles and struggle to keep the girl's theme-park attractions open for business.

From the film's point of view, the five emotions are the dominant force controlling the little girl's thoughts, memories, personality, and behavior; thinking, reasoning, and other cognitive activities are relegated to a sideshow. Truly, the little girl is an entirely emotional being. These details of the movie may not represent the way you think about emotions, but they characterize how many people do.

So what's wrong with the film's creative, engaging metaphor? Let's unpack a few of the key ideas about emotions that Inside Out showcases, highlight the errors in their underlying assumptions, and try to articulate the scientific questions that they raise. Although science may not yet have the answers, the exercise will help us frame the issues.

Idea 1. There are a few primary emotions. The prevailing view, enshrined in many psychology textbooks, is that there is a small set of "primary" or "basic" emotions: as we already mentioned, these are joy, anger, fear, sadness, and disgust, according to Inside Out. Different scientific emotion theories offer a big range in the number of basic emotions — anywhere from two to eleven! A second type of emotion is often called "social" or "moral" emotion and typically includes shame, embarrassment, pride, and others. These social emotions are thought to be more essentially tied to social communication than the basic emotions are. But although there are multiple schemes, many classic emotion theories tend to share the idea of a fixed, and relatively small, set of emotions that correspond to the words we have for emotions in English.

The idea of a small set of basic emotions was most notably introduced by the psychologist Paul Ekman, based largely on data from his studies of emotional facial expressions in humans. Ekman argued that facial expressions of basic emotions can be recognized across all human cultures (Ekman 1994); he studied them even among tribes in New Guinea. Ekman's set of basic emotions includes happiness, surprise, fear, anger, disgust, and sadness (although contempt is also sometimes included). The neurobiologist Jaak Panksepp similarly proposed a set of basic emotions, derived from his observations of animal behavior: seeking, rage, fear, lust, care, panic, and play (Panksepp 1998). These emotion theories have much to recommend them and stimulated entire lines of important research. But they also suggest two questionable background assumptions (which Ekman and Panksepp themselves may or may not have held).

Questionable assumption 1: Emotions (at least the "primary" ones) are irreducible. A presumption that often accompanies the idea of a small set of primary emotions is that they are irreducible units. According to this assumption, emotions like "fear" or "anger" cannot be broken down into further components that are still emotional. The psychologist Lisa Feldman Barrett has argued strongly against this assumption, pointing out that it requires belief in some kind of mysterious "essences" of emotions — the belief that there is something irreducible that makes each primary emotion the emotion that it is (Feldman Barrett 2017a). This central assumption underlies the representation of each of the primary emotions in Inside Out as a distinct character. "Joy" and "fear" do not merge with each other; they are each unique individuals. They have stable, fixed identities and functions, and do not share components (for example, in the movie's metaphorical language, they do not share internal organs, limbs, and such).

Yet there is scant scientific evidence that "joy," "fear," or "anger" are irreducible and do not share component parts. Equally plausible is an alternative view in which each of these emotions is made up of a collection of components, or building blocks, some of which are shared by other emotions. Initial doubts such as these lead to the following set of scientific questions that can serve as a starting point for further investigation:

"Are different emotion states composed of features or dimensions that are shared, to variable extents, across multiple emotions? Are some emotions composed of, or based on, combinations of other more basic emotions?"

Questionable assumption 2: the primary emotions correspond to those for which we have names in English.

Related to questionable assumption 1 is the idea that words like "happiness," "fear," "anger," and so forth in fact pick out scientifically principled categories of emotion. It is easy to see why this is unlikely to be the case. For one, we had these words for emotions long before there was any science of emotion — so why would one expect them to align well with scientific emotion categories? For another, different cultures have different words for emotions, and many of these turn out to be extraordinarily difficult to translate. In German, the word "Schadenfreude" denotes the emotion we feel when we feel happy about somebody else's misfortune. Should that be a primary emotion, just because there's a common word for it in German? There are many more such examples, entertainingly cataloged in Tiffany Watt Smith's book, The Book of Human Emotions (Smith 2016). This poses some important scientific questions:

"How should we taxonomize emotions? How many emotions are there, and what names should we give to them? Are there different emotions in different cultures? Are there different emotions in different species? Can we use a word like 'fear' to refer to the same type of emotion state in a person, a dog, and a cat? How and when in evolution did emotions first arise, and how did they diversify?"

Given how little we yet know about these questions, and given that there are good reasons to believe our current emotion categories ("happiness," "sadness," and such) will need to be revised, we will say little in this book about specific emotions. We will refer to some emotions (notably "fear") by way of example. And we will sketch how a future science of emotion might give us better categories or dimensions by which to taxonomize emotions. But this book is primarily about emotions in general, not about specific emotion categories.

Idea 2. Emotions are rigidly triggered by specific external stimuli. In the film Inside Out, all five emotion characters sit lazily around the control panel watching a screen that projects the outside world into the little girl's mind, and are aroused into action only when an appropriate stimulus or circumstance appears. In the film, some stimuli do not activate a given emotion at all (for example, the "anger" character often sits dozing in his chair and does not react unless something maddening happens to the girl), while other stimuli activate multiple emotions. If the depiction from the film were accurate, we could easily figure out the emotion states of other people (and presumably other animals) by a straightforward list of rules that link specific stimuli to specific emotions in a characteristic and inflexible manner. This picture assumes that emotions are far simpler and more automatic than we in fact now know them to be. According to Idea 2, emotions would be just like reflexes. Some things will make you happy, others will make you sad, and some will trigger a specific mix of emotions, according to a set of rules.

Questionable assumption 3. Emotions are like reflexes. The movie gets it right that emotions are often triggered by stimuli in our surroundings. But what determines which emotions are triggered by which stimuli and under which circumstances? Why would seeing a dog trigger only a minimal emotional response in some people, and strong fear or happiness (emotional responses of opposite valence) in others? What accounts for the extraordinary flexibility with which many different stimuli, depending on the context and depending on the person, can elicit emotions? One can pose the following scientific questions:

"What determines whether an external stimulus will evoke an emotion or not, and what determines the kind of emotion evoked? What role do development and learning play in determining an organism's response to a given stimulus? How does this process differ from simpler stimulus-response mappings, such as a reflex?"

Idea 3. Emotions control our behavior. The film portrays the emotion characters as controlling the little girl's behavior by operating joysticks on the control panel. The little girl is but a hapless puppet, with emotions determining her behavior. This central visual metaphor encapsulates the title of the movie: our behavior is controlled, from the "inside out," by our emotions. This feature is the counterpart to 2 above, with respect to the behavioral output rather than the stimulus input.

Questionable assumption 4. Specific emotions cause fixed and specific behaviors. Our subjective experience of emotion leads to the intuition that our emotions cause our behavior: I cry because I feel sad. Yet not all emotion theorists agree with this assumption. Indeed, the nineteenth-century American psychologist William James argued, counterintuitively, that emotions are a consequence, not a cause, of behavior: I feel afraid because I run from the bear, I do not run because I feel afraid (James 1884). Yet James already had doubts that just observing bodily reactions was sufficient to identify specific emotion categories. If it were true that specific emotions cause fixed and specific behaviors, we could infallibly deduce a person's emotions just from watching their behavior. If so, then taken together with questionable assumption 3, we wouldn't need emotions at all to explain behavior, there would simply be a set of rules linking stimuli to behavior. That was the view that behaviorism advocated in the earlier twentieth century. One reason for the demise of behaviorism was that people realized that mappings from stimuli to behavior were far too complicated, and too dependent on context, inference, and learning, to be formulated as rules. Emotions, in our view, are internal states that afford a flexible mapping to behavior, as we will detail throughout this book. This leads to the following scientific questions:

"Do internal emotion states cause behavior, or are they merely an accompaniment to behavior? Or might emotions actually be a consequence of behavior? What exactly are the causal links between stimuli, emotions, and behavior? How could we identify emotions in the absence of behavior? After all, we can be angry without punching somebody or showing any other easily detectable behavior."

Idea 4. Different emotions are located in different, discrete brain regions. The beguiling picture of emotions as walking, talking cartoon characters in Inside Out is closely aligned with the belief that different emotions must correspond to anatomically distinct modules in the brain. Is there a place in the brain for fear, for example? This is a question that has received a lot of attention, including serious scientific investigation!

(Continues…)

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Table of Contents

List of Illustrations ix

Preface xi

Acknowledgments xv

Part I Foundations

Chapter 1 What Don't We Know about Emotions? 3

Emotions According to Inside Out 4

Toward a Science of Emotion 13

Emotions Are Decoupled Reflexes 18

Questions We Will Not Answer in This Book 23

What Do We Want to Know about Emotions? 25

Chapter 2 A Framework for Studying Emotions 29

Warm-Up: Neuroscience Questions about Emotion 30

Toward a Functional Definition of Emotion 39

Proper Functions and Malfunctions 43

Emotions and Consciousness 49

An Experimental Example 52

Summary 57

Chapter 3 Building Blocks and Features of Emotions 58

Building Blocks versus Features 62

A Provisional List of Emotion Properties 65

Summary 98

Part II Neuroscience

Chapter 4 The Logic of Neuroscientific Explanations 103

Levels of Biological Organization 105

The Concept of Mechanism in Neuroscience 108

Testing Causal Relationships between Neural Activity and Behavior 114

Levels of Abstraction 115

Mixing of Terms in Neuroscience Explanations 120

Necessity, Sufficiency, and Normalcy 123

Summary 125

Chapter 5 The Neurobiology of Emotion in Animals: General Considerations 127

Why Do We Need Studies of the Neurobiology of Emotion in Animals? 131

What Do We Want to Understand about Emotion by Studying Animals? 140

The Relationship of Emotion States to Motivation, Arousal, and Drive 143

Psychiatric Drugs, Animal Models, and Emotions 153

Summary 159

Chapter 6 The Neuroscience of Emotion in Rodents 161

Emotion, Fear, and the Amygdala 163

Innate Defensive Behaviors and Emotions 179

Distributed versus Localized Emotions in the Brain 188

Anxiety 189

Other Emotion States: Aggression and Anger 193

Positively Valenced Emotion States 195

Summary 196

Chapter 7 Emotions in Insects and Other invertebrates 197

Learned Avoidance Behavior in Drosophila 198

Does Drosophila Have Emotion States? 203

Anxiety in Insects and Other Arthropods 208

Emotion States and Social Behavior in Insects 209

Internal States in Other Invertebrates 210

Summary 214

Chapter 8 Tools and Methods in Human Neuroscience 215

Historical Neuroscience Studies of Emotion in Humans 218

fMRI Studies of Emotion: The Method 233

Similarity Analyses 242

fMRI in Animals? 245

Summary 249

Chapter 9 The Neuroscience of Emotion in Humans 251

fMRI Studies of Emotion: The Logic and the Challenge 251

Lessons from Two Examples: Music and Faces 253

Attributing Emotions to Others 257

Imaging Emotion Concepts 260

Feeling Emotions 265

Central Emotion States 270

Dissociating Emotion States from Concepts and Experience 273

Summary 278

Part III Open Questions

Chapter 10 Theories of Emotions and Feelings 281

The Structure of Affect 282

Theories of Feelings 286

Philosophy of Emotion 299

Taking Stock 303

Summary 306

Chapter 11 Summary and Future Directions 308

The Main Points of This Book 308

Feelings Again 311

Future Experiments 313

Glossary of Terms and Abbreviations 327

References 337

Index 347

What People are Saying About This

From the Publisher

"It is not possible to comprehend biological evolution without factoring in emotions and related phenomena. Adolphs and Anderson, who have built their respective reputations on the study of human and animal emotions, have written the best and most comprehensive text yet on the subject. This is an indispensable book."—Antonio Damasio, author of The Strange Order of Things: Life, Feeling, and the Making of Cultures

"Adolphs and Anderson have written a blueprint for a modern science of emotion in mice and men."—Rebecca Saxe, Massachusetts Institute of Technology

"Tight and transparent logic threads through this entire book, yielding not only a compelling story but also authoritative science. On the topic of emotion, the book is unsurpassed in its breadth of coverage, depth of expertise, exposition of methods and techniques, and unfailingly good scientific sense. An agenda-setting discussion."—Patricia Churchland, author of Braintrust: What Neuroscience Tells Us about Morality

"We know a great deal about the science of perception, actions, learning, and memory but know relatively little about the science of emotion. This is why The Neuroscience of Emotion is so welcome. Adolphs and Anderson present a completely new understanding of how emotions work and why they are so important for everyday life. Their book is the best treatment of the biology of emotion and a must-read for anyone interested in the brain and behavior."—Eric Kandel, Nobel Prize-winning neuroscientist and author of The Disordered Mind: What Unusual Brains Tell Us About Ourselves

"Emotions have moved from obscurity to daylight, not only in psychology, but also in neuroscience. This accessible book offers the perfect introduction to the emotions of both humans and animals. It keeps feelings separate from bodily expressed emotions, and questions many common assumptions while offering a path to a truly scientific approach."—Frans de Waal, author of Are We Smart Enough to Know How Smart Animals Are?

"This timely and thought-provoking book provides excellent analysis of neuroscience and psychology studies of emotions in humans and animals, and connects the two domains in an original and engaging way. The Neuroscience of Emotion brings sophisticated concepts and cutting-edge techniques to the discussion."—Kent Berridge, University of Michigan

"The Neuroscience of Emotion argues that studying how emotions are implemented in the brain can offer a deeper understanding of their functions. Written by two major leaders in the field, this fantastic and rigorous book will influence many students and researchers."—Luiz Pessoa, University of Maryland

Editorial Reviews

"The sparsity of clear or robust answers spurred neuroscientists Ralph Adolphs and David Anderson to frame an integrated science of emotion. The result is scholarly, lucid and pertinent to both neurobiology and psychology."—-Barb Kiser, Nature

"There is a tight logic running throughout The Neuroscience of Emotion that integrates theories of emotions, recent studies, and commonsense analogies. . . . Adolphs and Anderson openly acknowledge that they do not provide a comprehensive theory of emotion. Indeed, despite the existence of substantial research on the subject, we are left with the impression that we actually know remarkably little about emotions at present. But their enthusiasm for the topic is genuine and makes The Neuroscience of Emotion compelling and engaging."—-Elizabeth Bauer, Science

"Their analysis is authoritative and unsurpassed in its intricate examination of the field. It is also fluent, but don’t expect a frolic: this is a commanding textbook for scientists and students."—-Helen Thomson, New Scientist

"This is an important, agenda-setting and clearly written book that should now be an essential starting point for the science of emotions."—-Shane O'Mara, Times Higher Education

From the Publisher