How Do You Feel? An Interoceptive Moment with Your Neurobiological Self

381 Pages·2014·91.25 MB·English

by  A D (Bud) Craig

HOW DO YOU FEEL?
••

HOW DO YOU FEEL?
••
An interoceptive moment with your neurobiological self
A. D. (Bud) Craig
Princeton University Press
Princeton and Oxford
Copyright © 2015 by Princeton University Press
Published by Princeton University Press, 41 William Street, Princeton, New Jersey 08540
In the United Kingdom: Princeton University Press, 6 Oxford Street, Woodstock, Oxfordshire OX20 1TW
press.princeton.edu
All Rights Reserved
Library of Congress Cataloging-i n- Publication Data
Craig, A. D.
How do you feel? : an interoceptive moment with your neurobiological
self / A.D. (Bud) Craig.
pages cm
Summary: “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-e dge 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 insid-
er’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”—Provided by publisher.
Includes glossary.
Includes bibliographical references and index.
ISBN 978– 0- 691– 15676– 7 (hardback)—ISBN 0– 691– 15676- X (hardcover) 1. Emotions—Physiological
aspects. 2. Affective neuroscience. 3. Neurobiology. I. Title.
QP401.C7 2015
612.8’23342—dc23
2014009903
British Library Cataloging-i n- Publication Data is available
This book has been composed in Charis SIL
Printed on acid- free paper. ∞
Printed in the United States of America
1 3 5 7 9 10 8 6 4 2
Contents
••
List of Figures and Plates ix
List of Boxes xi
Preface xiii
1
AN INTRODUCTION TO INTEROCEPTION 1
2
FEELINGS FROM THE BODY VIEWED AS EMOTIONS
Ideas from the lamina I projection map that add to the textbooks 16
16
An overview of the map
19
The central neural substrates for homeostasis
23
Textbook knowledge regarding touch
28
Textbook knowledge regarding pain and temperature
31
Irritating incongruities
33
Identification of the thermosensory pathway
38
Recognizing that temperature sensation is part of interoception
42
Viewing a thermosensory feeling as a homeostatic emotion
45
Thermal sensations become subjective feelings
46
Emergent ideas about feelings, moments, music, and time
50
Bivalent emotions in bicameral brains
3
THE ORIGIN OF THE INTEROCEPTIVE PATHWAY
Homeostatic sensory fibers and the interoceptive dorsal horn 54
55
Finding lamina I spinothalamic neurons
62
Lamina I spinothalamic neurons are “labeled lines”
71
Anomalous characteristics point to a new direction
74
Integrated lamina I activity generates thermoregulatory pain: the thermal grill
82
Identifying lamina I projections to autonomic neurons
90
Demonstrating that lamina I subserves homeostasis
94
The identification of homeostatic small- diameter sensory fibers
97
The development of the interoceptive dorsal horn
101
The interoceptive dorsal horn subserves homeostasis
103
The evolutionary origin of interoceptive and exteroceptive neurons
106
The homeostatic sensory system provides crucial vasoreceptive feedback
vi •• Contents
4
INTEROCEPTION AND HOMEOSTASIS
Lamina I terminations at cardiorespiratory sites in the brainstem 111
112
An overview of lamina I projections to the brainstem
115
Lamina I terminations in the lower brainstem (medulla)
118
Lamina I terminations in the middle brainstem (pons)
119
Lamina I terminations in the parabrachial nucleus
124
Lamina I terminations in the periaqueductal gray (upper brainstem)
129
Summary
5
THE INTEROCEPTIVE PATHWAY TO THE INSULAR CORTEX
Lamina I spinothalamic input to the thalamus and cortex in primates 130
131
My introduction to functional neuroanatomy
133
The significance of somatotopic organization
134
The lateral spinothalamic tract
135
Finding Waldo
139
The functional anatomical characteristics of the VMpo in the macaque monkey
145
The projection from the VMpo to the dorsal posterior insula in the macaque monkey
150
The organization of the dorsal posterior insula in the macaque monkey
155
The interoceptive pathway
160
The human VMpo
166
The human dorsal posterior insula
170
The human interoceptive cortex
173
Interoceptive touch
175
Summary, and an interoceptive perspective on cortical gyrification
6
BODILY FEELINGS EMERGE IN THE INSULAR CORTEX
Interoceptive integration generates the feeling of being alive 182
183
The structure of the insular cortex
185
Posterior- to- mid- to- anterior processing of interoceptive activity
188
Multimodal integration in the mid- insula
191
Feelings from the body emerge first in the mid- insula
194
Homeostatic sentience
197
Interoceptive integration improves energy efficiency
199
The model of interoceptive integration and the generalization of feelings
203
Interoceptive feelings come to awareness in the anterior insula
206
Emotional feelings emerge and come to awareness in the anterior insula
209
The embodiment of emotional feelings
7
FEELINGS ABOUT THOUGHTS, TIME, AND ME
Awareness emerges in the anterior insular cortex 216
219
The AIC is activated during cognitive activity
221
The model: Integration of cognitive feelings
223
Evidence that awareness is engendered in the AIC
Contents •• vii
226
Evidence that the AIC supports feelings about time
228
The model: Cinemascopic integration of moments of time
235
The model: The structural basis of awareness
243
The role of the AIC in the control of network activity
247
Evidence that the AIC is crucial for fluid intelligence
249
Evidence that the AIC optimizes energy utilization
251
Individual variability and maturation
254
Distorted feelings produce mental illness
8
FEELINGS AND EMOTIONS ON BOTH SIDES OF THE BRAIN
The asymmetric forebrain 257
260
Ethological evidence of forebrain asymmetry
262
Neuroanatomical evidence of forebrain and AIC asymmetry
263
Clinical evidence of forebrain and AIC asymmetry
265
Physiological evidence of forebrain and AIC asymmetry
267
Psychophysiological evidence of forebrain and AIC asymmetry
270
Two recent reviews uncover asymmetric activation of the amygdala and the AIC
272
The alignment of autonomic, behavioral, and affective control
274
Opponent inhibition
275
Specialization and balance
277
And something curious
9
A FEW MORE THOUGHTS ABOUT FEELINGS
Graded sentience and tail- wagging in dogs 280
280
A quick review
285
Scaling up homeostatic sentience
289
Graded sentience
293
Feelings in dogs
295
How about Watson?
Acknowledgments 297
Abbreviations 299
Glossary 301
Reference List 309
Illustration Credits 337
Index 339

List of Figures and Plates
••
Figure 1. The central projection map for homeostatic sensory inputs in the monkey. 14
Figure 2 / Plate 1. The cortical processing of innocuous cool sensory activity. 34
Figure 3. The characteristics of distinct types of lamina I spinothalamic neurons. 64
Figure 4 / Plates 2 and 3. The physiological basis of the thermal grill illusion of pain. 76
Figure 5. The developmental origin of lamina I neurons is exquisitely coordinated
with the arrival of the small- diameter sensory fibers. 98
Figure 6. The interoceptive and the exteroceptive dorsal horns are distinct. 102
Figure 7 / Plate 4. The codistribution of lamina I terminations and catecholamine
neurons in the monkey brainstem. 113
Figure 8. The identification of PHA- L- labeled lamina I spinothalamic terminations in the VMpo. 137
Figure 9 / Plate 5. Calbindin- labeled terminations in the VMpo. 144
Figure 10 / Plate 6. The organization of the insular cortex in the monkey and the human. 149
Figure 11 / Plate 7. The anteroposterior somatotopic organization of laser-e voked potentials
(LEPs) in the macaque monkey. 152
Figure 12 / Plate 8. The anteroposterior somatotopic organization of the human
interoceptive cortex. 167
Figure 13 / Plate 9. The cortical targets of the ascending homeostatic sensory pathway. 179
Figure 14 / Plate 10. Bodily feelings emerge in the bilateral mid- insula. 187
Figure 15 / Plate 11. The posterior- to- mid- to- anterior integration in the homeostatic model. 200
Figure 16 / Plate 12. The activation of anterior insular cortex during particular tasks and
subjective feelings. 205