A book that fundamentally changes how neuroscientists and psychologists categorize sensations and understand the origins and significance of human feelings
How Do You Feel? brings together startling evidence from neuroscience, psychology, and psychiatry to present revolutionary new insights into how our brains enable us to experience the range of sensations and mental states known as feelings. Drawing on his own cutting-edge research, neurobiologist Bud Craig has identified an area deep inside the mammalian brain—the insular cortex—as the place where interoception, or the processing of bodily stimuli, generates feelings. He shows how this crucial pathway for interoceptive awareness gives rise in humans to the feeling of being alive, vivid perceptual feelings, and a subjective image of the sentient self across time. Craig explains how feelings represent activity patterns in our brains that signify emotions, intentions, and thoughts, and how integration of these patterns is driven by the unique energy needs of the hominid brain. He describes the essential role of feelings and the insular cortex in such diverse realms as music, fluid intelligence, and bivalent emotions, and relates these ideas to the philosophy of William James and even to feelings in dogs.
How Do You Feel? is also a compelling insider's account of scientific discovery, one that takes readers behind the scenes as the astonishing answer to this neurological puzzle is pursued and pieced together from seemingly unrelated fields of scientific inquiry. This book will fundamentally alter the way that neuroscientists and psychologists categorize sensations and understand the origins and significance of human feelings.
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How Do You Feel?
An interoceptive moment with your neurobiological self
By A. D. (Bud) Craig
PRINCETON UNIVERSITY PRESSCopyright © 2015 Princeton University Press
All rights reserved.
AN INTRODUCTION TO INTEROCEPTION
How do you feel?
That's a familiar question that we hear every day. If I pause to examine my feelings now, at this moment, the very first observation I have is that I'm having lots of ongoing feelings. My feelings include several about my recent interactions with others, a few about my walk up the hill and my plans for the coming weekend, and recurrent feelings about my current goals, about writing this book, and about the ideas I want to share with you. I am also experiencing feelings that relate neither to the past nor the future, but rather to the immediate present. I have feelings about this room, about the lighting, and about the items I see nearby (my lunch!). I have feelings coming from different parts of my body, and I have affective or emotional feelings, mood feelings, which are constantly ongoing and which color everything. Emotional feelings extend across several timescales and occasionally become very strong, episodic, and maybe even overwhelming.
I'm sure you can describe your feelings similarly. We share a commonsense view of what feelings are. It is based in part on what our parents taught us. In the same way that they taught us what color belongs to the word "red" (regardless how it actually looks to you), they taught us what the word "hot" means by teaching us to associate the word "hot" with a particular sensation coming from our fingers, and they taught us what the word "angry" means by associating the word "angry" with the way they were behaving at the time, or the way you were behaving. Each one of us has exclusive access to our own subjectively experienced feelings, yet we humans share a common understanding of feelings that is based on language, culture, and empathy. At the core of our common understanding of feelings is a set of specific behaviors and facial expressions that are cross-cultural and biologically characteristic of our human species, which importantly are associated with specific feelings and emotions.
Nevertheless, we do not have a genuine understanding of what a "feeling" is or how we experience a feeling. In the dictionary, we find that the word "feel" in English has several different meanings. There are feelings of touch; so, I can say that I feel the keys as I type, or I can say how rough or smooth an object feels. I regard these as discriminative tactile sensations; a feeling is something deeper and more complex. As the dictionary tells us, the word "feel" can also have an indirectly tangible reference; I can describe the "feel" of a piece of cloth in my hand or a wine in my mouth or the air outside. I can also say that I feel the temperature of objects I touch, as in, "I can feel that the cup is hot." Notably, that usage can even be shortened by projection to the external object, as in, "the cup feels hot."
Emotional feelings, though, are even less tangible and more ephemeral. If I tell you how I feel or ask how you feel, we are referring mainly to our subjective personal feelings. Our personal feelings are of two kinds. First, there are the feelings that come from our bodies—I can say that my arm hurts or that my feet feel cold. Second, there are affective feelings that relate our moods, dispositions, and emotions—I can say that I feel happy or I feel sad. Affective feelings are of course what most people relate when they describe their feelings. "I feel anxious," or "I feel good today!"
Now when we say either of those expressions, we are referring not just to emotional feelings; we are referring also to how our bodies feel. Our descriptions of affective feelings in general seem to be associated with the body; we say that feelings come "from the heart" (as Aristotle taught), or we talk about "gut feelings" (which some equate with intuition). In fact, when we share our feelings, we don't use only words; we use tone of voice (prosody), facial expressions, and body language. Our emotions are expressed by our bodies, and we feel that.
So it makes sense to regard feelings from the body as the most primal feelings. We feel them all of the time, and they underlie most of our emotional feelings, if not all. The most basic feelings from the body represent aspects of its physical condition. Do I feel hungry or thirsty? Am I warm enough, or do I feel a chill? Does the small skin wound on my arm that is still healing itch or burn? Or, does the chair feel comfortable—which actually means, are my muscles and joints complaining about my physical position? In addition, I can feel less direct aspects of my body's physiological condition, such as, How much energy do I have? or, Am I overheated? or, Do I need a breath of fresh air?
Such feelings from the body that signal its condition are the basis for what some call "the material me," or what was called Gemeingefühl in the German literature of the nineteenth century (which literally means "common sensation"). There is a marvelous review of that literature in a chapter written by the preeminent British neurophysiologist Charles S. Sherrington, entitled "Cutaneous Sensations," in Schäfer's Textbook of Physiology (1900); when I first read it, I couldn't help imagining him seated at a long library table, writing in longhand under the pale light of tall windows and gas table lamps, as his thoughts flowed and, day by day, his synthesis slowly developed. Unfortunately, in his final analysis, he discarded the concept of common sensation. Yet my research showed that primates have a sensory pathway to the forebrain that represents the physiological condition of the body, a sensory capacity for which I redefined the term interoception.
The word "interoception" was coined by Sherrington (who received the Nobel Prize in 1932 for his studies of the motor system and the spinal cord) to refer to sensations from the interior of the body, especially the viscera. He differentiated interoception conceptually from exteroception (sensory inputs activated from outside of the body), proprioception (sensory inputs that relate limb position), teloreception (sensory inputs activated from a distance, i.e., vision and audition), chemoreception (taste and smell), thermoreception (temperature), and nociception (sensory inputs activated specifically by physically damaging or threatening stimuli, which cause specific motoric reflexes that Sherrington measured; a term also coined by him). He categorized nociception and thermoreception together with the sense of touch as aspects of exteroception, because he regarded all three as discriminative cutaneous sensations. Sherrington's codification underlies the conceptual organization of all modern neuroscience textbooks; they don't include the concept of common sensation because Sherrington didn't.
Like Sherrington, virtually all previous authors thought of sensations from the skin as exteroceptive sensory inputs activated from outside of the body, but my findings underlined the accumulated evidence indicating that most sensory receptors in the skin that have small-diameter fibers (or, axons) and cell bodies actually signal the condition of the tissue itself. The skin is the largest organ of the body, and it has very important functions for homeostasis, the continually ongoing process that maintains the health of the body (see chapter 2). For example, the skin is critical for water and electrolyte balance, thermoregulation, and vitamin D production. In the same manner, small-diameter sensory activity from muscle signals workload (energy use), metabolite concentrations, and vascular distension, in addition to physical conditions like mechanical distortion and temperature. As with the sensory input from the viscera, the small-diameter sensory inputs from skin and muscle (and from all other tissues of the body, including bone) provide the continuous flow of sensory information required for homeostatic control of ongoing changes in blood flow and respiration, that is, the control of smooth muscle. In contrast, the sensory fibers from skin that have large-diameter axons and cell bodies signal mechanical contact with external stimuli (pressure, velocity, stretch, vibration frequency), and those from muscle and joints signal changes in force, length, and position, all of which are important for guiding movements produced by skeletal (striated) muscle. Though not described in textbooks, this fundamental distinction provides the only sensible explanation for the presence of two completely separate anatomical pathways for ascending sensory activity, the dorsal column–medial lemniscal and the spinothalamic pathways, and for the presence of two morphologically separable regions in the sensory-processing portion of the spinal cord (i.e., the dorsal horn) that differentially process large-and small-diameter sensory input (described in chapters 2 and 3); in both cases, the first one serves exteroception and the second serves interoception. My research demonstrated that there is also a distinct interoceptive cortex, which contains the primary cortical representation for both thermoreception and nociception (see chapter 5); this finding substantiates the fundamental neurobiological distinctness of interoception. As explained in chapter 3, modern genetic analyses of the evolutionary origins of the vertebrate nervous system show that these two morphological/functional neural systems are produced by two distinct gene regulatory networks that have ancient sources.
Thus, one of the conceptual advances from my research is the enlargement of the term interoception to include small-diameter sensory input from the whole body—not only from viscera, muscle, joints, and teeth, but also from skin. This concept of interoception includes the idea of common sensation. And in this conceptual framework, nociception and thermoreception are aspects of interoception, not exteroception, because they report aspects of the physiological condition of the body conveyed by small-diameter sensory fibers and the spinothalamic pathway to the interoceptive cortex. The research described in this book demonstrates that feelings of pain and temperature are based on activity in body maps that occupy specific portions of interoceptive cortex.
Of course, the reason that thermoreception and nociception were so easily categorized as exteroceptive cutaneous sensations is that we have a spatial and intensive discriminative capacity in both modalities that closely resembles the discriminative capacity of cutaneous mechanoreception. We readily refer such thermal and noxious cutaneous sensations to a causative external stimulus, ignoring the fact that the sensations actually report the condition of the skin itself. That certainly confounds this fundamental conceptual shift. But all thermoreceptors and nearly all nociceptors in the skin can be activated either by an exogenous or an endogenous change in conditions; in contrast, cutaneous mechanoreceptors can be activated only by an externally applied force. For example, the skin can be rapidly cooled by a reduction in blood flow caused by autonomic vasoconstrictors, which the small-diameter thermoreceptors immediately signal; in fact, providing feedback for thermoregulation is their original and primary function. Similarly, nearly all peripheral receptors that are categorized as "nociceptors" can be activated by changing metabolic conditions in the skin, such as the pH changes and chemicals associated with inflammation (e.g., interleukin-1-beta) or with ectoparasites (e.g., mosquito bites). In contrast, the large-diameter mechanoreceptor sensory terminal that enwraps the base of a hair follicle is activated only when the hair is flicked sufficiently quickly by contact with an external object.
Nevertheless, our primate brains clearly enable interoceptive activity to be used for discriminative sensation. Furthermore, modern evidence indicates that some cutaneous nociceptors have sensory terminals in the exterior part of the skin, large-diameter fibers that are fast-conducting, and a central terminal branch that targets spinal interneurons which drive skeletal muscle reflexes; these certainly fit the Sherringtonian concept of a nociceptor. Another small subset signals graded sharpness, regardless whether it feels painful or not. Both of these receptors can be described as serving exteroception rather than interoception. However, these exceptional elements still share the basic morphological, chemical, and genetic properties that differentiate the interoceptive fibers, and they drive ascending spinothalamic axons that activate interoceptive cortex. In other words, they belong to the category of interoceptive fibers that represent the physiological condition of the body. (See box 3 for discussion of this issue.)
More generally, our perceptions of natural stimuli are always based on the central integration of activity across the various available sensory channels, and furthermore, as explained in this book, to my mind any sensation must be transformed to a feeling in order to be "felt," or experienced in subjective awareness. The model of interoceptive integration described in chapters 5–7 can explain how all types of sensory and neural activity generate feelings that are used to guide behavior.
* * *
The idea that we can feel the condition of all of the tissues of our bodies might be intuitively clear to you because we are all familiar with these feelings. Everyone I have met or know of (other than certain patients) can describe the most basic feelings from her/his body, like whether she or he feels warm or cool, hungry or thirsty, or how much something hurts, and whether the source is skin, muscle, or joint tissue. These feelings depend on the small-diameter sensory fibers from all tissues of the body and the interoceptive sensory pathway in the brain.
There is a wealth of experimental evidence demonstrating the deep significance of bodily feelings for human performance. The following paragraphs highlight some of this evidence. (The citations for these findings are all provided in the bibliography at the end of this book.)
As individuals, we each have a different capacity for so-called bodily awareness. Bodily awareness has been called interoceptive awareness by investigators interested in the effects of cardiorespiratory or visceral sensory activity on human mood, emotion, and performance. The feeling of heartbeat awareness is a quantifiable capacity that is often used as a measure of the capacity of individuals for interoceptive awareness. Heartbeat awareness can be measured by asking a person to count the number of heartbeats she or he feels in objectively timed intervals of 30, 45, and 60 seconds, and comparing those numbers to real counts obtained from an electrocardiogram (ECG) recording or a finger pulse oximeter. Alternatively, one can use the ECG or pulse oximeter signal to drive a tone generator and produce a short series of single beeps that are either in time with the heartbeat or are out of time by being delayed half of one second. The participant is asked to determine whether the tones are in time or delayed across repeated trials. In the latter paradigm, a control for each participant's attention can be obtained by using a similar short series of tones, varying one and asking the participant to report whether they are all the same or not. [Cameron, 2001; Schandry, 1981; Wiens, 2005]
Heartbeat awareness varies widely across individuals; it is not an all-or-none characteristic. It is used as a generalized index for interoceptive awareness, although there are only two relevant reports, both of which found that heartbeat awareness correlates with gastric sensitivity (this issue certainly needs more work). It may be related to particular cardiodynamic parameters. An individual's heartbeat awareness score also correlates with that individual's self-reported sense of bodily awareness and with her or his sensitivity to pinch and ability to tolerate a maintained painful stimulus. Importantly, an individual's heartbeat awareness score also correlates with that individual's ratings of the intensity of her or his own emotional feelings, whether positive or negative. Better heartbeat perceivers are better at reading their own emotional feelings, and subjects who are better at reading their own feelings are better at reading others' emotional feelings. [Whitehead and Drescher, 1980; Herbert et al., 2012; Schandry et al., 1993; Herbert and Pollatos, 2012; Pollatos et al., 2007b, 2012]
Those observations fit with the idea that the cortical processes that enable us to feel the interoceptive feelings of the body's condition also provide the basis for our awareness of emotional, social, and all other feelings. As described in this book, there is now plenty of evidence for this concept (see chapters 2 and 7). The detailed physiological and functional imaging findings on heartbeat awareness provide direct insights into the fundamental role of interoception in human feelings, and they directly corroborate the identification of a particular portion of and they directly corroborate the identification of a particular portion of our brains, the anterior insular cortex, as an essential site for our awareness of feelings. The distinct sensory pathway to the interoceptive cortex in primates that my research identified provides the substrate not only for the affective feelings from the body that we humans experience, but also for the interoceptive foundation of emotion that psychologists and psychiatrists have long envisioned. [Critchley et al., 2004; Pollatos et al., 2007a, 2007b; Craig, 2002]
Excerpted from How Do You Feel? by A. D. (Bud) Craig. Copyright © 2015 Princeton University Press. Excerpted by permission of PRINCETON UNIVERSITY PRESS.
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Table of ContentsList of Figures and Plates ix
List of Boxes xi
1AN INTRODUCTION TO INTEROCEPTION 1
2FEELINGS FROM THE BODY VIEWED AS EMOTIONS
Ideas from the lamina I projection map that add to the textbooks 16
An overview of the map 16
The central neural substrates for homeostasis 19
Textbook knowledge regarding touch 23
Textbook knowledge regarding pain and temperature 28
Irritating incongruities 31
Identification of the thermosensory pathway 33
Recognizing that temperature sensation is part of interoception 38
Viewing a thermosensory feeling as a homeostatic emotion 42
Thermal sensations become subjective feelings 45
Emergent ideas about feelings, moments, music, and time 46
Bivalent emotions in bicameral brains 50
3THE ORIGIN OF THE INTEROCEPTIVE PATHWAY
Homeostatic sensory fibers and the interoceptive dorsal horn 54
Finding lamina I spinothalamic neurons 55
Lamina I spinothalamic neurons are "labeled lines 62
Anomalous characteristics point to a new direction 71
Integrated lamina I activity generates thermoregulatory pain: the thermal grill 74
Identifying lamina I projections to autonomic neurons 82
Demonstrating that lamina I subserves homeostasis 90
The identification of homeostatic small-diameter sensory fibers 94
The development of the interoceptive dorsal horn 97
The interoceptive dorsal horn subserves homeostasis 101
The evolutionary origin of interoceptive and exteroceptive neurons 103
The homeostatic sensory system provides crucial vasoreceptive feedback 106
4INTEROCEPTION AND HOMEOSTASIS
Lamina I terminations at cardiorespiratory sites in the brainstem 111
An overview of lamina I projections to the brainstem 112
Lamina I terminations in the lower brainstem (medulla) 115
Lamina I terminations in the middle brainstem (pons) 118
Lamina I terminations in the parabrachial nucleus 119
Lamina I terminations in the periaqueductal gray (upper brainstem) 124
5THE INTEROCEPTIVE PATHWAY TO THE INSULAR CORTEX
Lamina I spinothalamic input to the thalamus and cortex in primates 130
My introduction to functional neuroanatomy 131
The significance of somatotopic organization 133
The lateral spinothalamic tract 134
Finding Waldo 135
The functional anatomical characteristics of the VMpo in the macaque monkey 139
The projection from the VMpo to the dorsal posterior insula in the macaque monkey 145
The organization of the dorsal posterior insula in the macaque monkey 150
The interoceptive pathway 155
The human VMpo 160
The human dorsal posterior insula 166
The human interoceptive cortex 170
Interoceptive touch 173
Summary, and an interoceptive perspective on cortical gyrification 175
6BODILY FEELINGS EMERGE IN THE INSULAR CORTEX
Interoceptive integration generates the feeling of being alive 182
The structure of the insular cortex 183
Posterior-to-mid-to-anterior processing of interoceptive activity 185
Multimodal integration in the mid-insula 188
Feelings from the body emerge first in the mid-insula 191
Homeostatic sentience 194
Interoceptive integration improves energy efficiency 197
The model of interoceptive integration and the generalization of feelings 199
Interoceptive feelings come to awareness in the anterior insula 203
Emotional feelings emerge and come to awareness in the anterior insula 206
The embodiment of emotional feelings 209
7FEELINGS ABOUT THOUGHTS, TIME, AND ME
Awareness emerges in the anterior insular cortex 216
The AIC is activated during cognitive activity 219
The model: Integration of cognitive feelings 221
Evidence that awareness is engendered in the AIC 223
Evidence that the AIC supports feelings about time 226
The model: Cinemascopic integration of moments of time 228
The model: The structural basis of awareness 235
The role of the AIC in the control of network activity 243
Evidence that the AIC is crucial for fluid intelligence 247
Evidence that the AIC optimizes energy utilization 249
Individual variability and maturation 251
Distorted feelings produce mental illness 254
8FEELINGS AND EMOTIONS ON BOTH SIDES OF THE BRAIN
The asymmetric forebrain 257
Ethological evidence of forebrain asymmetry 260
Neuroanatomical evidence of forebrain and AIC asymmetry 262
Clinical evidence of forebrain and AIC asymmetry 263
Physiological evidence of forebrain and AIC asymmetry 265
Psychophysiological evidence of forebrain and AIC asymmetry 267
Two recent reviews uncover asymmetric activation of the amygdala and the AIC 270
The alignment of autonomic, behavioral, and affective control 272
Opponent inhibition 274
Specialization and balance 275
And something curious 277
9A FEW MORE THOUGHTS ABOUT FEELINGS
Graded sentience and tail-wagging in dogs 280
A quick review 280
Scaling up homeostatic sentience 285
Graded sentience 289
Feelings in dogs 293
How about Watson? 295
Reference List 309
Illustration Credits 337
What People are Saying About This
"This fascinating book is truly a must-read for anyone interested in the biological underpinnings of human perception. Craig integrates evidence from neuroscience, psychology, and psychiatry to present new insights into how our brains enable us to experience the range of sensations and mental states known as feelings. Readers won't just learn about captivatingly novel findings, but will enormously enjoy the sheer elegance of Craig's thought."Nikos K. Logothetis, Max Planck Institute for Biological Cybernetics"An engaging and uniquely personal perspective on the neurobiology of feelings. One gains a clear, comprehensive, and integrative view of the evolution and future of the field through the lens of a creative neuroscientist and scholar."Helen S. Mayberg, Emory University School of Medicine"In this provocative and deeply creative book, Craig shares his journey of scientific discovery to reveal an insight that is both simple and sweeping: the nervous system contains a sensory pathway that is built for regulating homeostasis, and it functions as a fundamental, organizing feature of the mind. Many of the psychological phenomena that we think of as independent and separatemetabolism, emotion, stress, pain, and time perceptionare all united, in one way or another, by this sensory pathway. After reading this book, you will think differently about the nature of consciousness, and, ultimately, what it means to be human."Lisa Feldman Barrett, University Distinguished Professor of Psychology, Northeastern University"In this engaging book, Craig develops a revolutionary new approach to how we think about emotions. How Do You Feel? provides a compelling and comprehensive view of a major shift in the field. It reflects Craig's almost encyclopedic knowledge, and is an impressive collection and integration of scientific facts."Martin P. Paulus, University of California, San Diego