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Richard J. Davidson
Paul Ekman
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...
roscaence
The Foundations
of Human and
Animal E motions
JAAK PANKSEPP
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39001103267731
OXFORD
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P35
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Panksepp, Jaak.
in my eyes, then,
4. Psychobiology.
5. Psychology, Comparative.
I. Title.
II. Series.
BF531.P35
!56'.24-dc21
1998
98-15955
3579864
Printed in the United States of
on acid-free paper
Amcri c<l
BOGAZi<;:i
UNIVERSITESi
KUTUPHANESi
1 1 1111 1 1111111II
637444
Preface
This book was written with the student firmly in mind, but it is not a traditional textbook. It
is an attempt to clarify the interrelations betWeen brain and mind as expressed in the funda
mental emotional processes that all mammals share. I will explore how our knowledge of
the animal brain can help clarify the affective nature of the human mind and how our ability
to appreciate the basic emotions of the human mind helps us understand the functional or
ganization of the mammalian brain. This borderland of knowledge between the many disci
plines that study the animal brain and the human mind-the various subareas of neuroscience
and behavioral biology and the many schools of psychology and philosophy-should be
rich in intellectual commerce. Unfortunately, this is not so. At present, these disciplines are
only slowly being introduced to each other, like Europe and the Far East a millennium ago,
and xenophobia prevails. Just as the trade routes between those distant cultures were opened
slowly by explorers and adventurers, interchange between the disciplines that view human
nature from above (i.e., the viewpoint of our recently evolved rational and cultural mind)
and those that view it from below (the ancient networks of our brains) remains tortuous and
unsatisfactory. This book offers one view of how the needed trade routes may be constmcted
in the area of emotions and motivations.
A motive of the old explorers was adventure under the guise of economics-the search
for new vistas and knowledge in behalf of what is usefuL The motives that underlie the writing
of this book are the same. The aim is to enrich our knowledge about the brain/mind inter
face, but the more primal motive is the adventure of exploring uncharted spaces. At times,
the conceptual paths of the brain/mind charts presented here will be like the routes on an
cient maps that never really depicted the immensity of the journey. At present, ignorance is
more abundant than knowledge in this field, often forcing me to oversimplify in order to
formulate any coherent ideas and explanations at all. It will be a while before we have a true
and lasting science of emotions as opposed to the fragmentary knowledge that now exists.
But instead of just summarizing a patchwork of existing theories that are endemic in the
field, I will aspire to provide a cohesive map to guide future navigations. We are still in the
early stages of analyzing the psychobiology of emotions, and many additional generations
of careful work will be needed before we have precise maps.
This book is dedicated to a new synthetic psychology of the future that will be more
catholic than the present variants-one that will be built jointly on evolutionary, neuro
scientific, behavioristic, affective, and cognitive foundations. I will attempt to take nature
on its own terms by coming to grips with those intrinsic, ancient processes of the brain/
mind that mediate between environmental events and the natural classes of action tenden
cies that animals spontaneously generate in the real world. The basic premise here is that
the brain is a "symbolic organ" that reflects an evolutionary epistemology encoded in our
genes. The mammalian brain not only represents the outside world in symbolic codes based
on the properties of its sensory-perceptual systems but also has intrinsic operating systems
that govern ingrained psychobehavioral tendencies for coping with those ever-present chal
lenges that our ancestors confronted in their evolution. Many of these operating systems
arouse emotional states, which are probably internallY felt by other animals in ways not that
different from humans. While modern neuroscience has achieved great success in deciphering
viii
PREFACE
the anatonl.ical and physiological substrates of many sensory and motor processes at the
neuronal level, it has made only a modest beginning in deciphering the functional charac
teristics of that "great intermediate net" that intervenes between inputs and outputs. Here, I
advocate the position that many intervening neuropsychological processes, such as the ba
sic emotions, can now be understood in neuroanatornical, neurophysiological, and neuro
chemical terms. But that level of understanding does require more theorizing and utiliza
tion of indirect evidence than is common in the field.
This new, integrative form of psychobiology is still in its early stages. Its development
has been permitted only by the recent growth of neuroscience. The best evidence concern
ing emotional mechanisms has emerged largely from brain research on kindred animals such
as birds, rats, guinea pigs, dogs, cats, and monkeys. Some comes from work on creatures
even "lower" in the evolutionary "bush," arid an ever increasing amount is also now com
ing from studies of humans treated with various psychoactive drugs and hormones, as well
as those with brain damage. We must use many sources of knowledge to reveal the nature
of emotionality-what it really means to feel anger, fear, lust, joy, loneliness, happiness,
and the various other desires and vexations of the human "heart."
In my more optimistic moments, I hope that the lines of evidence summarized here could
serve as a foundation for a "new psychology" that recognizes that the discipline must be
grounded on solid neuroscience foundations. Although psychology can continue to deal with
the loftiest human aspirations, it also must become rooted in the evolutionary realities of
the brain if it is to become a true science. But that metamorphosis will be a difficult one,
since most of what psychologists do is not clearly linked to brain issues. Since few psy
chologists are doing brain research, it is hard to convince them that their thinking should be
premised on a deep respect for and understanding of the organ of the mind. Substantive
neurobiological offerings are still not part of the traditionally mandated curricular require
ment of many psychology programs. All too often the neural facts are offered in such a dry
manner that students shy away from immersion in such materials. My aim here has been to
provide a treatment with a bit more literary merit than may be typical for a book of this
type. I have aimed to maintain a friendly, readable style, in the hope of attracting the atten
tion of many readers who truly wish to appreciate the underlying complexities of the human
mind and to understand how our highest aspirations often remain tethered to the values elabo
rated by ancient parts of our animal brain.
I did choose to cast the present coverage in textbook format, with enough chapters for a
typical semester, divided into convenient thirds. Although this type of course is not yet a
traditional offering in psychology, I hope it will gradually emerge as one for advanced under
graduates and graduate students studying the psychology of emotions and motivations, as
well as neuroscience and behavioral biology students who wish to have an appreciation of
functional processes shared by all mammals. Also, the work will cover issues that should
be essential for related disciplines such as neurophilosophy and biological psychiatry. In
sum, I have tried to write a book for those interested in psychology who wish to know more
about brain matters and for those interested in neurosciences who wish to know more about
psychological matters. I have tried to write in such a way that little neuroscience or psycho
logical background is necessary to follow the story lines. At times, the going may be diffi
cult, especially when it comes to the essential background issues presented in Chapters 46
on neuroanatomy, neurophysiology, and neurochemistry. However, I trust that even the nov
ice will find them reasonably interesting.
I have also sought to keep the lay reader in mind by including enough general material
to make the more detailed materials worthy of continued attention, Many people are inter
ested in gaining a new and better understanding of the evolutionary sources of the human
mind, which must largely be obtained from brain research. Unfotiunately, there are few places
to go to obtain a substantive, yet interesting, coverage of emotional issues. Accordingly, in
this book I have taken a conceptual approach as much as an empirical approach. This is also
reflected in the referencing style, where I have tried to put ideas and carefully selected facts
in the foreground and to leave personalities who have done the hard investigative work, as
well as the myriad research details, in the background. I have used endnotes in preference
to the traditional name-date approach. I mention names only when we encounter the work
of investigators of considerable histOrical importance. However, the author index should
PREFACE
allow effective retrieval of those whose work has been covered. Obviously, there exists much
more raw material to be cited than I have chosen to cover. For instance, I recently received
two reviews on two of the topics covered here, hypothalamic control of feeding and aggres
sion, and each cited more than 1 ,000 original pieces of research. It would have been pos
sible to cite thousands of references for every chapter of the book, but my aim, more than
anything, was to generate a readable text. Thus, my str_ ategy in referencing materials was to
focus equally on review articles and research reports, with a view to maximizing the possi
bility that students could access related materials reasonably efficiently.
I have also tried to sustain a fairly natural style through the explicit recognition that
we humans are storytelling creatures. Our cultural evolution (and perhaps even our cere
bral evolution; see Appendix A) has been guided by aeons of sitting around campfires,
sharing our deepest perspectives about the worlds in which we live. The best teaching
must try to rekindle this spirit around the intellectual campfire of the modern classroom.
Thus, one of my main goals is to encourage a renewed interest in the types of experimen
tal inquiries that can take us toward a substantive understanding of how emotions are
organized in the brain. Unfortunately, in the present scientific climate (where we often
reward knowing more and more about less and less), there is remarkably little integrative
work by active investigators in the field and remarkably little work on the psychobiology
of emotions. Brain scientists are typically unwilling to use mentalistic words in discuss
ing their empirical findings, and psychologists, because of their lack of training in the
neurosciences, are typically unable to link their psychological concepts to brain functions.
The present effort is based on the assumption that our ability to pursue such linkages,
first verbally and then empirically, is essential for future scientific progress in understand
ing emotions. Accordingly, I have used the unusual literary device throughout this book
of labeling major emotional systems in folk-psychological terms, using capitalized let
ters to highlight that I am focusing on certain necessary albeit not sufficient neural sub
strates for distinct types of emotional processes.
Our stories and our semantic habits have profound consequences for how we proceed in
empirical inquiries, and as I will repeat, perhaps ad nauseum, there is really no other way to
obtain biological knowledge about emotional matters except through arduous brain research
(usually in other species), guided by meaningful psychological concepts. Thus, this book is
written especially for those students who wish to bridge psychological and neurological issues
in scientifically sound ways. For them, I have attempted to mill the abundant factual pep
percorns into tempting conceptual spices. I have tried to make this difficult journey into the
brain as stimulating as possible without doing injustice to the facts, even though I had to
neglect many important lines of evidence to prevent the book from becoming too cumber
some. In any event, I hope that there are a number of students of philosophy, psychology,
and the neurosciences who will find rny efforts sufficiently refreshing and provocative that
they will eventually set out on their own empirical journeys in search of answers to the mny
scientific questions that remain to be asked.
An
Overview
This book is divided into three parts: (I) Background issues are discussed in Chapters I-6,
(2) the primitive emotions and motivations are covered in Chapters 71 1 , and (3) the social
emotions form the topic of Chapters 1 2 16.
In Part I, Chapters 1-3 will elaborate key concepts related to the functional systems in
the brain and taxonomic issues. Chapters 46 offer an essential background for understand
ing the substantive individual topics covered in Parts II and III. Chapter 4 provides a rela
tively user-friendly summary of neuroanatomy, Chapter 5 touches upon relevant aspects of
neurophysiology, and Chapter 6 addresses key neurochemical issues. These sections may
be tough going for readers who have little knowledge of the brain, but I have tried to make
them sufficiently concise and interesting that, after several readings, even a novice may gain
a sense of mastery of the materiaL I have also tried to write so that experienced readers will
enjoy them as thumbnail sketches of the enormous fields they are. Other basic background
issues, such as the details of sensory and motor processes, will not be covered here, since
ix
PREFACE xi
they are peripheral to our major goal. I have also generally avoided peripheral autonomic
and psychophysiological issues, which are typically well handled in many other basic physi
ological psychology and neuroscience texts.
In Part II of this book, I will discuss topics that are typically covered in most physiologi
cal psychology texts, but my approach will be atypical-it will focus not simply on basic
behaviors bUt also on the probable affective consequences of these behaviors for the organ
ism. In Chapter 7, I will discuss how sleep is organized in the brain and especially how
dreaming may relate to the brain organization of emotionality. In Chapter 8, I will provide
a new view of how so-called reward or reinforcement systems (i.e., those that animals like
to "self-stimulate") participate in the organization of natural behaviors and mental life. The
assertion will be that in both animals and humans, these brain systems control foraging,
seeking, and positive expectancies rather than what is traditionally called pleasure. Chapter
9 will focus on how the body maintains certain constancies, such as of energy and water,
through the auspices of pleasure and aversion mechanisms of the brain. I will di.scuss how
such affective processes help inform animals of the homeostatic status of various bodily
functions. Finally, Chapter 1 0 will focus on the nature of anger in the brain, and Chapter 1 1
will cover what we know about the brain mechanisms of fear.
Part III offers perspectives on the more subtle social emotions. I will discuss distinct
topics in terms of the emotional cascade within the reproductive-developmental phase of
the life cycle, starting with sexuality in Chapter 12, followed by nurturance and maternal
behavior in Chapter 13, the sources of separation distress, grief, and social bonding in Chapter
14, the basic nature of playfulness in Chapter 15, and the most difficult topic of all, the
nature of the self and higher mental processes in Chapter 16. With each successive chapter,
we enter topics about which less and less is known, and all conclusions are accordingly
more tenuous. Three key issues that did not fit well in the main text are placed in Appen
dixes A, B, and C: the first on human evolution, the second on the vagaries of human Ian
guages, as used in science (especially psychology), and finally a brief discussion of dual
ism in the brain and behavioral sciences.
In each chapter, I pay special attention to how our present knowledge may impact our
understanding of emotional disorders. Throughout, animal and human issues will be
blended. This attempt at simplification is a strategy that assumes that an understanding of
the similarities will take us toward important scientific insights that can have a positive
impact on human welfare more rapidly than a focus on the all-pervasive differences among
species.
Acknowledgments
I have tried to steer a middle course between the various polar views that presently char
acterize different schools of psychology. My attempt at a synthesis is bound to receive
some criticism from colleagues who have strong antireduGtionist biases, for many still do
not feel comfortable trying to explain complex psychological phenomena in neurological
terms. My approach may also go against the grain of a long-standing tradition in behav
ioral neuroscience, which mandates that we should not talk about processes that we can
not see with our eyes. Several good friends and scientific colleagues warned me of the
dangers in such an enterprise, but ultimately they all encouraged me to proceed. They did
this with even greater urgency as, during the middle of the present efforts, I underwent
the most painful time of my life: My precious daughter, Tiina Alexandra, died along with
three friends, on a dismal Good Friday evening in 1 9 9 1 when a drunken driver, evading
arrest, careened into their car. After that event, my spirit was demoralized, and I could
not face the labors of this book for several years. Through the magic of friends and mod
ern psychiatric drugs, my spirits were partially restored. In the fall of 1993, I restarted the
project and eventually devoted renewed energies to these labors in loving memory of my
daughter. My Tiina was an emotionally rich child who did not hesitate to share her true
feelings with others. I recall a conversation I had with Tiina concerning human emotions
almost two decades ago, when I was first attempting to summarize the issues that are
the foundation of this book, "Toward a General Psychobiological Theory of Emotions,"
Behavioral and Brain Sciences 5 ( 1982): 407-467). I recorded the following conversa
tion in that article:
To shed more light on the issue, I turned from my desk to my six-year-old daughter
playing at my feet.
"Tiina, can you tell me something? [She looks up agreeably.] How many emotions
are there?"
"What's an emotion?" she queries.
"Mm . . . it's the way we feel. How many different ways can we feel?"
She places a finger to her lips and looks briefly puzzled, and then rattles off, "Happy,
mad, sad . . . . Is that right, Daddy?"
"I'm not sure-you tell me. Are there any more?"
"Mm, yes, yes, scared! Is that right?"
"You tell me."
"Mm . . . mm . . . rom . . . frowned? Are there any more?" [She is beginning to look
exasperated.)
"Hey, that's really good. Can you show me all those in faces?"
As I say "happy," she smiles and jumps up and down clapping her hands; as I say
"mad," she frowns, clenches her jaw, ad more or less growls at me; as I say "sad," she
pantomimes the mask of tragedy; as I say "scared," she retracts her torso, balloons her
eyes, and shows a frightened mouth; as I say "frowned," she looks puzzled, scratches
her head a little, and finally crunches her face in a way that communicates little to me.
(p. 455)
Thanks, Tiina, wherever your spirit may bel
Many others along the way have helped me better understand the nature of emotions and the
nature of the scientific enterprise that must be pursued in order to understand the deep, neu
rological nature of human emotionality. Foremost among those have been the writings of Paul
MacLean and students, too numerous to mention, who have joined me in classes and labora
tories to explore the nature of emotions. Irreplaceable advice, assistance, and perspective tak
ing have been provided by several close colleagues at Bowling Green State University-es
pecially Pete Badia, Vern Bingman, Bob Conner, Kevin Pang, and John Paul Scott-as well
as visiting scholars and friends who came to BGSU to work and talk with me about emo
tional issues, especially Bruce Abbott, Manfred Clynes, Dwight Nance, and John Jalowiec,
who provided insightful input on an entire early version of this manuscript. Lonnie Rosenberg
did most of the very fine artwork in this book; the rest was done by myself and several gradu
ate students. I have been fortunate to have had many outstanding investigators who have shared
an interest in my work, most especially the editors of Oxford University Press's Series in
Affective Science-Richie Davidson, Paul Ekman, and Klaus Scherer. They, along with other
colleagues of the core faculty of the ongoing National Institute of Mental Health Postdoctoral
Training Program on Emotion Research, are foremost among the scholars who are presently
revitalizing emotion research around the world.
Several times I have used drafts of this book for teaching purposes at BGSU and the
University of Salzburg, Austria. I wish to thank my hosts in Austria-Guenther Bematzky
and Gustav Bernroider of the Institute of Zoology, Wolfgang Klimesch of the Institute of
Psychology, and Patrick Lensing of School Psychology of Upper Austria-for helping cre
ate an excellent environment for trying out new ideas. I also thank Joan Bossert and the
other good people at Oxford University Press, who were patient and encouraging in my
protracted struggle to get this project completed.
However, without a muse and a kindred spirit, all this would not have happened. Dr.
Anesa Miller, my wife, supported me well in the many roles that were needed to sustain
these efforts-providing emotional support, critical feedback, and her special worldview,
poetry, and music as needed. She read most of this book several times and provided endless
suggestions on how to make a better, more understandable manuscript. She helped sharpen
my thinking and brought clarity to many jumbled words. The readability of this work was
enhanced enormously by her remarkable linguistic skills and her sense of beauty, meaning,
and personal integrity. Much of this help was provided during a period when her own ere-
xii
PREFACE
ative fires were also burning intensely. The book of poetry she wrote to commemorate the
tragic passages of our lives-A Road Beyond Loss ( 1 995, published by the Memorial Foun
dation for Lost Children, Bowling Green, Ohio)-is an incomparable expression of the
emotions we all experience in times of grief. I thank you, Anesa, for your special help, and
I value you for the remarkable person that you are.
To the extent that semantic ambiguities and opacity of thought still abide on these pages,
I sincerely apologize, for I have labored earnestly to get at the truth and to convey it more
clearly than is possible in this difficult area of human knowledge.
Bowling Green, Ohio
September 1996
Contents
J. P.
PART I
CONCEPTUAL BACKGROUND
10
11
PART Ill
12
13
14
15
PART II
Appendix A:
Appendix B :
Appendix C:
Notes
343
Author Index
431
Subject Index
449
336
A.Hedive Neuroscience
PART I
Conceptual Background
CONCEPTUAL BACKGROUND
CONCEPTUAL BACKGROUND
Although the various forms of emotional arousal do many things in the brain,
one ofthe most important and most neglected topics in neuroscience is the attempt
to understand how emotional feelings are generated. An attempt to grapple with
this issue is one of the main goals of this text. Although most of the critical evidence
remains to be collected, I will try to deal with this difficult problem in a forthright
manner. I will accept the likelihood that other animals do have internal feelings we
commonly label as emotions, even though the cognitive consequences of those states
probably vary widely from species to species. This empirically defensible assump
tion will allow me to utilize information derived from simpler brains to highlight the
fundamental sources of affective experiences in humans. This is not to deny that
much of cognitive as well as emotional processing in the brain transpires at a sub
conscious level but to assert that basic, internally experienced affective states do
have an important function in determining how the brain generates behavior and
that other animals probably have internally experienced feelings.
In asserting the above, I should emphasize that the complexity of the human
brain, especially at its highest neocortical reaches, puts all other brains "to shame."
The human brain can generate many thoughts, ideas, and complex feelings that
other animals are not capable of generating. Conversely, other animals have many
special abilities that we do not have: Rats have a richer olfactory life, and eagles
have keener eyes. Dolphins may have thoughts that we can barely fathom. But
the vast differences in cognitive abilities among species should not pose a major
difficulty for the present analysis, for the focus here will be mainly on those
ancient subcortical operating systems that are, to the best of our knowledge,
homologous in all mammals. Although detailed differences in these systems exist
across species, they are not sufficiently large to hinder our ability to discern gen
eral patterns.
In short, many of the ancient, evolutionarily derived brain systems all mam
mals share still serve as the foundations for the deeply experienced affective pro
clivities of the human mind. Such ancient brain functions evolved long before the
emergence of the human neocortex with its vast cognitive skills. Among living
species, there is certainly more evolutionary divergence in higher cortical abilities
than in subcortical ones. Hence cognitive subtleties that can emerge from the
shared primitive systems interacting with more recently evolved brain areas will
receive little attention here. An analysis of those issues will require the types of
conceptualizations presently being generated by evolutionary psychologists. The
species differences in those higher functions are bound to be more striking than
the differences in the nature of the basic emotional systems that will be the focus
of discussion here. However, to the extent that the subcortical functions are shared,
we can create a general foundation for all of psychology, including evolutionary
psychology, by focusing on the shared emotional and motivational processes of
the mammalian brain. These systems regrettably have been neglected by main
stream psychology.
Why has it taken us so long to recognize the general organizational principles
for mind and behavior that are found within the primitive genetically dictated
areas of the brain that all mammals share? It is partly because the actions of those
ancient brain systems are very difficult to see clearly within our own behavior pat
terns, especially through the complex cognitive prisms of the human cortex that
generate subtle behavioral strategies and layers of learning and culture that are
uniquely human. It is partly because until recently we simply did not know enough
about the brain to have any confidence in such generalizations. However, it is also
because for a long time, 20th century psychology insisted that we should seek to
explain everything in human and animal behavior via environmental events that
assail organisms in their real-life interactions with the world rather than via the
evolutionary skills that are constructed in their brains as genetic birthrights.
CONCEPTUAL BACKGROUND
CONCEPTUAL BACKGROUND
ogy, and the modernized label for all of these disciplines: behavioral neuroscience.
The present coverage will rely heavily on data collected by individuals in these
fields, but it will put a new twist on the evidence. It reinterprets many of the brain
behavior findings to try to account for the central neuropsychic states of organ
isms. It also accepts the premise that most animals-certainly all mammals-are
" active agents" in their environments and that they have at least rudimentary rep
resentations of subjectivity and a sense of self. With such assumptions, we can
create a more realistic and richer science by recognizing the number of basic pro
cesses we share with our kindred animals.
Progress in affective neuroscience will be critically dependent on the develop
ment and use of compelling experimental models. Obviously, to do this we must
exploit other animals. This leads me to briefly confront, at the very outset, the
troublesome issue of ethics in animal research. Because of such issues, animal brain
research has diminished markedly in university departments of psychology through
out the United States. While the animal rights movement applauds such change,
some of us feel that it compromises the future development of substantive knowl
edge about the deep sources of human nature that can help promote both human
and animal welfare. I t can also reduce zoophobia in the human sciences.
Indeed, the "Afterthoughts" will often highlight the most critical issues, such as
the following concern that all sensitive people must have about biological research
on live animals.
'
Although animal research will surely not reveal why humans have strong emo
tions regarding issues such as abortion, rape, and the many civil injustices that
still characterize our society and our world, it can provide a substantive answer to
questions such as what it means to be angry, scared, playful , happy, and sad. If
we understand these important brain processes at a deep neurobiological level
(an end result that can be achieved only with animal brain research), we will bet
ter understand the fundamentally affective nature of the human mind. Thereby,
we will also be in a better position to help animals and humans who are in emo
tional distress. The aim of this book is to n u rture the growth of such knowledge.
Affective Neuroscience
History and Maior Concepts
Literary intellectuals at one pole-at the other scientists . . . . Between the two a
gulf of mutual incomprehension-sometimes (particularly among the young)
hostility and dislike, but most of all lack of understanding. They have a curious
distorted image of each other. Their attitudes are so different that, even on the
level of emotion, th ey can't find much common ground.
C. P. Snow, Two Cultures and the Scientific Revolution (1959)
The "emotions" are excellent examples of the fictional causes to which we com
monly attribute behavior.
R F. Skinner, Science and Human Behavior ( 1953)
CENTRAL THEME
Our emotional feelings reflect our ability to subjectively
experience certain states of the nervous system. Although
conscious feeling states are universally accepted as major
distinguishing characteristics of human emotions, in
animal research the issue of whether other organisms feel
emotions is little more than a conceptual embarrassment.
Such states remain difficult-some claim impossible-to
study empirically. Since we cannot directly measure the
internal experiences of others, whether animal or human,
the study of emotional states must be indirect and based
on empirically guided theoretical inferences. Because of
such difficulties, there are presently no direct metrics by
which we can unambiguously quantify changes in emo
tional states in any living creature. All objective bodily
measures, from facial expressions to autonomic changes,
are only vague approximations of the underlying neural
dynamics-like ghostly tracks in the bubble chamber
detectors of particle physics. Indeed, all integrative psy
chological processes arise from the interplay of brain cir
cuits that can be monitored, at present, only dimly and
indirectly. Obviously, a careful study of behavioral actions
is the most direct way to monitor emotions. However,
many investigators who study behavior have argued that
emotions, especially animal emotions, are illusory con
cepts outside the realm of scientific inquiry. As I will seek
to demonstrate, that viewpoint is incorrect. Although
much of behavioral control is elaborated by unconsCious
brain processes, both animals and humans do have simi-
10
CONCEPTUAL BACKGRO U N D
AFFECTIVE N E U ROSCIENCE
11
ill
12
AFFECTIVE NEUROSCIENCE
CONCEPTUAL BACKGROUND
13
14
AFFECTIVE NEUROSCIENCE
CONCEPTUAL BACKGRO U N D
15
16
AFFECTIVE N E U ROSCIENCE
CONCEPTUAL BACKGRO U N D
17
18
CONCEPTUAL BACKGRO U N D
AFFECTIVE N E U ROSCIENCE
--+{)
"""""CATSMELL
CONDITIONED
BEHAVIORS
(CAT-SMELL)
UNCONDITIONED
BEHAVIORS
19
I
'
'
'
I
I
'
'
I
(Fearfulness)
20
CONCEPTUAL BACKGROU N D
AFFECTIVE NEUROSCIENCE
REPTILIAN SRAIN
HABITS EMERGE FROM 11-IE
REPTIUAN BRAIN THROUGH
T A
G:R ggllVgOCN'.,
;,E
's'''--
OLD-MAMMALIAN BRAIN
21
22
CONCEPTUAL BACKGROU N D
AFFECTIVE NEUROSCIENCE
VARIABLE
RATIO
Rapid responding
near time for
Steady Responding
TIME
Figure 1 .4. Schematic depiction of some of the laws of operant behavior. Represen
tative types of response patterns (arbitrary scales) of animals working on traditional
partial reinforcement schedules of reward. Animals on fixedratio (FR) schedules
work at high constant rates and exhibit short postreinforcement pauses after acquiring
each reward. On variable-ratio (VR) schedules, animals respond at fast constant rates
that are somewhat slower than rates on FR schedules. On fixedinterval (FI) sched
ules, animals exhibit slowly accelerating modes of responding, with the most rapid
rates exhibited just prior to each reward (which reflects an "expectancy type" of
gradually intensifying pattern of behavioral arousal). On variableinterval (VI)
schedules, responding is very steady but generally much slower than any of the other
schedules of reinforcement. Obviously, gambling places such as Las Vegas prefer to
keep their clients working on VR schedules of reinforcement.
23
Suggested Readings
Barkow, J., Cosmides, L., & Tooby, J. (eds.) (1990).
The adapted mind: Evolutionary psychology and
the generation ofculture. New York: Oxford Univ.
Press.
Bunge, M. (1990). What kind of discipline is psychol
ogy: Autonomous or dependent, humanistic or
scientific, biological or sociological? New Ideas in
Psychology 8 : 121-137.
Byrne, R., & Whiten, A. (eds.) ( 1 988). Machiavellian
intelligence. Oxford; Oxford Univ. Press.
Churchland, P. ( 1 985). Neurophilosophy. Cambridge,
Mass.: MIT Press.
Clynes, M., & Panksepp, J. (eds.) (1988). Emotions and
psychopathology. New York: Plenum Press.
Griffin, D. R. ( 1984). Animal thinking. Cambridge,
Mass.: Harvard Univ. Press.
Lewis, M., & Haviland, J. M. (eds.) (1 993). Handbook
of emotions. New York: Guilford Press.
MacLean, P. D. ( 1990). The triune brain in evolution.
New York: Plenum Press.
Plutchik, R. ( 1980). Emotion: A psychoevolutionary
synthesis. New York: Harper and Row.
Wilson, E. 0. ( 1 975). Sociobiology: The new synthe
sis. Cambridge, Mass.: Harvard Univ. Press.
.,
..
..
.-----------
r;-:r
l-('
CENTRAL THEME
Ultimately the emotional systems of the brain create
mixtures of innate and learned action tendencies in
humans, as well as in the other creatures we must study
in order to fully understand the neural substrates of
affective processes. As we now know, there are no
credible, routine ways to unambiguously separate the
influences of nature and nurture in the control of be
havior that will apply across different environments.
To understand the aspects of behavior that derive their
organizational essence mainly from nature, we must
first identify how instinctual behaviors emerge from the
intrinsic potentials of the nervous system. For instance,
animals do not learn to search their environment for
items needed for survival, although they surely need to
learn exactly when and how precisely to search. ln other
words, the "seeking potential" is built into the brain,
but each animal must learn to direct its behaviors to
ward the oppo1tunities that are available in the envi
ronment. In addition, animals do not need to learn to
experience and express fear, anger, pain, pleasure, and
joy, nor to play in simple rough-and"tumble ways, even
though all of these processes come to modify and be
modified by learning. Evidence suggests that evolution
has i mprinted many spontaneous psychobehavioral
potentials within the inherited neurodynamics of the
25
24
. I
,.
,.
I,
I
26
CONCEPTUAL BACKGRO U N D
EMOTIONAL DEVELOPMENT
,___
SEEKING /FEAfl. I RA
to
2C
$0
''
70
SEPARATlO:\ DISTRESS
;,,.,t, o.,ly
pupOoOO
peh<ty wly
"!"l'hMI'
27
nr
'
'
. -
I
..
.
...------ --- i. ' !
;-
28
P-
CONCEPTUAL BACKGROUND
0 G?
1, ,/?flf!J
- -
29
r-30
CONCEPTUAL BACKGROUND
Affirming
Consequents
in the
Study of
Emotions
first Dilemma:
."
Therefore, I Am Angry,-
. Second Dilemma:
The Solution
Neu r o p s y c h o I o g y
C o g n i t i ve
Faculty
Neuroscience
MIND
J
L-
31
AFFECTIVE
NEUROSCIENCE
and
Behavioral
Neuroscie nce
C o g n itive
BEHAVIOR
. qj
Figure 2.4. Progress in understanding the biological nature of affective processes can
only proceed through the integration of psychological, behavioral, and neuroscientific
approaches. At present, there is no discipline that utilizes all of these approaches in a
balanced manner. The various disciplines that bridge two of the three components are
indicated. Affective neuroscience aspires to bridge all three, and the dissection of the logo
used for this book helps symbolize the complexities we face: We need to come to terms
with ancient reptilian brain functions, old mammalian brain functions, as well as the
crowning glory of the human cortex.
32
CONCEPTUAL BACKGRO U N D
1}
Stimulus
2)
Stimulus
-+
----+
lnlerpretation
dation issues.
Bodily
Responses
Emotions
3)
<
Bodily
Responses
4)
Stimulus
Bodily
--+ Emotions
Responses
Interpretation
<
Bodily
Responses
t !
Emotional
Response
33
control behavior.
traditional folk
i i
!
34
CONCEPTUAL BACKGRO U N D
R
N
E
s
s
COGNITIVE
PRIMATES
AWARENESS
AFFECTIVE
LISENCEPHALIC
AWARENESS
REFLEXIVE
BEHAVIOR
MAMMALS
REPTILES
FISH
25
250
GREAT APES
AWARENESS
A
w
1 1 ).
0
F
SELF
HUMANS
R
F:
35
2.5
YEARS IN MILLION
16),
commanding role in
gibles tangible.
Since we may never be able to specify when affec
tions. At present, there are very few ideas that meet such
analysis (Figure
the
36
CONCEPTUAL BACKGRO U N D
Figure 2.7. The marine snail Aplysia californica has a simple nervous system of about
20,000 nerve cells and a set of defensive reflexes that have been used effectively to study
the neuronal basis of learning (especially classical conditioning; see Figure 1.2). For
instance, touching the siphon or gill leads to a withdrawal of these organs, but this
response habituates rapidly. If, ho"Yever, this type of conditioned stimulus (touch) is paired
with electric shock to the tail, the animal develops a conditioned gill-withdrawal response
to touch . .Although this type of classically conditioned learning has been most extensively
studied in this creature, there has been some success in training these animals to also
exhibit instrumental learning.
37
#[
I
!
38
CONCEPTUAL BACKGROUND
39
40
CONCEPTUAL BACKGRO U N D
Suggested Readings
Ekman, P., & Davidson, R. (eds.) ( 1 994). Questions
about emotions. New York: Oxford Univ. Press.
Gallistel, C. R. ( 1 980). The organization of action: A
new synthesis. Hillsdale, N.J.: Lawrence Erlbaum.
Kanner, M. ( 1982). The tangled wing: Biological con
straints over the human spirit. New York: Holt,
Rinehart and Winston.
Oaksford, M., & Brown, G. (eds.) ( 1 994). Neurody
namics and psychology. New York: Academic
Press.
Plomin, R., De Fries, J. C., & McCleam, G. E. ( 1 990).
Behavioral genetics: A primer (2d ed.). San Fran
cisco: Freeman.
Schulkin, J. (ed.) ( 1 993). Hormonally induced changes
in mind and brain. San Diego: Academic Press.
Tinbergen, N. ( 1 95 1 ) . The study of instinct. London:
Oxford Univ. Press.
Valenstein, E. S. ( 1 973). Brain control. New York:
Wiley.
Vernon, P. A. (ed.) ( 1 994). The neuropsychology of
individual dljferences. New York: Academic
Press.
Wright, R. ( 1994). The moral animal. New York: Ran
dom House.
making language the expositor of nature, instead of making nature the exposi
tor of language.
Alexander Brian Johnson, A Treatise on Language, as quoted by
Frank A. Beach, "The Descent of Instinct" ( 1955)
CENTRAL THEME
Scholars down through the ages have disagreed about
the number and nature of basic emotions. Investiga
tors have not even agreed on the criteria to be used in
the classification of emotions. A great deal has been
written on such matters, but most of it remains con
troversial. Until recently, this question could not be ap
proached from a neurological perspective. As we will
see in this chapter, now it can. First, I will consider how
we might define primary emotional systems, or "af
fect programs," and then summarize the types of ba
sic emotional circuits that exist in the brain. A limited
number of powerful primal emotional circuits-those
that appear to elaborate fear, anger, seeking, and sor
row-have now been sufficiently well characterized
41
""I I ''
i
r
42
CONCEPTUAL BACKGROUND
43
44
CONCEPTUAL BACKGROUND
EMOTIONS
MEDIATED
INDIRECTLY
FOLLOWING
BODILY
AROUSAL
COGNITIVE
PERCEPTUAL
PROCESS
AUTONOMIC
PROCESSES
SOCIAL-CONSTRUCTIVIST VIEW
WEAK INTERACTIONS
STRONG INTERACTIONS
COGNITIVE
PERCEPTUAL
PROCESS
AUTONOMIC
PROCESSES
MEDIATED
DIRECTLY
VIA
BRAIN
CIRCUITS
PSYCHOBIOLOGICAL VIEW
Figure 3 .2. Two major current views of how emotions are organized in the brain.
The top view represents the essence of the James-Lange perspective (see the
'Afterthought" of this chapter), which has guided social-constructivist thinking
about emotions to the present day. The bottom view represents a more accurate
perspective that is based on existing neuroscience evidence, where centrally situated
emotional systems in the brain extensively interact, in strong and weak ways (as
highlighted by bolder and lighter lines, respectively), with higher and lower brain
functions. A third approach (not shown), the componential one, is really a mixture of
the other two. The componential view would be an amalgamation of these views,
without the suggestion that there are any coherent emotional systems of the brain.
Instead, emotional coordination is achieved by many component responses coming
together as a function of learning.
45
Taxonomies of Emotions
As highlighted at the beginning of this chapter by Tho
mas Willis's comments on the passions, there have been
many taxonomies of emotions down through the ages
and all too many sterile controversies. 8 Some scholars,
especially those with postmodern deconstructive orien
tations, believe that psychological processes are intrin
sically so complicated by multiple causation that logi
cal analysis through reductionism and manipulation of
simple systems (such as those using animal models) will
never provide the answers that we need. Diversity of
taxonomies and ideas is sustained, and no one's thoughts
are excluded. Unfortunately, they cannot all be correct
at the biological level.
One response to a proliferation of taxonomies is a
movement in the opposite direction-toward a minimal-
t"
46
CONCEPTUAL BACKGROUND
47
48
CONCEPTUAL BACKGROUND
Figure 3.3. The various neural interactions that characterize all major
emotional systems of the brain: ( 1 ) Various sensory stimuli can uncondi
tionally access emotional systeri1s; (2) emotional systems can generate
instinctual motor outputs, as well as (3) modulate sensory inputs. (4)
Emotional systems have positive feedback components that can sustain
emotional arousal after precipitating events have passed. ( 5) These
systems can be modulated by cognitive inputs and (6) can modify and
channel cognitive activities. Also, the important criterion that emotional
systems create affective states is not depicted, but it is assumed that
arousal of the executive circuit for each emotion is a necessary condition
for getting feeling states activated within the brain, perhaps by interacting
with other brain circuits for self-representation, such as those that appear
to exist in the midbrain periaqueductal and deep tectal circuits that interact
with frontal cortical systems (see Chapter 16).
49
50
CONCEPTUAL BACKGRO U N D
SOCIAL
LOSS
IRRITATION,
RESTRAINT
and
FRUSTRATION
51
52
[;,_
CONCEPTUAL BACKGROUND
FORWARD LOCOMOTION,
SNI FFING,
53
tNVESTtGATION
,.
e,
.
>o
w
c.
_z
0
(/)
"'
1:r:
C!l
"'
"'
"'
!G
"'
<
0
(')
...1
u..
)>
c5
,...
;::;
:!:
0
w
w
a:
"-
_z
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0
"
"
0
z
;!
0
ATTACK,
BITI N G ,
FtGHTtNG
Figure 3.5. The major emotional operating systems are defined primarily by genetically
coded neural circuits that generate well-organized behavior sequences that can be evoked
by localized electrical stimulation of the brain. Representative behaviors generated by the
various systems are indicated, and the approximate locations of the SEEKING, FEAR, and
RAGE systems are depicted on a small frontal section through one side of the hypothala
mus. As is evident, there is considerable overlap and hence neural interaction among
systems. Some of the possible major interactions are indicated by the various interconnect
ing lines that suggest various excitatory and inhibitory influences among systems.
(Adapted from Panksepp, 1982; see n. 26).
54
CONCEPTUAL BACKGROUND
55
56
CONCEPTUAL BACKGROUND
57
58
CONCEPTUAL BACKGRO U N D
..
.
. .
..
. . . . . . . . ... .
. ... . .
. . . ..
. .\
.
..
..
..
Neurostatics
./
FC
. ..
..
..
. ..
.
our observation only extends to thought and emotion as connected with the liv
ing body, and, according to the general verdict of consciousness, more espe
cially with certain parts of the body; namely, the central organs of the nervous
OB
Suggested Readings
Birbaumer, N . , & Ohman, A. (eds . ) ( 1 993). The
structure of emotions. GOttingen: Hogrefe and
Huber.
Christianson, S.-A. (ed.) ( 1 992). The handbook of
emotion and memmy. Hillsdale, N.J.: Lawrence
Erlbaurn.
Whatever may be our opinions as to the relations between "mind" and "matter,"
.. . . .
.
. ..... . .. . . . . .. .
,
CENTRAL THEME
Many who have considered the matter believe that an
understanding of psychological and behavioral processes
must initially guide our understanding of the functions
of the brain. less well appreciated is the fact that un
derstanding of the brain can highlight the nature of
psychological processes. Intellectual commerce is always
a two-way street. Recent discoveries about the brain
have finally established a foundation for a mechanistic
understanding of the mind. Numerous new techniques
now exist to illuminate brain-mind relations, and the
painstaking collection of new information continues at
a fever pitch. The "neuroscience revolution" of the last
few decades has enabled us to conceptualize human
nature in dramatically new ways, and the debate is shift
ing from the issue of whether mind emerges from brain
to how specific mental states, traits, and abilities arise
from the brain. The ongoing breakthroughs are so im
portant that even remote disciplines such as philosophy,
economics, and political science are beginning to pay
close attention to what the psycholog'1cally or'1ented
neuroscientists are doing. AI! past progress in this quest
has been premised on acceptance of the " neuron doc
trine" -the recognition that individual neurons are the
fundamental units that transfer information throughout
the brain. Just as each h uma.n being has individual quali
ties as a receiver and transmitter of information, so too
does each neuron have such qualities, both electrical and
chemical. But a single neuron does nothing important
psychologically by itself. Psychological processes emerge
from the neurodynamic interactions of many intercon-
60
CONCEPTUAL BACKGROUND
Neuroanatomical Homologies
Studying neuroanatomy entails an almost endless exer
cise in relating arcane nomenclatures to the topographic
landmarks of a very complex organ. Brain structure
brings to mind the wonderful intricacies of medieval
cathedrals: A grand and stately order repeats itself, in
general plan, from one mammalian species to the next.
But variety is always there.
Fortunately, if one learns the subcortical neuro
anatomy of .one mammalian species, one has learned
the ground plan for all other mammals. Indeed, by
mastering the brain of one mammal, one immediately
enjoys a good understanding of the subcortical neu
roanatomy of most other vertebrate species. This is di
rect evidence for many structural homologies in the
brain, which helps justify the belief that many brain
functions are also homologous across species. Indeed,
the most striking insight of many students when they
first become entranced by neuroscience is the remark-
NEUROSTATICS
61
NEUROSTATICS
2)
EMOT
NERVOUS
SYSTEM
AXIS
MOTOR
OUTPUT
Figure 4. 1 . Schematic representation in the human brain of the major axes of visceral
(hypothalamic-limbic axis-stream of feeling) and somatic (thalamic-neocortical axis
stream of thought) information processing. They converge on the reptilian brain, or basal
ganglia. The dorsal streams of neural activity are related more to information coming from
the external senses (vision, hearing, and touch), while the ventral-visceral streams of
neural activity are related more to the chemical and internal senses (taste, smell, tempera
ture, and various hormone and body energy and water detectors). Both streams of
information converge on basic sensory-motor control programs of basal ganglia to
generate behavior in which both somatic and visceral processes are blended to yield
coherent behavior output.
'
'
-- -
'
'
'
'
P R OG R A M S
>---------T---<1
I
'
Highly permeable to 1
\ environmental events
'
'
.,>,
1
E N V I R O N M E NT
C LO S E D
LAU G H I N G
PROGRAMS
YAWN I N G
Relatively impermeable
NAUSEA
to environmental events
TASTE
SMELL
'
R ET R O G R A D E
'
63
N U RT U R A N C E
LA NG UA GE
S E E KI N G
A N X I ETY
PL AY
Figure 4.2. Schematic representation of closed and open programs of the brain. Environ
mental events trigger closed programs into fairly stereotyped actions such as yawning and
laughing. Open programs are much more extensively modified by interactions with
environmental events according to various principles of learning.
N UCLEI
(Clusters of Neurons)
I
'
TRACTS
(Clusters of Axons)
I
I
\
'
RETICULAR S U B STANCE
(Diffuse interdigitation of
Neurons and Axons)
Figure 4.3. Neural tissue is composed of three general types of tissues: nuclei (or clusters of
nerve cells), tracts (clusters of axonal fibers), and reticular substance (where the two
interdigitate to such an extent that the pattern of interconnections is more difficult to discern).
Anterograde (away from the cell body) and retrograde (toward the cell body) anatomical
projections can now be studied with a host of neurochemical techniques, and the neurochemi
cal character of individual neurons can be highlighted with immunocytochemical approaches.
r
64
NEUROSTATICS
CONCEPTUAL BACKGROU N D
Nissl Stain
(Stains Neurons)
C1 4-2-deoxy-D-Giucose
(Detects Rate of Metabolism)
Figure 4.4. Two views of the rat brain highlighting different properties of brain tissues:
on the left, cell staining using the Nissi procedure; on the right, the same brain section
processed for radioactive 2-DG, which clearly highlights differences between somatic
(thalamic-neocortical) and visceral (hypothalamic-limbic) areas of the brain. There are
many anatomical, neurophysiological, and neurochemical distinctions between these
zones of the brain, which clearly indicate that the dichotomy between the "thinking" and
"feeling" parts of the brain is a fundamental distinction and not just a poetic metaphor.
The greater mass of reptilian brain is anterior to this section, but the wedge between the
lower wing of the corpus callosum (cc) and the descending motor fibers of the cerebral
peduncle (cp) contains striatal tissue called the globus pallidus (GP). Other anatomical .
abbreviations are: Cx: cortex; CG: cingulate gyrus; ci: cingulum; HC: hippocampus; St:
stria tenninalis; sm: stria medularis; Thai: thalamus; ML: medial lemniscus; MTT:
mammilo-thalamic tract; LH: lateral hypothalamus; Fx: fornix; Am: amygdala; DMN:
dorsomedial nucleus of the hypothalamus; MH: medial hypothalamus.
65
66
CONCEPTUAL BACKGRO U N D
N E U ROSTATICS
may finally understand how the intensity and duration of
neomammalian (neocortex).
67
Chemical Anatomy
A universal function of all cells is to manufacture proteins.
To do this effectively, cell bodies have highly specialized
uptake mechanisms for absorbing the constituent amino
acid building blocks. In neurons, many proteins are con
universal of which is
as the
brain, or
immunocytochemistry. In ptinciple,
0
0:
_,
<(
z
TELENCEPHALON
0:
"'
GANGLIA
THALAMUS
DIENCEPHALON
Figure 4.5. On the left arc depicted the progressive swellings of the brain as a
function of development. On the right, a more realistic depiction of the types of
flexures and expansions that gradually lead to a mature appearance of the brain.
:rpt:
68
CONCEPTUAL BACKGRO U N D
NEU ROSTATICS
NERVOUS
SYSTEM
PERIPHERAL
VISCERAL/AUTONOMIC
NERVOUS SYSTEM
69
CENTRAL
COLUMNAR
ORGANIZATION
AT 3 LEVELS OF THE CNS
' '!
;!.:,.,':.,
***
8.?E ;
:
M
TEM
T
Y
s
PARASYMPATHETIC
SYSTEM AS WELL AS
HEART
LUNGS
STOMACH
LIVER
SMALL INTESTINE
PANCREAS
ADRENAL MEDULLA
KIDNEY
BLADDER
***
PONS
"!.
'?,
LARGE INTESTINE
BLADDER
REPRODUCTIVE ORGANS
<;:.
SOMATIC-SENSORY (SS)
VISCEAALSENSOAY (VS)
VISCERAL-MOTOR (VM)
SOMATICMOTOA (SM)
SACRAL PARASYMPATHETIC
COCCYGEAL
COLUMNAR ORGANIZATION
AT 3 LEVELS OF THE CNS
CEREBRAL ARTERIES
CAUDAL
Figure 4.6. Blood supply depicted on the ventral smiace of the rat brain. The rostral parts
of the brain are fed by the carotid arteries entering the circle of Willis. The blood is
distributed to each of the hemispheres by anterior and middle cerebral arteries. The brain
stem is fed by the ascending vertebral artery on the base of the brain, and it also contrib
utes to the perfusion of the back of the cerebral hemispheres via the posterior cerebral
artery.
70
CONCEPTUAL BACKGRO U N D
NEU ROSTATICS
4.4).
71
Figure 4.8. Three-dimensional depiction of the rat brain from the anterior lateml perspective.
Each of the three frontal (or "coronal") sections depicts major subcortical structures of the
reptilian brain and limbic system. The stippling on each section is indicative of the density of
opiate receptors at these levels of the brain (for a full depiction of opiate receptors in the rat
brain, see Figure 6.8).
are the
who stated that the "royal road to the soul goes through
alized as the
ing upon old parts. For instance, animals seek out food
an
Please note that there are also more ancient limbic cor-
72
CONCEPTUAL BACKGROUND
Nonspecific
III Cortico
Cortical
Specific
Thalamic
Single Neuron
Figure 4.9. Left: General plan of cortical organization, with a single Golgi
stained neuron on the left Can you find that neuron in the full cross section of
cortex in the middle? It is indicated by an asterisk, and the location of that whole
cortical section is depicted on the asterisk-highlighted coronal section of the brain.
The other squares indicate approximate locations for the Fos immunocytographs
depicted in Figure 15.7. Right: Summary of the six layers of cortex and their
vario.us connections to other brain areas. The nonspecific influences from biogenic
amine systems such as those depicted in Figures 6.5 and 6.6 are concentrated in
the topmost layers of the cortex. Layer III connects similar locations in the two
hemispheres. Since layer IV is small in this section, it must be motor cortex. If this
layer were large, it would be sensory cortex, getting input from the thalamus.
Layers V and VI send information downward in the brain. About a thousand
cortical neurons working together as a functional unit are called a column, which
is hard to see in this view of the brain.
_j
'
Cortico
Subcortical
74 CONCEPTUAL BACKGROUND
Behavioral spontaneity is possible only when the
midbrain and hypothalamus are intact and remain con
nected to the lower brain stem. However, the behavior
of such animals, in which more rostral tissue has been
removed, is still quite disorganized and fragmented.
Even though they do initiate spontaneous actions, they
exhibit little behavioral flexibility and coherence. For
instance, animals in this state will become more active
when they are hungry, but they will not direct their
activity effectively.
Organized and sequenced instinctual behavior oc
curs only when the basal ganglia are connected to the
hypothalamus and brain stem. In other words, the mere
removal of the neocortex does not lead to major defi
cits in instinctual behaviors, although such animals are
certainly not very bright.26 Experiments of this type, as
well as localized brain-stimulation studies that evoke
specific emotional behaviors, suggest that a series of
emotional circuits exist within the limbic system. There
are operating systems for exploration, aggressive de
fense, fear, and various social initiatives, all of which
can be demonstrated at the midbrain level. Although the
lower brain stem and spinal cord contain most of the
sensory and motor nuclei that actually control outward
behavior and accompanying autonomic changes, only
the rudiments of behavioral spontaneity are found in
these lower reaches. I will discuss some of these struc
tures in subsequent chapters in conjunction with the
individual emotional systems. Here I will focus only on
the major circuits of the higher brain, which are the basic
psychoneurological operating systems for behavioral
spontaneity.
NEUROSTATICS
works" or ''cell assemblies." An especially important
point to remember is that even though the human brain
has much more neocortex than other animals of com
parable size, this is achieved by the addition of more
columnar modules and their interconnections rather than
by increasing the quality (i.e., complexity) of cortical
columns.
In addition to well-organized inputs (afferents) from
the thalamus and other cortical areas, the major inputs
(efferents) of the cottex are descending circuits back to
the thalamus, as well as massive dispersion of informa
tion into the basal ganglia (Figure 4. 1 0). The output of
the entire cortical mantle to the striatum is enormous
and topographically organized, and most of its synapses
transmit information via the simple amino acid known
as glutamate. The basal ganglia send information back
to the ventral thalamus via the output circuits of the
globus pallidus, the ansa lenticularis. These messages
are then processed by the thalamus and flow upward
into the cortex once more. In this way, the "stream of
thought" probably comes to be connected with basic
daily plans for action that are encoded within the basal
ganglia.
Cognitive information presumably has to percolate
thmugh this loop an undetermined number of times
before coherent behavioral plans emerge. If the loop is
experimentally broken, as can be done by placing neu
rotoxins into the caudate nucleus, animals' behavioral
flexibility is compromised in ways that are just begin
ning to be documented. Indeed, in the human brain dis
order known as Huntington 's disease, this type of dam
age occurs for genetic reasons that have recently been
identified.28 In the brains of such individuals, excessive
levels of endogenous glutamate may gradually destroy
the basal ganglia. Although these patients eventually
exhibit severe motor disabilities, their mental status is
initially compromised by a schizoid type of disorder
characterized by disjointed .cognitive activity.29 For
instance, a person may remember all the steps in a favor
ite recipe but not be able to sequence them into a final
product. Apparently, the flow of information through
striatal-thalamic-cortical loops helps solidify behavior
sequences based on various component parts. The cor
tex contains the component parts, but the striatum welds
them into a coherent plan.
It is generally believed that complex factual memo
ries (often termed declarative or semantic memories)
are stored in the interconnections of the cortex, but
many simple memories, such as motor habits, are con
trolled by subcortical circuits. For example, the basic
motor memory for the classically conditioned eyeblink
reflex (e.g., the anticipatory blinking caused by a tone
that has been paired with a puff of air directed at an eye)
resides within an ancient part of the cerebellum,30 a
structure that was traditionally thought to simply facili
tate motor coordination but is now known to participate
in many other processes, including emotional ones>H
Even in the case of such basic learning, higher brain
THE"RATIONAL" BRAIN
75
76 CONCEPTUAL BACKGROUND
Connections of the Limbic System
NEUROSTATICS
cesses. The trunks reflect the ancient executive cores of
each system, which are influenced by various bodily and
simple perceptual states, and the roots lie in basal gan
glia and brain stem areas, providing connections to
various motor processes. Indeed, these discrete neuro
chemical pathways help generate and synchronize cog
nitive, physiological, behavioral, and feeling states within
widely distributed areas of the nervous system. By view
ing basic emotional systems in this way, we can ap
preciate why categorical, componential, and social
constructivist perspectives on the study of emotions need
not compete but instead can work together. My preferred
approach, the categorical one, can best characterize
"trunk-line" issues concerning the organization of emo
tionality in the brain; the componential approach can
identify how various fragments of experience are in
corporated into emotional states; and the social
constructivist approach can describe how these systems
contribute to cultural evolution and the cognitive inter
pretation of our great varieties of real-life experiences.
77
f!J
N E UROSTATICS
SAGGITAL SECTIONS
FRONTAL SECTIONS
DORSAL
VENTRAL
..J
<(
a:
w
1<(
..J
CAU DAl
H O R IZONTAL
S ECTIONS
Figure 4.1 1 . Stereotaxic atlas of the rat brain in three coordinates. These are actual tracings
from photographed brain sections. Anatomical designations are: AC: Anterior Commissure;
AL: Ansa Lenticularis; Am: Amygdala; EN: Bed Nucleus of the Stria Tenninalis; CC: Corpus
Callosum; Cereb: Cerebellum; CG: Cingulate Cortex; CP: CaudatePutamen; cp: Cerebral
Peduncle; Cx: Cortex; EP: Entopeduncular Nucleus; FC: Frontal Cortex; Fx: Fornix;
GP: Globus Pallidus; HB: Habenula; HC: Hippocampus; IC: Inferior Colliculus; ic: internal
capsule; IPn: Interpeduncular Nucleus; LG: Lateral Geniculate; LH: Lateral Hypothalamus;
LC: Locus Coeruleus; M: Medulla; MFB: Medial Forebrain Bundle; MG: Medial Geniculate;
MH: Medial Hypothalamus; ML: Medial Lemniscus; MTf: Mammilothalamic tract;
NA: Nucleus Accumbens; OB: Olfactory Bulb; ot optic tract; P: Pons; PAG: Periaqueductal
Gray; PB: Parabrachial Area; POA: Preoptic Area; R: Raphe; RF: Reticular Formation;
S: Septum; SB: Subiculum; SN: Substantia Nigra; SC: Superior Colliculus; Thai: Thalamus;
V: Motor nucleus of cranial nerve tive; VTA: Ventral Tegmental Area.
79
80
CONCEPTUAL BACKGROUND
Suggested Readings
Braitenberg, V., & Schulz, A. (1991). Anatomy of the
cortex. New York: Springer-Verlag.
Brodal, A. ( 1981). Neurological anatomy in relation to
Neurodynamics
The Electrical Languages of the Brain
The brain is waking and with it the mind is returning. It is as if the Milky Way
entered upon some cosmic dance. Swiftly the head-mass becomes an enchanted
loom, where millions of flushing shuttles weave a dissolving pattern, always a
meaningful pattern, though never an abiding one: A shifting harmony of sub
patterns.
Sir Charles Sherrington, Man on His Nature ( 1 940)
CENTRAL THEME
The view of the brain as an "enchanted loom" is one of
the most famous images of the nervous system in op
eration. To some extent it is an elegantly simple picture:
Individual neurons convey information via a universal
electrochemical process, speaking to other neurons in
chemical dialects. But the simplicity is deceptive. It only
provides the beginning of understanding as far as psy
chology is concerned. The study of the electrical re
sponses of individual neurons has yet to give us a cred
ible picture of the intrinsic neurodynamics of the mind.
There is a yet unfathomed internal harmony to brain
functions, with many neural systems working together
to produce mind. One of the best ways to approach the
operations of the brain holistically and in real time is via
electroencephalographic (EEG) measures, which can
monitor the joint dendritic activities of large ensembles
of neurons. A shortcoming of this technique is its inabil
ity to reveal the deep functions of the intact human
brain. One of the most difficult problems is that the brain
has so many endogenous subcortical functions (i.e., ones
that were constructed through evolutionary selection
rather than within the individual life experiences of an
organism), and we cannot readily study such processes
in humans using electrical recording procedures. Jn ani
mals, we can demonstrate the role of specific subcorti
cal circuits in various psychobehaviora! processes via
various interventions, but the dynamic electrical codes
that operate within these circuits are difficult to decipher
using objective procedures. There is a massive sponta
neity of neuronal activity throughout the brain. Jt is as
if we were confronted by many hieroglyphics, with no
Rosetta stone. Although early theorists thought the
machinery of the brain was only set into action by ex81
82
CONCEPTUAL BACKGROUND
ACTION POTENTIALS
--
-- l I
DENDRITES
AM TRANSMISSION
(Graded Potentials or
Amplitude Modulated)
/
AXONS
83
84
CONCEPTUAL BACKGROUND
85
86
CONCEPTUAL BACKGROUND
Single-Unit Studies
87
88
CONCEPTUAL BACKGROUND
89
Child P.
Control Child
ERD
-1 00%
-80%
-40%
Child M.
- 1 0%
0
10%
40%
1 0-12 Hz
80%
1 00%
BASELINE
2 Hours
24 Hours
after
N a l trexone
after
Naltrexone
ERS
90
CONCEPTUAL BACKGROUND
91
PET Scans
92
CONCEPTUAL BACKGROUND
0::
0
0::
w
1z
<(
Figure 5.4. Horizontal PET (positron emission tomography, left) and MRI (magnetic
resonance imaging, right) images through the brain of normal indiv:iduals and those
exhibiting obsessive-compulsive disorder. The MRI scans indicated that no structural
differences were evident. However, the functional PET scans of brain glucose uptake
indicate hypermetabolism in medial frontal areas of the brain where behavioral plans are
generated. Each reflects computer-averaged images from 1 0 individuals. These images
were kindly provided by Dr. Gordon Harris of the New England Medical Center. (A full
description of these findings iS in Harris & Hoehn-Saric, 1995; see n. 50.)
93
94
CONCEPTUAL BACKGROUND
95
96
CONCEPTUAL BACKGROUND
Suggested Readings
Bruni a, C. H. M., Mulder, G., & Verbaten, M. N. (eds.)
(1991). Event-related brain research. New York:
Elsevier.
Neurodynamics
Neurochemical Maps of the Brain
The intention is to furnish a psychology that shall be a natural science: that is, to
represent psychical processes as quantitatively determinate states of specifiable
material particles, thus making those processes perspicuous and free from con
tradiction. , . The neurons are to be taken as the material particles.
Sigmund Freud, Project for a Scientific Psychology ( 1895)
CENTRAL THEME
raphy.
97
98
CONCEPTUAL BACKGROUND
DNA
l
l
l
TRANSCRIPTION
RNA
TRANSLATION
EVERYTHING
ELSE
F ig u re 6 . 1 . Summary of the current "central dogma"
that underlies the analysis of all biological processes,
including those that mediate basic psychobiological
processes. The only major concept missing from this
schematic is the environment, and these influences
permeate all phases of these transactions.
99
Acety i C o A
C h o l i ne
P R E- S Y N A PT I C
ENDING
Acety l c h o l i n e
C h o l i n esterase
Acetyl
Choline
POST-S Y N A PTIC
E N DI N G
100
CONCEPTUAL BACKGROUND
101
Galanine (Memory)
NPY (Feeding, Hunger)
Growth of Knowledge
Dynorphin (Hunger)
Concerning
B-Endorphin
Neuropeptide Control
of Behavior
[!!']
-J"'-"'
Oxytocin
Angiotensin
Substance P
Bradykinin (Pain)
- - - - - - - - - - - - - - - - - - - - - -
--------
1 960
1965
1 970
1 975
1 980
1 985
YEAR OF DISCOVERY
Figure 6.3. Time line of the discovery of major neuropeptides that participate in various
brain functions related to the control of behavior and various emotional and motivational
processes. Progress was slow in the beginning (dotted line) but sped up enormously
around 1970. The numbers inside squares indicate the number of amino acids in each of
these neuropeptides.
102
CONCEPTUAL BACKGROUND
Table 6 . 1 . Relationships between Some Neuropeptides and Their Peripheral and Central Functions
Peptide
Peripheral Function
Central Function
Thirst and water intake
Angiotensin
LH-RH
Sexual readiness
Oxytocin
CRF
oc-MSH
TRH
Metabolic arousal
Vasopressin
Memory retention
Behavioral persistence
Male sexual behavior
Somatostatin
103
104
CONCEPTUAL BACKGROUND
Neurochemical Systematics
For organizational purposes, I will categorize brain neu
rotransmitter systems15 into four categories: (1) amino
acids that undergo only minor modification when em
ployed as transmitters, (2) the enzymatically modified
amino acids, known-as the biogenic amines, (3) the chains
of amino acids known as neuropeptides, and (4) a mis
cellaneous gro.u p including ACh and a variety of other
items. For instance, as mentioned, there are gaseous trans
mitters, ones that may emerge ftom fatty acids, and it
remains possible that certain common metabolic inter
mediaries such as glucose may also participate in infor
mation transmission in the brain. 16 These latter items will
not receive much attention here, since most do not yet
interface clearly with emotional issues.
1 . The simplest, and perhaps most abundant, items
are the amino acid transmitters. The main excitatory
transmitter, whose task is to initiate neuronal firing, is
glutamate, essentially the same substance commonly
used to add t1avor to foods, especially in oriental cook
ing. There is reason to believe it participates in virtually
all brain functions, with memory being the focus of much
current research.17 It is tempting to speculate that in the
"primordial soup" in which life on earth presumably
originated, glutamate was one of the most useful and
abundant nutrients available. Early cells developed a
sense for it, a "taste" if you will, which eventually al
lowed it to serve as a neurotransmitter in brain circuits.
Glutamate is the most common and abundant excitatory
transmitter in the mammalian brain, and it is usually syn
thesized from the precursor amino acid, glutamine. Con
versely, its metabolic product, GABA, is the most abun
dant inhibitory transmitter in the brain, and it functions
as widely as glutamate. However, in contrast to gluta
mate, which is abundant throughout the body, GABA is
not a widely distributed amino acid, essentially existing
only within the brain. There it is synthesized from gluta
mate via a single decarboxylation step that is mediated
by the enzyme glutamic acid decarboxylase. Because of
this tight metabolic interconnection between brain
glutamate and GABA, brain inhibition and excitation can
TYROSINE
Tyrosine
TRYPTOPHAN
5-HTP
Decarboxylase
DOPAMINE
Tryptophan
Hydroxylase
L-DOPA
D A - 13 Hydroxylase
NOREPINEPHRINE
Pre-synaptic
Endings
SEROTONIN
Synaptic Cleft
R
CATECHOLAMINE
SYNAPSE
105
Post-synaptic
Endings
I N DOLEAMINE
SYNAPSE
NOREPINEPHRINE
(Function: Sustains high signal/noise ratios
107
SEROTONIN
VB"l
'--- A1 - A5
BF
(Function:
.rA10
MUMC VTA
...____./
DOPAMINE
Ch1 - Ch4
(Function: Mediates attention and arousal
in all sensory systems)
ACETYLCHOLINE
Figure 6.5. Parasaggital depictions of the dispersions of acetylcholine and biogenic amine
(dopamine, norepinephrine, and serotonin) systems in the rat brain. LC: locus coeruleus;
DB: dorsal noradrenergic bundle; VB: ventral noradrenergic bundle; CN: caudate nucleus;
AC: anterior commissure; OB: olfactory bulb; CTX: cortex; BF: basal forebrain; HC:
hippocampus; TH: thalamus; SC: superior colliculus; IC: inferior colliculus; NS:
nigrostriatal pathway; ML/MC: mesolimbic and mesocortical pathways; HY: hypothala
mus. "A" designations indicate major norepinephrine and dopamine cell groups; "B"
designations indicate major serotonin/raphe cell groups; "Ch" designations indicate major
cholinergic cell groups.
Central Catecholamines:
Arousal Systems of the Brain
In the previous chapter, I described some aspects of the
organization of brain DA systems. DA is just one of a
109
110
CONCEPTUAL BACKGROUND
L - TYROSINE
111
112
CONCEPTUAL BACKGROUND
B-ENDORPH I N
08
VASOPRESSIN/OXYTOCIN
(Functions: AVP promotes male-typical persistence;
Oxytocin, female-type nurturance and acceptance)
CHOLECYSTOKININ
(Functions: Regulation of emotional systems:
feeding, sex, exploration, anxiety, and pain)
Figure 6.7. Parasaggital depiction of the dispersions of fom major neuropeptide systems.
LC: locus coeruleus; DB: dorsal noradrenergic bundle; VB: ventral noradrenergic bundle;
CN: caudate nucleus; AC: anterior commissure; OB: olfactory bulb; CTX: cortex; BF:
basal forebrain; HC: hippocampus; TH: thalamus; SC: superior colliculus; IC: inferior
colliculus; CC: corpus callosum; POA: preoptic area; VTA: ventral tegmental area. Small
circles in the cortex indicate the presence of local interneurons for CRF and cholecystoki
nin systems.
113
114
CONCEPTUAL BACKGROUND
115
In Vivo Volta.metry
Subtractive Autoradiography
Push-Pull Approaches
In Situ Hybridization
1 1 6 CONCEPTUAL BACKGROUND
AMYGDALA
AFTERTHOUGHT: The Neurochemistry of
Some Emotional Processes
MEDIAL RAPHE
INFERIOR COLLICULUS
117
1 1 8 CONCEPTUAL BACKGROUND
opened up a Pandora's box-or a treasure chest, de
pending on your perspective-of ways to modify the
moods and emotions of humans by pharmaceutical
means. For a summary of opioid receptor distributions,
see Figure 6.8.
Down through the ages, two of the most emotion
ally attractive types of drugs have been narcotics, such
as morphine and heroin, and psychostimulants, such as
cocaine and more recently the amphetamines. We nbw
understand why people and animals are strongly at
tracted to voluntarily self-administer these agents. The
drugs interact with specific receptors in the brain that
normally help mediate various pleasures and psychic
excitement.
Although there are many environmental and psy
chosocial reasons for people to take such drugs, ulti
mately the only reason there is heroin addiction is be
cause the brain contains mu-opiate receptors. These
receptors normally control an animal's urges to main
tain various brain and bodily balances (i.e., homeostatic
balance) via feeding, sexual/social behavior, and so
forth. The psychic reflections of doing "the right thing
biologically" are feelings of satisfaction and pleasure
(see Chapter 9). Which of the many brain opiate sys
tems actually mediate this subjective feeling is not well
understood, but animals will self-administer opiates
directly into various parts of the biain. The most effec
tive locations are in the brain stem, near the central gray
of the midbrain, and the ventral-tegmental area, where
the A l O mesolimbic DA cells are situated.
Cocaine and amphetamine produce their psychic
appeal via this same system-namely, by increasing DA
availability at synapses of the mesolimbic circuit. Ifthis
system is damaged, self-administration ofpsychostimu
lants declines. One of the normal functions of this sys
tem is to energize appetitive behavior (see Chapter 8).
Thus, it is no wonder that humans develop a strong
craving for these drugs, since the normal function of
the underlying brain system is to facilitate a general
ized form of appetitive behavior. Through the availabil
ity of psychostimulant drugs, animals can directly acti
vate the brain systems that normally motivate them to
explore and investigate their world and to vigorously
pursue courses of action. When they get into the vicious
cycle of self-stimulating this system, everything else in
the world decreases in their value hierarchy. The psy
chic appeal of cocaine seems to be mediated by the
dopamine reuptake site, since knockout mice without
this receptor do not appear to desire psychostimulants.76
Also, it should be noted that the euphoria and craving
that are induced by elevated DA at synapses apparently
are due to interactions with one type of receptor (0 )
2
rather than the other major variant of the dopamine re
ceptor (D 1 ) 77
.It is likely that certain addictive behaviors in hu
mans, such as compulsive gambling, are strongly con
trolled by internal urges that are generated by dopam-
119
EPINEPHRINE
"'
- - HYPOTHA L A M I C-SYMPAH
R ES P O N
:>'\
:::>
0
0
.,
""
;?
,.
'""
t>o rJl
' "
0 ...
t =:s:
"'
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"
Vl
0
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"
""
"'
"q
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,
0
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- ...._..
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'
Suggested Readings
Bousfield, D. (ed.) (1985). Neurotrcmsmitters in action.
New York: Elsevier.
Cooper, J. R., Bloom, F. E., & Roth, R. H. ( !995). The
biochemical basis of neuropharmacology. New
York: Oxford Univ. Press.
Costa, E., & Greengard, P. (eds.) ( ! 969- 1984). Ad
vances in biochemical psychopharmacology, vols.
1-39. New York: Raven Press.
Feldman, R. S., & Quenzer, L. F. ( ! 984). Fundamen
tals of neuropsychopharmacology. Sunderland,
Mass.: Sinauer.
Ganten, D., & Pfaff, D. (eds.) ( ! 990). Behavioral as
pects of neuroendocrinology: Current topics in
neuroendocrinology, vol. 10. Berlin: Springer
Verlag.
120
CONCEPTUAL BACKGROUND
PART II
I n the preceding chapters, we have seen the great esteem that Nobel Commit
tees have had for major advances in our basic understanding of how the brain
functions. Most of the recognition has gone to individuals who have worked out
mechanisms that have broad implications for understanding neural actions. By com
parison, the pursuits of individuals who have worked on the integrative functions
of the whole brain have not been comparably lauded. The work of Hess was an
exception. When recognition for integrative work was offered again, it went not
to the behaviorists who had been working on the nature of learning but to the
ethologists who had been working on. the spontaneous behavior patterns of ani
mals. In appreciation of the fact that an understanding of instinctual processes is
of first-order importance for understanding brain functions, in 1973 the Nobel
Committee recognized the work of Konrad Lorenz, Nico Tin bergen, and Karl Von
Frisch, the founding fathers of modern ethology "for their discoveries concerning
organization and elicitation of individual and social behavior patterns. "
The work of these ethologists has generated lasting understanding of behav
iors in our fellow animals. Lorenz characterized the rapid imprinting or social at
tachment processes that emerge between mother geese and their offspring soon
after birth. He also found that under artificial conditions this type of social bond
ing or preference would develop for members of other species, including Lorenz
himself. Tin bergen demonstrated that animals are prepared to respond in stereo
typed ways to certain aspects of their environments. For instance, young seagulls
would beg for food by pecking the feeding spot on the bills of inanimate models
that barely resembled the beaks of their parents. He also demonstrated that such
"sign stimuli" also existed in stickleback fish, which exhibited aggression simply
toward the bulging red belly of a model fish. Von Frisch was the first to work out
the innate communication system of another species, namely, the ability of hon
eybees to inform other members of their hive about the location of food sources
by performing a "waggle dance." I n fact, the ethological tradition represented
by these works goes back to the 1872 classic The Expression of the Emotions in
Man and Animals, in which Charles Darwin promoted analysis of the various
emotional behavior patterns animals and humans exhibit in nature, a tradition that
is being pursued vigorously to this day through the analysis of facial expressions
of emotions in humans and postural expressions.of emotions in animals.
For a while, ethology, this uniquely European tradition of studying animal be
havior, provided a credible alternative to the traditions started by American be
haviorists, such as J. B. Watson and B. F. Skinner. While behaviorism pursued the
general research strategy of observing the learning behavior of animals in artifi
cial environments, the ethologists sought to clarify how animals spontaneously
122
behaved in their natural environments. For many years, ethologists and behav
iorists quarreled over which was the proper approach.
We now recognize that each was partially right. Ethology deals more effectively
with the relatively " closed programs" of the brain, and behaviorism deals better
with the more "open programs" that permit behavioral flexibility via new learning.
The two finally started to come together when it was realized that the so-called
misbehavior of organisms (see Chapter 1 ) arose from the fact that in the midst of
difficult learning tasks, animals would often tend to revert to their instinctual be
havioral tendencies. Likewise, it was gradually recognized that animals are " pre
pared" to learn certain things more easily than others. In other words, evolution
had constructed different animals to subsist best in different environments.
Although both traditions provided many new and lasting " laws of behavior, "
until q uite recently, neither tradition tried to link itself to the other or to brain re
search. Both now recognize that their scientific future is limited if they do not
cultivate connections to neuroscience, and so the powerful new disciplines of
neuroethology and behavioral neuroscience have emerged. Mainstream psychol
ogy is also slowly coming to realize that it must pay closer attention to the nature
of the brain in order to make progress in understanding the causes of basic psy
chological processes.
It is becoming increasingly clear that humans have as many instinctual operat
ing systems in their brains as other mammals. However, in mature humans such
instinctual processes may be difficult to observe because they are no longer ex
pressed directly in adult behavior but i nstead are filtered and modified by higher
cognitive activity. Thus, i n adult humans, many instincts manifest themselves only
as subtle psychological tendencies, such as subjective feeling states, which pro
vide internal guidance to behavior. The reason many scholars who know little about
modern brain research are still willing to assert that human behavior is not con
trolled by instinctual processes is because many of our operating systems are in
fact very "open" and hence very prone to be modified by the vast layers of cog
nitive and affective complexity that learning permits. Still, the failure of psychol
ogy to deal effectively with the nature of the many instinctual systems of human
and animal brains remains one of the great failings of the discipline. The converse
could be said for neuroscience.
I nstinctual operating systems of the brain must underlie sophisticated human
abilities. For example, the general urge and ability of young children to pick up
language is instinctual (i.e., based on specific brain operating systems that are
coming to be well understood; see Appendix B). Of course, these genetically pro
vided abilities are remarkably "open" and hence permeable to many environmental
influences, so that the end results exhibit incredible diversity of external forms in
the real world. However, diversity is always supported from below by a variety of
shared mechanisms. When the underlying brain programs are damaged in adults,
language abilities are predictably impaired. As linguist Noam Chomsky has force
fully argued, there is a "deep linguistic structure" in the human brain , which un
folds spontaneously during early development, giving a distinctive human stamp
to all human languages around the world. Here I will begin to analyze the propo
sition that human emotions are controlled likewise-by the deep structure of emo
tional circuits that we still share with other animals. The best way to understand
these emotional systems in human brains is to analyze the corresponding emo
tional behavior patterns generated by animal brains.
Before discussing the details of some of the emotive systems in animal brains,
let me first summarize the perspective developed so far. The basic emotions ap-
pear to arise from executive circuits of the brain that simultaneously synchronize
a large number of mental and bodily functions in response to major life-challeng
ing situations. Although many emotional nuances can be "socially constructed"
by the human mind, usually designed by the textures of specific human cultures,
the affective strength of the basic emotions arises from intrinsically " motivating"
neurophysiological properties of genetically ordained subcortical emotive systems.
Since brain emotive systems were designed through evolutionary selection to
respond in prepared ways to certain environmental events, it often seems from
our "mind's-eye" perspective that world events are creating emotions as opposed
to just triggering evolutionarily prepared and epigenetically refined states of the
brain. In fact, many of the feelings and behavioral tendencies that characterize
the basic emotions reflect, more than anything else, the intrinsic, genetically pre
pared properties of brain organization. Although the underlying emotional circuits
influence and guide learning, their initial adaptive functions were to initiate, syn
chronize, and energize sets of coherent physiological, behavioral, and psychological
changes that are primal instinctive solutions to various archetypal life-challenging
situations. The subjective experience of emotions presumably allows organisms
to code the value of environmental events so as to facilitate the expression of
various learned behaviors.
In the second part of this book, I will discuss five types of emotional and mo
tivational systems that all mammals share. I discuss ( 1 ) the concept of " state con
trol systems" as highlighted by an analysis of the sleep-waking mechanisms in
the context of which all behavior has to occur; (2) how SEEKING circuits for inter
est, curiosity, and eager anticipation help generate expectations and direct ani
mals to the positive rewards to be had from the environment; (3) how those sys
tems help maintain physical "drive" states, such as water and energy balance,
which need to be regulated, in part, by behavioral means via interaction with
specific environmental " incentives" ; (4) RAGE circuits for anger and impassioned
aggression that help counter irritations, frustrations, and other threats to one's
freedom of action; and (5) various FEAR and anxiety circuits that help protect an
animal from physical harm. Although there are many other social-emotional and
motivational systems in the brain, as summarized in the final third of this text, the
systems covered in this section provide a solid cross-species foundation for the
complexities to follow.
123
CENTRAL THEME
Shakespeare proposed one possible function of sleep
when he suggested that it "knits up the raveled sleeve
of care.'' A great number of functions have now been
attributed to sleep and dreaming, but few have been
definitively demonstrated with the tools of science.
One thing is certain, though. Each day our lives cycle
through the master routines of sleeping, dreaming, and
waking. All our activities are guided by the age-old
rhythms of nature, and many neural mechanisms as
sure that we remain in tune with the cycling of days
and nights across the seasons. Our brains contain en
dogenous daily rhythm generators and also, perhaps,
calendar mechanisms that respond to monthly lunar
cycles, as well as the transit of the seasons. Brain sci
entists have been. especially eagerto study the mecha
nisms that control these processes, and our various
states of vigilance have been pursued vigorously thanks
to highly objective electroencephalographic (EEG) pro
cedures to monitor the brain in action. During waking,
the EEG is typically full of low-amplitude, high-fre
quency beta waves, which indicate that the brain is
processing information. As one goes into q uiet sleep,
which deepens through several stages, the cortex ex
hibits increasingly large high-amplitude slow waves.
This reflects a brain state where very little active pro
cessing is transpiring. Slow wave sleep (SWS) is typi
cally followed by a highly activated form of sleep, ac
companied by cortical arousal (more energized than the
waking EEG), a flaccid muscular paralysis (atonia), and
rapid eye movements accompanied by vivid dreaming
(i.e., rapid eye movement [REM] sleep). It is generally
believed that SWS reflects ongoing bodily repair pro-
125
127
128
129
130
1 31
sws
GROWTH H.
Figure 7 .2. Overview of the types of brain transections that led to the general
locations of major waking, SWS, and REM systems within the neurO- axis. For
instance, with the midpontine pretrigeminal cut, waking and SWS were left in the
forebrain, while the potential for REM was only manifested in neural and bodily
systems below the cut. Whenthe cut was slightly further rostral, through the
midbrain (i.e., the cereveau iso!J cut), the forebrain remained perpetu-ally in the
darkness of SWS, while tissue below the cut cycled between waking type arousal
and activated sleep states. Also, note that growth honnone secretion from the
pituitary occurs in conjunction to SWS episodes, while ACTH secretion is
entrained to REM periods.
133
134
135
sws
REM SWS
REM
sws
i E-
137
WAKING
EXCITATION
. . . : /;:
;/
.
--- -- - -----
-- .
(\
.(:, . . ;
M
UJ
_,
w
>
: .. . . .
I . . .
ACTH
\CO RTISOL
\,.,
__
_
a:
0
:r
TIME
Figure 7.3. Patterns of hormone secretion (bottom) and possible neurochemical changes
(top) as a function of cycling stages of SWS and REM. Different phases of sleep probably
promote different types of brain and body restoration. It is possible that the successive
phases of SWS and REM help regulate overall excitatory and inhibitory potentials in the
brain so as to sustain a balance of neurochemistries to help mediate coherent behaviors
during waking. (Adapted from Panksepp, 1 98 1 ; see n. 99.)
138
139
141
Possible Neurochemical
Functions of REM
It is generally agreed that sleep stages have some type
of restorative effects on the neurobiological functions
of the brain. The most common hypothesis has been that
they allow certain transmitters to be rejuvenated. The
most well-developed idea has been that brain NE is
restored during REM. 97 Even though no support has
been found for this idea when brain levels of NE are
measured, it is possible that REM selectively facilitates
synaptic efficacy. In other words, REM may control NE
postsynaptic receptor regulation, and it has been found
that during waking, when NE systems are active, brain
NE receptor sensitivity does decline. Conversely, dur
ing REM sleep, when NE neurons cease firing, there is
an up-regulation of receptors, promoting restoration of
normal synaptic transmission.98 Parenthetically, these
findings do seem paradoxical from the perspective that
REM deprivation can alleviate depression (i.e., some
antidepressants also facilitate NE activity), but it is no
doubt the case that REM helps restore many other neu
rochemical systems, including presumably some that
intensify negative affect. Also, it is possible that REM
helps solidify affectively negative cognitions, which can
then intensify depressive episodes.
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142
AFTERTHOUGHT: Activities of
Neurochemically Characterized
Neurons and Hallucinations
In Chapter 6, I discussed the geographies of the major
biogenic amine systems of the brain: norepinephrine,
dopamine, and serotonin. Since such biogenic amine
neurons are tightly clustered in the brains of rats, it has
been possible to characterize the neuronal activities of
each of these systems during the various vigilance
states. The results have been clear and striking.
Brain NE and 5-HT systems exhibit their highest
levels of activity during waking. They slow down sub
stantially during SWS, and a few moments prior to
REM they cease firing and remain inhibited through
out the ensuing REM period.104 In short, they are inac
tive during dreaming. By comparison, DA cells show
comparatively little change from one vigilance state to
the next, even though they begin to exhibit bursts of
firing when animals seek rewards. Otherwise, they fire
at a steady rate throughout waking, SWS, and REM,
Suggested Readings
Binkley, S. ( 1 990). The clockwork sparrow: Time,
clocks, and calenders in biological organisms.
Englewood Cliffs, N.J.: Prentice-Hall.
143
CENTRAL THEME
The desires and aspirations of the human heart are end
less. It is foolish to attribute them all to a single brain
system. But they all come to a standstill if certain brain
systems, such as the dopamine CDA) circuits arising
from midbrain nuclei, are destroyed. Such was the trag
edy that overtook Leonard L. in his childhood, and it
was not until he was a grown man that he was able to
partake again of worldly delights. What allowed him
to achieve the feelings of success described by Sacks
was L-DOPA, the precursor of DA This medicine had
already alleviated the psychomotor problems of ordi
nary parkinsonian patients, who had weaker forms of
deterioration in their ascending DA systems. ln such
individuals L-DOPA can dramatically alleviate the in
ability to initiate movements, allowing them to enjoy
everyday pleasures. Now we know that ascending DA
tracts lie at the heart of powerful, affectively valenced
neural systems that allow people and animals to oper
ate smoothly and efficiently in all of their day-to-day
pursuits. These circuits appear to be major contribu
tors to our feelings of engagement and excitement as
we seek the material resources needed for bodily sur
vival, and also when we pursue the cognitive interests
that bring positive existential meanings into our lives.
Higher areas of the motor cortex are also energized into
action by the presence of DA Without the synaptic
"energy" of DA, these potentials remain dormant and
stilL Without DA, human aspirations remain frozen, as
it were, in an endless winter of discontent. DA synapses
resemble gatekeepers rather than couriers that convey
detailed messages. When they are not active at their
posts, many potentials of the brain cannot readily be
144
145
MOTOR OUTPUT
GENERAL AROusAL
I"ORWARO LOCO
MOnON
2. EXTERNAL STIMULI
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147
149
150
1 51
152
153
154
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Figure 8 . 2 . Relative
frequencies of "stimulusM
bound" appetitive behaviors
in quadrants of the hypothalaM
mus, with horizontal and
vertical coordinates running
through the fornix bundle.
(Reprinted with permission
from Panksepp, 198 1 ; see
chap. 3, n. 25.)
( J
VENTRAL
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Figure 8.3. Changes in neuronal activity during simple appetitive learning consisting of a
tone followed by food one second later. (A) summarizes behavioral changes and learned
neuronal changes during acquisition of the task. (B) summarizes the temporal sequence
with which brain areas start to exhibit neuronal changes in the well-trained animal.
(Adapted from Panksepp, 1 9 8 1 ; see chap. 3, n. 25.)
159
Trials 1 90-1 99
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Figure 8.5. Elaboration of sniffing in rats working for rewarding brain stimulation on
a fixed-interval schedule of reinforcement. It is noteworthy that spontaneous sniffing
increased markedly one second prior to the first lever press within each response
segment. This suggests that the brain substrates that arouse sniffing, namely, the
circuits of the SEEKING system, mediate appetitive behavior patterns seen when
animals are required to exhibit operant responses in order to obtain food. It should be
noted that the theta rhythm, which invades the hippocampus when it is integrating
information, is of the same frequency as sniffing, and the neuronal systems that activate
theta arise from the brain stem and course through the lateral hypothalamus. (Reprinted
with permission from Panksepp, 1 98 1 ; see chap. 3, n. 25.)
1 61
162
AFTERTHOUGHT: Self-Stimulation
and Dreaming
Jn the previous chapter, I focused on possible relation
ships between schizophrenia and dreaming. As we have
now seen, there is also a credible linkage between
schizophrenia and SS. Accordingly, one might predict
that there is an intimate relationship between SS and
. dreaming. Indeed, interesting connections between the
two have been found in REM-deprived animals. REM
deprivation in rats leads to an increased sensitivity of
the LH-SS system: Animals work at higher rates for
lower current levels, as if REM deprivation sensitized
the substrates of the SS system.101 Conversely, it has
also been found that allowing animals to self-stimulate
for a few hours during the course of ongoing REM dep
rivation eliminates the need for subsequent REM recov
ery sleep. In other words, the drive for increased levels
of REM following REM deprivation is apparently dis
charged by allowing animals to self-stimulate during the
deprivation period.
It is noteworthy that schizophrenics also fail to ex
hibit compensatory elevations of REM sleep following
imposed periods of REM deprivation.102 Thus, there
appears to be a fundamental relationship between the
schizophrenic process and the neuropsychological (emo-
1 63
Suggested Readings
Le Moal, M., & Simon, H. ( 1 991). Mesocorticolimbic
dopaminergic network: Functional and regulatory
roles. Physiol. Revs. 7 1 : 155-234.
Liebman, J. M., & Cooper, S. J. (eds.) ( 1 989). The
neuropharmacological basis of reward. Oxford:
Clarendon Press.
Olds, J. ( 1 977). Drives and reinforcements: Behavioral
studies ofhypothalamicfunction. New York: Raven
Press.
Panksepp, J. ( 1 9 8 1 ). Hypothalamic integration of be
havior: Rewards, punishments, and related psycho
logical processes. In Handbook of the hypothala
mus. Vol. 3, Part B, Behavioral studies of the
hypothalamus (P. J. Morgane & J. Panksepp, eds.),
pp. 289-431 . New York: Marcel Dekker.
Plutchik, R., & Kellerman, H. (eds.) ( 1 986). Emotion:
Theory, research, and experience. Vol. 3, Biologi
cal foundations of emotion. New York: Academic
Press.
Rolls, E. T. ( 1 975). The brain and reward. Oxford:
Pergamon Press.
Routtenberg, A (ed.) ( 1 980). Biology of reinforcement:
Facets of brain stimulation reward. New York:
Academic Press.
Schultz, S. C., & Tamminga, C. A . (eds.) ( 1 989).
Schizophrenia: Scientific progress. New York:
Oxford Univ. Press.
Valenstein, E. S . (ed.) ( 1 973). Brain stimulation and
motivation. Glenview, Ill.: Scott, Foresman.
Wauquier, A., & Rolls, E. T. (eds.) (l976). Brain-stimu
lation reward. Amsterdam: North-Holland.
ENERGY I S DELIGHT
Energy Is Delight
The Pleasures and Pains
of Brain Regulatory Systems
As the human understanding surpasses that of the ape, and that of the ape surw
passes that of the fishes, so in almost as extreme a degree the vertebrate brain
surpasses the nervous organs of the invertebrates. A reason for this difference,
one thinks, is to be found in history, and in a very elementary biological fact.
All animals are dependent on either plants or animals for food, and from its
beginnings the evolution of the animal kingdom has in the main presented a
pageant of predator and prey-eat or be eaten!
H. W. Smith, From Fish to Philosopher ( 1 953)
CENTRAL THEME
Mammals can survive only if they maintain relative
constancy of various bodily processes, including oxy
gen and carbon dioxide content in blood, body water
levels, salt and energy balance, and body temperature.
Complex brain and body systems sustain these con
stancies, and the overall concept used to describe this
ability is homeostasis. Some people prefer the word
heterostasis, since the level of regulation sometimes
changes as a function of environmental conditions as
well as internal bodily cycles (e.g., 24-hour rhythms).
Homeostasis is sustained by a diversity of mechanisms
ranging from rapid physiological changes, such as re
flexive modification of breathing rate as a function of
oxygen need (which is actually signaled to the brain
by carbon dioxide buildup in the bloodstream), to in
stinctual behavioral tendencies, such as an animal's
urge to seek resources needed for longerterm survival,
including food, water, warmth, and micronutrients such
as vitamins and minerals. Bodily needs instigate distinct
forms of bodily arousal and psychological feelings of
distress such as h unger, thirst, and coldness. Animals
have exquisite sensory systems to identify the most
important items they need-for example, the ability to
taste sweetness identifies foods laden with sugar, and
saltiness identifies sources of sodium. Jt is commonly
believed that color vision evolved, in part, to help pri
mates identify the ripest fruit. The needed items that
cannot be identified by taste-for instance, many vi-
164
165
166
ENERGY I S DELIGHT
1 67
Regulatory Behaviors
and the SEEKING System
As we saw in Chapter 8, the SEEKING system can
motivate animals to pursue a diversity of distinct re
wards in the environment. The nervous system does
most of this automatically, with no obvious delibera
tion. Many bodily needs access the SEEKING system
and thereby arouse appetitive search tendencies that
motivate animals to approach and learn about available
resources. It would have been wasteful for evolution to
have constructed separate search and approach systems
for each bodily need. The most efficient course was for
each need-detection system to control two distinct func
tions: a generalized, nonspecific form of appetitive
arousal and various need-specific resource-detection
systems. In addition, learning would increase the effi
ciency with which the SEEKING system could guide
animals to appropriate goal objects. This is, in fact, what
transpires in the mammalian brain.
Thus, resource depletions within the body can lead
to a generalized arousal of seeking behaviors regard
less of the specific regulatory imbalances that exist, and
specific need states that sensitize distinct consumma
tory reflex tendencies (e.g., licking, biting, chewing, and
HO ME OSTATIC INP UT
S INT O A
GE NE RA LIZ ED SE EK
ING SYSTEM
PATHWAYS
NON-SPECIFIC
SYSTEMS
BRAIN-STEM CONSUMMATORY
REFLEX CONTROL AREAS
MEDIAL HYPOTHALAMIC
HOMEOSTATIC DETECTORS
Figure 9 . 1 . A conceptual schematic of how specific regulatory detector systems in the
medial hypothalamus access a shared SEEKING system in the lateral hypothalamus.
(Adapted from Panksepp, 198 1 ; see n. 5.)
168
ENERGY IS DELIGHT
nivores, on the other hand, must stalk, chase down,
pounce upon, and kill their quarr before they have an
.
opportunity to grg.e on energy-nch eals. Parnt eu
.
cally, it is more dtfflcult to obtam conststent self-stimu
lation from the LH of cats than of rats, perhaps because
of the predatory foraging style of carnivores. The high
degree of behavioral inhibition necessary for stalking
followed by rapid pursuit may be incompatible with
vigorous self-stimulation behavior.
.
Although the goal of energy balance regulatiOn can
achieved
by
a
variety
of
easily
observed
behavior
be
patterns-from the consumption of one meal a day to
continual nibbling-the nature of the regulated pro
cess is not as evident. The essence of energy regula
tion is well hidden from scientific view, apparently
in the deep metabolic recesses of the hypothalamus.
Because of the difficulty of studying such hidden pro
cesses, investigators have generally focused on the
clear and measurable characteristics of feeding pat
terns, rather than on the intrinsic nature of internal
processes that can only be inferred from outward be
havioral signs. Indeed, for a long time it was assumed
that if we carefully study the relationships between
meals and intermeal intervals, special insights would
emerge concerning the underlying regulatory pro
cesses. This hope has been fulfilled only marginally,
since the balancing of energy intake is typically only
accurate in the long term, with many inaccuracies in
the short term. One reason that individual meals tell
us rather little about the regulatory mechanisms of the
brain is because regulatory patterns change during the
animal's circadian metabolic cycles. In addition, many
other psychological processes, from fear to pleasure
mechanisms, can easily subvert the brain's regulatory
actions for extended periods. For instance, fearful
animals eat little-. On the other hand, animals take large
meals if their food is especially tasty but become fin
icky nibblers if it is not. They also take large meals if
food is hard to find but tend to make many small meals
if food is abundant.14
Let us consider in some detail one example of why
asingle meal may tell us little about regulation. Omni
vores, such as rats and humans, are opportunists. If
given sudden access to rich and appealing food, they
typically gorge like carnivores, with little heed for their
immediate energy needs. This "dessert effect" makes
the analysis of overall energy regulatory processes prob
lematic unless one uses constant dietary conditions,
which obviously makes human research especially dif
ficult. Humans actively seek culinary variety, which can
temporarily override regulatory signals. The variabil
ity in short-term regulation also appears to be greatest
among individuals who have a constitutional tendency
toward obesity and those who follow sedentary life
Styles. Likewise, if rats living in small cages are given
continuous access to a variety of tasty foods, compa
rable to a typical human diet (the so-called supermar-
169
ENERGY IS DELIGHT
C A L O R I C A DJ U STME NT OF F E E D I N G
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172
ENERGY IS DELIGHT
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173
Day 4
10
20
30
40
50
60
70
80
90
100
Time ( ho u rs )
Figure 9.5. Average daily feeding cycle across three to four days in a group of 10
normal rats and 10 diabetic rats given free access to food. The satiety ratios
(postmeal interval/meal size) reflect the duration of feeding inhibition for each unit
of food eaten. The low points indicate where the animal is eating many meals that
do not quell its appetite for a long period, while the peaks reflect periods during the
day when the animal eats fewer meals and the meals are much more satiating. The
equations reflect the best-fitting cosine function for these results. (Adapted from
Panksepp, 1978; see n. 32.)
174
ENERGY IS DELIGHT
175
one side of the equation are balanced by compensatory suggests that the circulating metabolic signals were
changes on the other side.
integrated as if each animal was contributing one half
Although most investigators assume that an energy of a critical signal to the other's brain. The critical area
regulatory mechanism exists somewhere in the hypo
of the brain that probably receives this signal is the
thalamus, our knowledge about its precise nature re ventromedial hypothalamus (VMH). VMH lesions have
mains incomplete. A key question that needed to be
long been known to produce overeating and eventual
answered before one could actually study the regula
obesity, and when a VMH-lesioned animal was joined
tory mechanisms in the brain was: What is regulated?
to a normal nonlesioned partner, the results were strik
There have been many proposals concerning the major
ing. The VMH-lesioned animals were not affected by
signals that may mediate the homeostatic control of the signal emerging from the neurologically normal
feeding, including glucostatic, aminostatic, lipostatic,
"Siamese twins." On the other hand, the normal part
and thermostatic theories of regulation. These perspec
ners detected too much of a repletion sigrial from the
tives viewed blood sugar, blood amino acids, some as
VMH-lesioned animals. While the VMH-lesioned ani
pect of adipose tissue metabolism, or the overall abil mals still overate and became obese, their partners lost
ity of the body to maintain a consistent temperature to their appetite completely and became emaciated.
be the regulated variables.42
We still do not know exactly what the fat-repletion
Although all ofthese factors surely participate in feed
signal is in this situation, although it might arise from
ing control, the common denominator for longtenn regu the leptin protein mentioned earlier, since normal ani
lation appears to be the overall ability of the body to
mals parabiosed to an oblob animal also lose weight.
sustain energy metabolism. Hence anenergostatic theory
However, such weight patterns may also reflect meta
has been proposed by sevet:al investigators as the "cen
bolic energy from the excessive eating of the VMH
ter of gravity" around which feeding behavior and bodily
animal as it is monitored by the long-term energy inte
energy balance are regulated.43 The basic evidence for grator in the VMH of the normal animal. In other words,
this theory is that animals adjust their daily food intake if the brain's integrative systems sense more meals com
quite well when a proportion of their daily energy need
ing into the body than are actually consu:ffied, feeding
is administered directly into their stomach, regardless of behavior may be reduced.
the energy source. If animals are given a sufficient
The second finding was related to the long-standing
amount of time to adjust, the compensation is quite pre assumption that the VMH senses some type of "satiety
cise and comparable for all the major macronutrients signal" that normally terminates bouts of feeding (Fig
fats, proteins, and carbohydrates (Figure 9.2). However,
ure 9.7). This part of the brain clearly contains gluco
this does not really tell us much about the exact mecha
receptive neurons, but, surprisingly, direct administra
nisms by which the regulation is achieved.
tion of glucose into this brain area does not reduce the
In general, how might the brain's energy balancing size of subsequent meals. Animals without this brain
mechanism work? Conceptually there are two possibili
area fail to exhibit normal responsivity to food depri
ties: ( l ) that the brain merely senses circulating nutri
vation. These paradoxes led to a simple modification
ents or correlated substances in the blood and adjusts
of the notion of a "satiety center": The VMH does not
feeding accordingly, and (2) that the brain itself sus elaborate a shprt-term satiety signal but rather a longer
tains an ongoing energy-dependent integrative process term signal of body-energy integration.45 Accordingly,
that parallels bodily processes and adjusts feeding in
the prediction would be that direct administration of
response to its own local energy transaction mechanisms glucose into this brain area would reduce daily food
or highly correlated processes. It presently seems likely
intake, but not necessarily the size of the meal that
that both types of mechanisms are operative, and it followed. In fact, this is the ca<;e,46 and many of the para
seems clear that the key to overall bodyMenergy balance doxes in our knowledge of brain feeding control sys
resides in some type of longer-term regulatory process
tems were resolved by this shift of theoretical per
that operates throughout the day rather than among the spective. Of course, such facts concerning regulatory
short-tenn signals that arise from individual meals. Two signals form only a small, albeit central, part ofthe feed
intriguing findings highlight the need for a clear dis
ing story.
tinction between short-term feeding control and long
Considering the essential role of energy intake in
term energy-regulatory factors.
sustaining survival and reproductive fitness, it is not
First, many years ago investigators joined two rats surprising that feedingcontrol systems are located in
together in parabiotic union ("Siamese twins," who
several areas in the brain, from frontal cortical and tem
shared each other's blood circulation via a surgically poral areas that register the value of specific foods to
produced skin-flap connection).44 Each of these normal . brain stern levels that govern chewing, swallowing,
animals gradually ate less, and eventually each con and simple gustatory acceptance.47 However, the most
tained only half the body fat that a normal rat contains.
important findings in the field have been made at the
This peculiar result suggests that each animal's brain
hypothalamic level (Figure 9.7). Damage to theLH was
was perceiving theirjoined metabolic dynamic as if two found to produce severe feeding deficits, and for a while
bodies constituted a single fat mass (Figure 9.6). This that area of the brain was thought to contain a "feeding
ENERGY I S DELIGHT
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VMH
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for
H UNGER
Necessary for
Inhibition of Feeding
BRAKE
177
178
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ENERGY I S DELIGHT
additi onal ways to control body weight. A variety of
endogenous molecules, most of them neuropeptides,
have now been found that can dramatically reduce appe
tite and body weight in normal animals. Among the
most exciting recently discovered ones are items such
as GLP- 1 , fibroblast growth factor, and urocortin.61 Of
course, as already discussed, it will be critical to deter
mine which of these is actually producing a normal type
of satiety as opposed to illness or some other emotional
effect. Good control experiments of the type described
earlier remain to be done, and they will be needed to
resolve such issues.
It should also be remembered that most of these mol
ecules, which are fairly large peptides, do not cross the
blood-brain barrier readily. Chemists would have to de
velop new variants of regulatory molecules that could
get into the right areas of the brain before we could ever
use them as magic bullets to curb appetite. Also, in the
regulation of bodily functions such as energy balance,
everything is multiply determined. Thus, it may be es
sential to use several strategies concurrently, including
ones that take advantage of metabolic mechanisms to
help balance the body's energy equation. Recent work
with mutant mice, where one enzyme that is important
for fat metabolism has been changed, leads to chronic
leanness, even when animals are challenged with high
fat diets. 62 Clearly, better ways to control metabolic
information transactions may be essential for long-term
control of appetite and body-weight problems.
179
180
ENERGY IS DELIGHT
3o r---==;=====------------
---o.....0...
25
ts --
----
Control
EOS 50 pg/DAY
20
15
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10
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181
ENERGY IS DELIGHT
183
GLUCOSE CROSSOVER
w
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UNTREATED
f- -;- 1
PERCENT PREFERENCE
DAYS
DAYS
Figure 9.1 0. Summary of the patterns of sugar water consumption in animals given
continuous daily access to two solutions of different concentrations. Animals initially take
most of their sugar from the concentrated solution but gradually shift over to the less sweet
dilute source. The right-hand graph summarizes the glucose crossover patterns of various
animals having different regulatory problems. (Adapted from Panksepp & Meeker, 1977;
see n. 8 1 .)
ENERGY IS DELIGHT
1 85
COUNTERCONOJTIONlNG
WITH MORPHINE
20
[
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MORPHINE
PAIRED SO Ll'UI<JN !a
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Figure 9.1 1 . Changes in saccharine solution intake in animals in which one solution
odorized with lemon or vanilla was paired with 1 mg/kg of morphine, while the other
was paired with 1 mg/kg of the opiate antagonist naloxone. Clearly, animals preferred
the morphine-paired solution under a variety of testing conditions, and these prefer
ences could be extinguished and counterconditioned readily. (According to unpublished
data, Panksepp & Jalowiee, 1982.)
186
10
Suggested Readings
Bolles, R. C. ( 1 975). The01y ofmotivation(2d ed.). New
York: Harper and Row.
Booth, D. A. (ed.) ( 1 978).Hunger models: Computable
theoty of feeding control. London: Academic
Press.
Brownell, K. D., & Foreyt, J. P. (eds.) ( 1 986). Physiol
ogy, psychology, and treatment of the eating disM
orders. New York: Basic Books.
Katsuki, Y . , Sato, M., Taklagi, S. F., & Oornura, Y.
(eds.) ( 1977). Food intake and chemical senses.
Tokyo: Univ. of Tokyo Press.
Kleiber, M. ( 1975). Thefire ofl(fe. New York: Krieger.
LeMagnen, J. ( !992). Neurobiology offeeding and
nutrition. San Diego: Academic Press.
Navin, D., Wyrwicka, W., & Bray, G. A. (eds.) ( 1 976).
Hunger: Basic mechanisms and clinical implica
tions. New York: Raven Press.
Panksepp, J. ( 1974). Hypothalamic regulation of energy
balance and feeding behavior. Fed. Proc. 33: 1 1 501 1 65.
Stunkard, A. J., & Stellar, E. (eds.) ( 1 984). Eating and
its disorders. New York: Raven Press.
Young, P. T. ( 19 6 l ). Motivation and emotion. New
York: Wiley.
CENTRAL THEME
Although aggression has multiple causes, in psychiat
ric practice the most problematic forms arise from
q.nger. Many stimuli can provoke anger, but the most
common are the irritations and frustrations that arise
from events that restrict freedom of action or access
to resources. Although psychologists have documented
numerous environmental precipitants of anger and agM
gression, they have yet to clarify the difficult q uestion:
What is anger? One reason this topic has been avoided
is that anger is a primitive state of the nervous system
that cannot be explained by mere words or environ
mental events. It must be clarified through a study of
the underlying neuroevolutionary processes. As most
observers have agreed throughout history, the emo
tion of anger is a human birthright, arising from our
ancestral heritage. During this century, we have finally
come to understand, at least in part, the nature of brain
circuits that generate these powerful and often dan
gerous feelings, which yield behaviors that moral phi
losophers of the previous century said "deserved rep
rehension" and which emerge from our potential for
"evil." Modern evidence suggests that anger emerges
from the neurodynamlcs of subcortical circuits we Share
homo!ogously with other mammals. The general loca
tions of these circuits have been identified by localized
electrical stimulation of the brain. The RAGE circuits
1 87
188
On Aggression
At times animals threaten, bite, and kill each other.1
Such behavior is known as aggression. Its manifesta
tions range from a threatening baring of teeth to the
tearing of flesh, from the graceful dive of a hunting
hawk to the spitting spectacle of a cornered cat, from
the display of pompous sexual plumage to the catastro
phes of welloiled guns and hidden bombs. Aggression
is neither a universal nor a unidilnensional phenom
enon. Many invertebrates, like mollusks, exhibit no
apparent aggression during their life cycles. However,
nearly all vertebrates exhibit aggression from time to
time, and such behavior can have several distinct envi
ronmental and brain causes.
Three distinct aggressive circuits have been provi
sionally identified in the mammalian brain: predatory,
intermale, and affective attack or RAGE circuits. Only
the last one provokes enraged behaviors, and presum
ably the experience of anger. For instance, males that
fight each other for access to sexual resources do not
appear to be enraged but instead present themselves as
potential champions on the field of competition. Of
course, they may eventually become angry at each other
as they lock horns. Likewise, predators kill other ani
mals not out of anger but because they need food to live.
We must assume that the hunt and the kill is as positive
a psychological experience for the predator as it is a
fearful one for the prey. Predatory attack is a distinct
type of aggression that arises from different circuits than
anger or the seasonal competition for dominance among
males of"toumament species." However, as we will see,
it is not fully distinct from the SEEKING circuits dis
cussed in Chapter 8.
Are there other aggression circuits? Perhaps, but we
do not have sufficient evidence to discuss them as dis
tinct entities. For instance, killing and injury of the
young (infanticide and child abuse) are common behav
iors in nature and human societies, but these tendencies
may emerge from some combination of the three brain
systems already mentioned, as well as others. Also, does
189
190
191
192
Figure 1 0.1 . Schematic suggestion of likely interactions between neural systems that
mediate the anticipatory behaviors of SEEKING and arousal of the RAGE system.
(Adapted from Panksepp, 1 98 1 ; see chap. 3, n. 25.)
193
194
195
AMYGDALA
RAGE C I RC U ITS
Figure 10.3. Summary of the localization of RAGE circuitry in the brain. (Adapted from
data in Siegel & Brutus, 1990; see n. 39; and Siegel & Schubert, 1995; see n. 8 1 .)
196
c?
/ :
101
NSE N
ON HIGHER BRAIN AREAS
H YPOTHALAMUS
AMYGDALA
RESPONSE DEPENDENT ON
PAG BUT NOT THE AMYGDALA
RESPONSE DEPENDENT ON
THE PAG AND HYPOTHALAMUS
Figure 1 0. 4 . Hierarchical control of RAGE in the brain. Lesions of higher areas do not
diminish responses from lower areas, while damage of lower areas compromises the
functions of higher ones.
1 97
REWARD
EVALUATION
198
Quiet-Biting Attack
As already indicated, the major brain areas that yield
predatory aggression during ESB overlap remarkably
with brain areas where self-stimulation is obtained, al
though quiet-biting attack has typically been studied in
cats, while rats have been the species of choice for self
stimulation studies. If both self-stimulation and preda
tory attack actually emerge from a homologous basic
brain function, it is understandable why cats are so
rarely used in self-stimulation research. Cats do not
acquire self-stimulation behavior as readily as rats, and
when they do, they do not behave in a rapid, agitated
way like rats. Presumably, this is because a eat's typi
cal food-aquisition strategy is stealthy hunting that re
quires considerable motor inhibition. Rats, on the other
hand, acquire the behavior rapidly and behave energeti
cally, probably because their natural foraging style,
which is accompanied by vigorous activity and object
manipulation, fits nicely with vigorous lever pressing.
Conversely, it is much easier to obtain quiet-biting
attack from cats than from rats, probably because rats
normally harvest energy by searching and scavenging
for their food rather than hunting. In one of the first
199
200
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Mixed Effects:
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SOCIAL
INTERACTION
EXPLORATION
OFFENSE
Post-Synaptic Effects:
Decreased Aggression
(Supersensitivity in DHT
Animals at the Low Dose)
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1111 CONTROL
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204
205
Suggested Readings
Averill, J. R., ( 1982). Anger and aggression: An essay
on emotion. New York: Springer-Verlag.
Dollard. J., Miller, N. E., Doob, L. W., Mowrer, 0. H.,
& Sears, R. R. (1939). frustration and aggression.
New Haven, Conn.: Yale Univ. Press.
Johnson, R. N. ( 1 972).Aggression in man and animals.
Philadelphia: Saunders.
Miczek, K. A. (ed.) ( 1 98 1 ). The psychopharmacology
of aggression and social behavior. Special issue
of Pharmacology Biochemistry and Behavior 1 4
(suppl. l ) . Fayettesville, N.Y.: ANKHO Interna
tional.
Moyer, K. E. ( 1976). The psychobiology ofaggression.
New York: Harper and Row.
Olivier, B., Mos, J., & Brain, P. F. (eds.) ( 1 987).
Ethopharmacology ofagonistic behaviour in ani
mals and humans. Dordrecht: Martinus Nijhoff.
Scott, J. P. ( 1 958). Aggression, Chicago: Univ. of Chi
cago Press.
Svare, B. B. (ed.) ( 1 983). Hormones and aggressive
behavior. New York: Plenum Press.
Valzelli, L. (1981). Psychobiology of aggression and
violence. New York: Raven Press.
Valzelli, L., & Morgese, I. (eds.) (1981). Aggression
and violence: A psychobiological and clinical
approach. Milan: Edizioni Centro Culturale E.
Congressi Saint Vincent.
11
CENTRAL THEME
. :
206
207
208
UNCONDITIONAL RESPONSES
PAIN. NOISE, ETC
PREDATORS
OPEN SPACES
SUDDEN MOVEMENTS
CONDITIONAL INPUTS
ALL EXTERNAL SENSES
Figure 1 1 . 1 . Schematic summary of the trajectory of the FEAR system and the various
symptoms induced by stimulation of the system. (Adapted from Panksepp, 1 990; see n. 2.)
209
Learned
With Punishment
No Punishment
Freezing to shock
Open-field exploration
Defensive burying
Stimulation
Social-interaction tests
f fear circuits
Plus-maze test
Predatory odors
210
211
212
213
214
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215
216
HIGH
FEAR
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Figure 1 1 .4. Lesions of subcortical but not cortical auditory processing areas disrupt
conditioning of fear response to acoustic stimuli paired with foot shock. (Results adapted
from Le Doux, 1993; see n. 53.) Behavioral data on top, and locations of lesions on
bottom. The damage to the auditory cortex was on the lateral surface of the brain, depicted
by dotted lines.
217
218
219
220
'
'
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221
222
,. . .
Suggested Readings
Burrows, G. D., Roth, M., & Noyes, R., Jr. (eds.)
( 1 990). Handbook of anxiety. Vol. 3, The newo
biology ofanxiety. Amsterdam: Elsevier.
PART m
224
the learning of social skills, which can facilitate reproductive success. It is one of
the major systems in the brain that can generate happiness and joy.
Finally, in Chapter 16, I will consider a variety of critical issues concerning higher
brain mechanisms in emotionality, including such fundamental aspects of brain
organization as the nature of "the self," which must be addressed by neuroscience
if we are ever to understand how emotional feelings are actually generated by
the brain. I will attempt to clarify some of the most difficult and important issues
in neuroscience, but unfortunately they are ones that have barely been touched
empirically. To scientifically consider such topics, we must work concurrently at
high theoretical and basic empirical levels. Many have suggested that there is prob
ably no coherent neural representation of "the self" within the brain, but here I
will advocate the position that there is such a neural entity, and that it elaborates
a basic motor representation of the organism as an active creature in the world.
This neural representation may be essential for an animal to have affective feel
ings. To help us talk about such a complex function of the brain, I will refer to its
primordial neural substrates, deep in the brain stem, as the SELF (Simple Ego-type
Life Form). I will develop the idea that this mechanism is multiply rerepresented
in the brain during development and that it provides the center of gravity for the
emergence of affective consciousness in brain evolution. Although adult human
emotional experience also relies on higher brain representations of emotional sys
tems, the position advocated here is that those higher functions could not subsist
without the integrity of the lower functions.
'
CENTRAL THEME
Male and female sexuality are subservient to distinct
brain controls, although they also share many influ
ences. The primordial plan for both female and male
fetuses, in mammals but not in birds, is initially femi
nine. Some have called this the "default" plan, since
masculinization results from the organizational effects
of fetal testosterone, which, in humans, occur during
the second trimester of pregnancy. Others would call
it the "without fault" plan, since the female brain co
ordinates the use of both cerebral hemispheres more
effectively than does the male brain. Contrary to some
creation myths, in mammals maleness arises from
femaleness, rather than the other way around. If all
biochemical events go according to the masculiniza
tion plan during this phase of gender specialization, the
initially feminine brain is masculinized in utero by the
timed secretion of testosterone and its conversion to
the active organizational hormone, estrogen. The de
veloping female brain is protected by prophylactic mol
ecules, such as alpha-fetoprotein, which neutralize the
effects of maternal estrogens that would otherwise
tend to masculinize the brain. To be masculinized means
that certain areas of the brain, especially specific nuclear
groups in the anterior hypothalamus, grow larger in
males than in females, while other areas remain smaller,
225
226
'''''
Sexual Feelings
,/
227
228
T H E SOCIAL EMOTIONS
229
230
::
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Evolutionary Sources .
of Mammalian Sexuality
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231
232
aromatase
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233
Brain Masculinizatio
:>
Body Masculinizatio
Figure 1 2. 3 . Both the brain and body of mammals are initially organized according to a
female characteristic plan. Maleness emerges from two distinct influences of testosterone
on body tissues-masculinization of the brain being mediated by estrogen (E) and of the
body by dihydrotestosterone (DHT). Different tissues can convert testosterone to different
products because of the enzymes they contain. DHT is manufactured in cells containing
S-a-reductase, and E is manufactured in those that contain aromatase.
234
235
Hypothalamus
Median Eminence
Gonadotropin Releasing
Factor
Posterior
Pituitary
Feedback to Brain
Feedback to Brain
Testes
Testosterone
Sperm Production
Estrogen Secretion
Ovulation
236
:;..
SENSORY
INPUTS
Figure 1 2.5. Lateral view of the rat brain summarizing two major areas that provide
differential control over male and female sexual behaviors. Males contain a larger
POA, and this area is essential for male sexual competence. The VMH is clearly more
influential in female sexual responsivity. These systems operate, in part, by sensitizing
various sensory input channels that promote copulatory reflexes. The extent to which
these circuits control the affective components of sexual behavior remains uncertain.
Stress-Induced Suppression
of Brain Masculinization
Although nature is strongly disposed toward creating
relatively clear-cut male brains within male bodies and
female brains within female bodies, we have now seen
that it can easily produce other permutations. These
237
238
logical changes that work against the normal masculin opiates during the second trimester would be expected
to have a higher incidence of homosexuality than the
ization of the male brain.
The fetal spurt of testosterone that normally mas offspring of nonaddicted women.
Does maternal stress also affect the development of
culinizes male rats occurs several days prior to birth
(around 19 days of fetal age).53 Under conditions of the female offspring? The answer was thought to be no,
but some behavioral differences in females have now
maternal stress, the critical cascade of events is dis
rupted so that the peak of testosterone secretion occurs been detected. The most noteworthy, in the present
context, is that female offspring of stressed mothers
several days earlier than it should, when brain tissues
exhibit weaker maternal tendencies than those from
are not yet ready to receive the organizing message. It
is as if the organizational camera shutter had been nonstressed mothers-just the converse of the pattern
clicked without the lens cap being removed: Although seen in males, who tend to become more nurturant.57
Such changes in nurturance have been evaluated using
enough testosterone is secreted, it simply comes too
a "sensitization" or "concaveation" procedure, whereby
early, and the neural image of maleness is not ade
virgin animals (either male or female) are given free
quately imprinted upon the brain. In addition, maternal
access to rat pups. Across several days of exposure,
stress impairs enzymes that help synthesize testoster
one in the gonads. Delta5-3G-hydroxysteroid dehydro these initially nonmaternal animals begin to exhibit such
behaviors as retrieving pups and huddling over them
genase is inhibited, especially around days 1 8 and 19
(see also Chapter 13). The females from stressed moth
of gestation, when the enzyme is normally available in
highest levels. Likewise, brain aromatase, which allows ers take longer to exhibit this type of sensitization, while
testosterone to be converted to estrogen, is "inhibited at the males begin to exhibit nurturant behaviors more
the same time. These factors combine in such a manner rapidly than controls.58
Another urgent question is whether human babies
that the brains of the affected males remain more fe
exhibit similar brain changes when their mothers are
malelike. For instance, the SDN-POA becomes femi
nized because of the normal female-typical progression confronted by stress. Although several positive findings
of cell loss in that area, since the effect of estrogen in are available, they are generally deemed controversial.
For instance, it has been documented that one highly
promoting nerve growth is absent.54
stressful historical period, namely, the years of declin
Recent work has clarified whether it is-the psycho
ing fortunes for Germany during World War II, led to
logical consequences of maternal stress that cause de
a higher incidence of homosexual individuals, as mea
masculinization or whether stress-related physiological
changes suffice: The effect seems to be a direct result sured by their sexual preferences in later years. In other
words, boys born during the peak years of wartime
of the mother's bodily stress response. Of the several
prominent stress hormones, excess opioid (perhaps stress were reported to have a higher incidence of homo
sexuality than those born during the years of peace
B-endorphin) secretion appears to mediate the demas
culinizing effect of stress. Pituitary B-endorphin release before and after the war.59 Also, there has been some
is pattly a counterregulatmy hormonal mechanism that work relating the levels of perceived stress during the
various trimesters of pregnancy to homosexuality in
helps prevent other excessive stress responses, such
male offspring. Elevated stress during the second tri
as those arising from adrenocorticotrophic hormone
mester has been reported by some investigators to be
(ACTH) secretion. The possible role of an opioid com
related to a higher incidence of homosexuality in the
ponent in stress-induced neurodevelopmental changes
0
has been evaluated simply by blocking opioid recep offspring.6
Of course, scientific caution is always advised in
tors during maternal stress with long-acting drugs such
as naltrexone; the result was a complete restoration of trying to extrapolate from animal data to the human
condition. As one scientist who has done much of this
masculinization. Stress-induced abnormalities in vari
ous biochemical parameters, such as reduced aromatase work points out, "The optimistic conclusion . . . that
this (i.e., stress) syndrome provides a direct explana
production, were also rectified. 55
tion of homosexuality in human males should be
Since opiate receptor blockade can mildly increase
the psychological perception of stress in humans, these greeted with some caution."61 At the same time, how
results suggest that the opioid component of the stress ever, to insist that such findings have no implications
response, as opposed to any psychological response to for human issues is to sustain an excessively cautious
the stressor, is the critical element in the cascade of stance about the underlying dynamics of the human
body and brain.
events that lead to the failure in fetal masculinization.
In sum, even though environmental effects clearly
This line of research also suggests that external admin
istration of opioids to pregnant mothers may demas modify one's self-perceptions, the sources of gender
identity, as genetic sex itself, are heavily rooted in bi
culinize males, and there is some evidence for this in
ology. Although it would be foolish to conclude that
animals. 56 One must wonder whether similar changes
would occur in the male offspring of women addicted sexual preferences are completely controlled by nature,
we can no longer discount innate biological influences.
to opiates during pregnancy. At present we do not know,
but the prediction is clear: Boys born to mothers using The reason such factors were not considered more fully
239
240
241
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Post
30 Mins
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Phase of Testing
Figure 1 2 .6. Effects of sexual arousal, ejaculation,
and postejaculatory interval on average plasma
oxytocin (OXY) and arginine-vasopressin (AVP)
levels in human males. (Adapted from Murphy et al.,
1987; see n. 87.)
242
243
244
, ...
T H E SOCIAL EMOTIONS
245
Suggested Readings
Allgeier, R. A., & Allgeier, E. R. ( 1 995). Human sexu
ctlity (4th ed.). Lexington, Mass.: Heath.
Becker, J. B., Breedlove, S . M., & Crews, D. (eds.)
( 1 992). Behavioral endocrinology. Cambridge,
Mass.: MIT Press.
Campbell, B. (ed.) ( 1 972). Sexual selection and the
descent of man. Chicago: Aldine.
Crews, D. (ed.) ( 1987). Psychobiology of reproductive
behavior. Englewood Cliffs, N.J.: Prentice HalL
Dorner, G. ( 1976). Hormones and brain differentiation.
Amsterdam: Elsevier.
Kincl, F. A. ( 1990). Hormone toxicity in the newborn.
Berlin: Springer-Verlag.
Le Vay, S. ( 1 993). The sexual brain. Cambridge, Mass.:
MIT Press.
Money, J. ( 1980). Love and love sickness: The science
of sex, gender difference, and pair-bonding. Bal
timore: Johns Hopkins Univ. Press.
Symonds, D. ( 1979). The evolution of human sexual
ity. New York: Oxford Uni. Press.
Ziegler, T. E., & Bercovitch, F. B. (eds.) ( ! 990).
Socioendocrinology ofprimate reproduction. New
York: Wiley-Liss.
inside you.
J. W. Anglund, "Love Is a Special Way of Feeling" ( 1 960)
CENTRAL THEME
:.1
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DAYS O F PREGNANCY
B I RT H
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Experience-Induced Solidification
of Maternal Behavior
It should be emphasized that well-established maternal
behavior no longer requires brain oxytocin arousal;
oxytocin blockade impairs maternal behavior only if
administered to mothers during the birth of their first
litter of pups. In animals that have been allowed to ex
hibit maternal behavior for several days, oxytocin an
tagonists have no outward effect on maternal compe
tence. In other words, they cannot block previous social
learning.
The ability of several days of normal maternal ex
perience to solidify maternal competence is also evident
253
254
B EH A V I O R A L
OUTP UT
Figure 1 3 .4. General overview of maternal behavior circuits in rodents. The central
integrator is in the dorsal preoptic area (POA) and the ventral bed nucleus of the stria
terminalis (VBN), which receives various sensory cues for maternal behavior and distrib
utes controls into widespread brain areas, including the medial hypothalamus (MH), the
ventral tegmental area (VTA), the periaqueductal gray (PAG), the habenula (HAB), and
the septal area (S). The precise functions of these various areas remain to be identified.
S I M I LA R I T I E S B ETW E E N
O P IATE ADDICTION
& SOCIAL D E P EN D E N C E
1 ) Drug Dependence
1 ) Social Bonding
2) Drug Tolerance
2) Estrangement
3)
3)
Drug Withdrawal
a) PSYCHIC PAIN
b) LACRIMATION
c) ANOREXIA
d) DESPONDENCY
e ) INSOMNIA
f) AGGRESSIVENESS
255
Separation
Distress
a) LONELINESS
b) CRYING
c) LOSS OF APPETITE
d) DEPRESSION
e) SLEEPLESSNESS
I) I R R IT A B ILITY
256
\(.
257
258
259
Thoughts on Altruism
AFTERTHOUGHT:
The " Mere-Exposure" Effect
260
Suggested Readings
Alexander, R. D. ( 1987). The biology ofmoral systems.
Hawthorne, N.Y.: Aldine de Gmyter.
Bowlby, J. ( 1 972). Attachment and loss. Vol. l , Attach
ment. New York: Basic Books.
Emde, R., & Harmon, R. (eds.) ( 1982). The develop
ment of attachment and affiliative systems. New
York: Plenum Press.
Fletcher, D. J. C., & Michener, C. D. (eds.) ( 1987). Kin
recognition in animals. London: Wiley.
Harlow, H. F. (1971). Learning to love. San Francisco:
Albion.
Klaus, M. H., & Kennell, J. H. ( 1 976). Maternal-infant
bonding. St. Louis, Mo.: Mosby.
Koobi!, E., & Neill, J. D. (eds.) ( 1 988). The physiol
ogy of reproduction. New York: Raven Press.
Krasnegor, N. A., & Bridges, R. S. (eds.) (1990). Mam
malian parenting: Biochemical, neurobiological,
and behavioral determinants. New York: Oxford
Univ. Press.
Pedersen, C. A., Caldwell, J. D., Jirikowski, G. F., &
Insel, T. R. (eds.) ( 1 992). Oxytocin in maternal,
sexual and behaviors. Special issue of Annals of
New York Academy of Sciences, Vol. 652. New
York: New York Academy of Sciences.
Winberg, J., & Kjellmer, I. (eds.) (1994). The neurobi
ology of injCmt-parent interaction in the newborn
period. Acta Paediatrica, Vol. 83, Suppl. 397.
Oslo: Scandinavian Univ. Press.
14
CENTRAL THEME
One of the great mysteries of psychology is the nature
of the "something" that Walt Whitman extols in his
masterpiece "I Sing the Body Electric." That subtle feel
ing of social presence is almost undetectable, until it is
gone. We simply feel normal and comfortable when we
are in the midst of friendly company, and that same fee!M
ing becomes warmer when we are among those we love
deeply, especially when we have not seen them for some
time. We often take these feelings, like air itself, for
granted. But we should not, for when this feeling of nor
malcy is suddenly disrupted by the undesired loss of a
lover or the unexpected death of a loved one, we find
ourselves plunged into one of the deepest and most
troubling emotional pains of which we, as social crea
tures, are capable. In everyday language, this feeling is
called sorrow or grief, and it can verge on panic in its
most intense and precipitous forms. At a less acute but
more persistent level, the same essential feeling is called
loneliness or sadness. This psychic pain informs us of
the importance of those we have lost. In psychologi
cal terms, "importance" is not easy to define, but in evo
lutionary terms it is. We grieve most when we lose those
in whom we have invested a great deal of genetic ef
fort (our children) or those who have helped us to thrive
(our parents, friends, and relatives)-in short, when we
lose those with whom we have social bonds. Obviously,
the loss of a parent is most acute when one is young
and still dependent; the pain is less intense and pro
tracted when a grown child loses an elderly parent. On
261
262
DEPRESSION
SEPARATION DISTRESS
RESPONSES
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PLACE
ATTACHMEN T
MECHANISMS
THERMOREGULATION
PAIN
CONTROLS
Figure 1 4 . 1 . Schematic
summary of the various
influences and levels of
analysis that are important in
analyzing the potential nature
of an integrative emotional
system for social affect.
(Adapted trom Panksepp
et al., 1997; see n. 3.)
264
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Figure 1 4.3. Distress vocalizations of young guinea pigs as a function of age, tested
either alone or with mother in familiar and unfamiliar environments. (Adapted from
Pettijohn, 1979; see n. 14.)
STIMULATION-INDUCED
DISTRESS VOCALIZATIONS
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calls of 5-6-day-old chicks socially isolated from their flock for a two-hour period.
(Adapted from Panksepp, 1996; see n. 30.)
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Figure 1 4.8. Mean number of vocalizations in 4-5-day-old chicks during successive three
minute testing blocks either in ambient silence or during exposure to music. Half of the
animals were administered 0.25 !lg of kainic acid (KA) into their ventricular systems just
before testing. Not only did the KA markedly increase vocalizations, but the "comforting"
effects of music were totally eliminated. The same pattern of results is obtained if one uses
mirrored environments to reduce the vocalization. (Adapted from Normansell; 1988; see n. 30.)
271
272
OXYTOC I N
D I S T R I B UTI O N S
R E C E PT O R
1 0 DAY O L D RATS
273
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274
275
276
277
278
arms and legs, and, indeed, all over the body . 1 ; 6 To the
best of our knowledge, this response reflects a mixture
of vasoconstriction, local skin contractions caused by
piloerection, and perhaps changes in evaporative cool
ing at the skin surface. Such effects can be objectively
measured as a galvanic skin response (GSR), which is
a general yardstick of skin resistance. Of course, there
is great variability i n the incidence of this response.
Some people rarely recognize such feelings in their
lives, while others, probably the more social ones, de
light in them frequently. For many years, I have sought
to understand this intriguing phenomenon. Here I will
summarize the insights I've obtained, as described in
detail elsewhere.1 17
I will refer to this shivery-tingly experience by the
term chills, although many, especially males, tend to use
the term thrills. [ prefer the label chills because females
use it predominantly, and it is clear that females, as a
population, exhibit this response more frequently than
males. There are many exceptions, of course. I, for one,
am so sensitized that I can have the experience on a
regular basis just thinking about events. Females typi
cally recognize that sad music is more likely to produce
this chill phenomenon than happy pieces, while males
more commonly suggest that happy music is the cause.
However, when one actually conducts an experimental
analysis, it is clear that sad music does in fact produce
more chills than does happy music, even in males.
Conversely, those pieces of music that produce more
chills are typically rated as sad rather than happy by
listeners. People tend to have many more chills to pieces
they themselves have selected, which may reflect the
rich networks of associations people have to music they
have enjoyed often. What is the underlying meaning of
this emotional phenomenon?
An intriguing possibility is that a major component
of the poignant feelings that accompany sad music are
sounds that may acoustically resemble separation
DVs-the primal cry of being lost or in despair. In other
words, a high-pitched, sustained crescendo capable of
piercing the "soul" seems to be an ideal stimulus for
evoking chills. A single instrument, like a cello or trum
pet, emerging from a soft orchestral background is
equally provocative. Thus, the chills we experience
during music may represent the natural tendency of our
brain emotional systems, especially those that are tuned
to the perception of social loss, to react with an appro
priate homeostatic thermal response. When we are lost,
we feel cold-not only physically but also as a neuro
symbolic response to social separation. As mentioned
earlier, the roots of the social motivational system may
be strongly linked to thermoregulatory systems of the
brain (Figure 14.1). Thus, when we hear the sound of
someone who is lost, especially if it is our child, we
also feel cold. This may be nature's way of promoting
reunion. In other words, the experience of separation
establishes an internal feeling of thermoregulatory dis
comfort that can be alleviated by the warmth of reunion.
Suggested Readings
Bowlby, J. ( 1973).Attachment and loss. Vol. 2, Separa
tion: Anxiety and anger. New York: Basic Books.
279
ROUGH-AND-TUMBLE PLAY
15
CENTRAL THEME
When children are asked what they like to do more than
anything else, the most common answer is "to play ! "
I t brings them great joy. And roughhousing play is the
most fun of all, even though most investigators recog
nize other types such as "object play" and "fantasy
play." Although thousands of papers have been writ
ten on the topic, play is still considered a frivolous area
of inquiry among most neuroscientists. Only recently
have some become interested in the underlying brain
issues. Now increasing numbers of investigators are
beginning to realize that an understanding of play may
reveal some major secrets of the brain and yield impor
tant insights into certain childhood psychiatric problems
such as autism and attention deficit disorders (or
hyperkinesis, as it used to be known). It is now certain
that the brain does contain distinct neural systems de
voted to the generation of roughhousing or rough-and
tumble (RAT) play. Indeed, one of the best species for
systematic study of this behavior is the laboratory rat,
and practically all the work summarized here is based
on such play in rats. Although our knowledge about the
underlying PLAY systems remains rudimentary, RAT
play appears to be intimately linked to somatosensory
information processing within the midbrain, thalamus,
and cortex. Certain synaptic chemistries are especially
effective in arousing play (e.g., acetylcholine, glutamate,
and opioids), while others reduce playful impulses (e.g.,
serotoni n , norepinephrine, and GABA), but neuro
pharmacological studies tel! us little about the adaptive
280
281
282
ROUGH-AND-TUMBLE PLAY
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AGE OF TESTING
Figure 1 5 . 1 . Ontogeny o f play i n socially isolated and socially housed laboratory rats.
(Adapted from Panksepp, 198 1 ; see n. 18). The pinning measure is depicted in Figure 15.2.
283
ROUGH-AND-TUMBLE PLAY
A Description of
Rough-and-Tumble Play
It is difficult to capture the dynamic image of real-life
play in words. But the overall impression given by prac
tically all mammals is a flurry of dynamic, carefree ram
bunctiousness. In rats, one sees rapid spurts of activity,
toward and away from a play partner. Sometimes one
animal "bowls" the other animal over, which leads to a
flurry of playful chasing. In turns, the animals pursue
each other, with rapid pivoting and role reversals. Ani
mals often pounce on each other's backs as if they are
soliciting vigorous interaction; these "dorsal contacts"
can be easily quantified and have been commonly used
as an explicit measure of play solicitations (Figure 15.2).
Sometimes the dorsal contacts do not yield reciprocation,
instead ending up as prolonged bouts of dorsal groom
in g. At other times, the recipient of play solicitations
responds by either running away or twisting laterally; an
apparent bout of Wrestling ensues, in which one animal
winds up on its back with the other animal on top. This
"pinning" posture can also be easily quantified (Figure
15.2) and is the clearest measure of the consummatory
aspects of play. If animals are allowed to play on an ac
tivity platfonn, one can also obtain an overall measure
of RAT activity. There are surely many other ways to
monitor play, and each of these measures can be sub
categorized. For instance, most pins are of short dura
tion, occurring in the midst of ongoing "wrestling"
matches, while others are more prolonged, often signal-
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AGE (Days)
Figure 1 5.3. Pinning on successive days, with one animal getting naloxone (1 mgfkg) and
the other getting morphine at the same dose. After seven days, drug conditions were
reversed. (Adapted from Panksepp et al., 1985; see n. 22.)
T
.
286
ROUGH-AND-TUMBLE PLAY
287
288
ROUGH-AND-TUMBLE PLAY
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Figure 1 5.4. Mean (SEM) levels of chirping in 44 and 89Mdayold rats as a function of
social history and the area of the body tickled. The animals had been weaned and individu
ally housed at 24 days of age, and half the animals (socials) had received two 0.5-hour
play sessions each day through puberty (50 days of age), while the others (isolates) had no
opportunities for social interaction. Testing occmTed in both groups following 48 hours
without social interaction. Pinning and dorsal contacts during a 2minute play session on
an adjacent day are also provided. (Unpublished data, Panksepp & Burgdorf, 1 997 .)
289
290
ROUGH-AND-TUMBLE PLAY
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39
AGE (Days)
Figure 1 5.5. Play as a function of age in animals treated at the nape of the neck with
xylocaine after 25, 3 1 , and 37 days of life. The reduction of play exhibited no clear
tolerance, suggesting that without appropriate somatosensory input, the consummatory
aspects of play are seriously compromised. (Adapted from Siviy & Panksepp, 1987; see
n. 40.)
291
292
ROUGH-AND-TUMBLE PLAY
30
293
FOS Expression
During PLAY
25
43
37
33
49
5i
DAYS OF AGE
PARAFASCICULA
REA
294
ROUGH-AND-TUMBLE PLAY
295
ATTRIBUTIONS
PERCEPTIONS
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GENERAL
AROUSAL
296
ROUGH-AND-TUMBLE PLAY
297
298
ROUGH-AND-TUMBLE PLAY
Suggested Readings
Aldis, 0. ( 1975). Play fighting. New York: Academic
Press.
Fagen, R. ( 1 9 8 1 ) . Animal play behavior. New York:
Oxford Univ. Press.
Groos, K. ( 1 898). The play of animals. New York:
Appleton.
299
16
CENTRAL THEME
300
301
302
A Prospectus
303
304
305
306
307
The most discrete disruptions of perceptual aware tion.22 Still, because of such examples, we should obvi
ness occur as a result of various forms of cortical dam ously remain cautious in trying to understand conscious
age. One of the most striking is the loss of consciously awareness in animals by simply interpreting their out
appreciated vision following damage to the occipital ward behaviors. Special behavioral assays need to be
cortex. Although individuals with these impairments conducted before such conclusions are warranted. When
report being completely blind, they can accurately iden we do use procedures such as conditioned place pref
tify the locations of moving objects in their visual fields. erence and avoidance, a mass of data from animals as
This "blindsight" has perplexed students of conscious well as humans suggests that the fundamental sources
ness, for it highlights how wrong our conscious under for affective and intentional consciousness are subcor
standing of our behavioral abilities can be. It seems tical, but they are also represented in higher regions.
likely that blindsight is mediated by our ancient frog
. type visual abilities, seated in the superior colliculi of
the midbrain. That ancient visual system allows all ani Split-Brain Data and the Subcortical
mals to identify where objects are in visual space with Sources of Consciousness
out being able to decode what they are. Our higher lev
els of conscious awareness are no longer well tuned to A subcortical location for the essential mechanisms of
movement information in the absence of object infor consciousness can be derived from the many fascinat
mation. Such blindsight leaves only a vague feeling of ing studies of "split-brain" individuals in whom the
corpus callosum has been severed, eliminating the main
something having happened.20
Comparable types of effects have been found with communication channels between the two cerebral
the loss of face-recognition abilities, orprosapagnosia, hemispheres. Although such data are more commonly
following damage to the bottom surface of the tempo used to argue that human conscious awareness is corti
ral lobes and the neglect of personal space following cally elaborated, the continued unity of primary-process
damage to the parietal lobe, especially when these forms consciousness and a primal form of behavioral inten
of damage are situated in the right hemisphere. Such tionality following the splitting of the human brain are
agnosias clearly tell us how important specific types of also striking.
Although each hemisphere can have independent
cortical information are for constructing a detailed
awareness of our world. Not only are aft1icted individu realms of perceptual awareness, cogitate independently,
als still able to identify others by their tone of voice and and have distinct emotional communication styles, care
by the clothes they wear, they can still process incom ful behavioral observation of split-brain individuals
ing facial information at a preconscious level. For yields an additional overriding conclusion: Despite
instance, people with prosapagnosia still selectively ex massive hemispheric disconnection, the deep and essen
hibit galvanic skin responses to familiar faces, indi tial coherence of each person' s personality and his or
cating that their autonomic nervous systems remain in her sense of unity appears to remain intact. Most forms
touch with the facial features of the people they have of intentionality and deep emotional feelings are not
known.21 We do not know whether this type of auto split in any obvious way by a parting of the hemi
nomic information is simply unable to be represented spheres. Only the cognitive interpretations of specific
in consciousness, or whether it has come to be neglected events are affected. For instance, when one side of the
during development because of the power of the more brain is exposed to a sexually arousing visual stimulus,
salient types of visual information-namely, it became the other side feels the arousal but is not able to inter
a "preconscious" ability. I would assume that the latter pret the precipitating event correctly and often dis
is true, and that such alternative channels of information sembles and rationalizes.23 The unity of an underlying
can be made more salient within affective conscious form of consciousness in splitbrain individuals, per
ness through emotional education (i.e., by training haps their fundamental sense of self, is affirmed by the
fact that the disconnected hemispheres can no more
people to get in closer touch with their feelings).
Phenomena such as blindsight and prosapagnosia easily execute two cognitive tasks simultaneously than
highlight how powerfully preconscious perceptual pro can the brains of normal individuals.24 The inability to
cesses may control our behavior. Such findings have distribute attention simultaneously to two tasks is a
generally led to the widespread view that the contents of characteristic feature of a unified consciousness in neu
consciousness are mediated by very specific neocortical rologically intact individuals. In split-brain people, a
functions. As a consequence, it is now commonly be central workshop of consciousness,25 which simulta
lieved that most subcortical processes operate uncon neously influences both hemispheres, continues to limit
sciously. However, this is far from true. By comparison distribution of attentional resources.
Only with special procedures can we demonstrate
to cortical damage, very small lesions of subcortical
areas can severely compromise human consciousness, distinct types of cognitive and affective styles, as well
and electrical and chemical stimulation at many sub as perceptions and information-processing strengths
cortical sites can have effects on affective consciousness within each hemisphere.26 To put it simply, the left
that cannot be matched by any form of cortical stimula- hemisphere is generally more socially communicative
308
309
Conceptualizations of
SELF-Consciousness
311
312
CONVERGENCE OF SOMATIC
INFORMATION IN THE
SUPERIOR COLUCULUS
VISION
PANIC
FEAR
RAGE
SEX/NURTURANCE
SEEKING
CONVERGENCE OF EMOTIONAL
INFORMATION IN THE
PERIAOUEOUCTAL GRAY
313
314
315
, /
V
316
I
I
I
--_.-' - CINGULATE
/
-- - - '-..
-""
"--
SEEKING .
"
'\
"
"
EXPECTANCIES :; "
. . : : :..:: :
'
"\
'._ )
\
I
-...
_ _ _ _
_.... ,...,..
TEMPORAL LOBE
AMYGDALA
\
'
'- """I
'
\.
Figure 1 6.2. Overview of forebrain zones that are devoted to elaborating higher manifes
tations of basic emotional processes. Each of the emotional systems has higher spheres of
influence, with FEAR and RAGE concentrated in the lateral and medial temporal lobes,
SEEKING in the ventromedial frontal lobes, and various social emotional processes such
as separation distress or PANIC in the anterior cingulate. All of these systems converge on
the emotional and SELF representation zones of the midbrain. (Adapted from Panksepp,
1989; see n. 80.)
317
318
i
\J
319
320
321
322
to the extent that they do not. However, within these of them quite unseemly, can be played out, we have only
constraints, there are all too many options to consider, modest reason for optimism and solace. It is sad to note
including, as always, the dream of reason that creates that our sense of sympathy may be intrinsically weaker
than our sense of retribution.
monsters.94
There arc reasons to believe that cold reason, unfet
This may be the most in1portant overall message to
take away from our consideration of the many emotional tered by the impulses of social emotions, can yield per
systems that exist within our human brain. These ancient sonalities that are egotistic, selfish, and willing to hurt
neural systems, which constitute the foundations of our others for their own gratification (as long as the per
deeply telt personal values and standards of conduct, only ceived costs to themselves are not too high). There is
give us options to consider in our social worlds. The rela no intrinsic reason that such personalities could not
tive importance we give to various emotional factors in present themselves as highly extroverted and sensitive
each social equation will be determined as much by his while seeking to skillfully take advantage of others in
torical and ecological forces as by neurobiological ones. social and economic encounters. The existence of the
Environments where one must battle for resources will social emotions within the human brain provides no
promote different social solutions than environments shield against the existence and future evolution of
where circumstances are more generous and forgiving. cutthroat, self-serving individuals who have no desire
This, of course, makes the study of cross-cultural differ to advance cooperative altruistic behavioral tendencies
ences in emotionality a remarkably difficult area of in in human societies. It is troubling to contemplate that
quit)'. Even though the different branches of the human such individuals may be especially highly motivated to
family may have slightly different patterns of emotional aspire to positions of political and economic power. The
responsivity, for both genetic and cultural reasons, it is massive growth of the human neocortex now provides
now clear that we also share the same fundamental feel options such as these for the human spirit.
To grow fruitfully into the future, society must learn
ings. The same goes for the various genders.
What should scare us most is the 20th century rec how to recognize and benignly discourage and shun
ognition of the layers of deviousness that evolution may those who have no wish or ability to practice and pro
have bred within our intermediate cognitive systems mote stable and honest cooperative strategies. It remains
(those areas of the higher limbic brain that intrinsically possible that some individuals pursue such avenues of
interface between primitive emotional systems and life because of atypical responsivities of their basic
higher cognitive realms). Understanding human nature emotional systems, while others pursue asocial life ac
is surely not as simple as understanding the nature of tivities because of more personal choices. We may even
the subcortical emotional systems we share with other tually be able to detect such personality traits at an early
mammals, even if they are the ancient centers of gravity age, using sophisticated brain measurement procedures,
for our affective value systems. On top of these systems a troublesome possibility that is almost at our door
we also have strong intrinsic potentials for Machia step.98 It is hard to imagine how we might seek to mea
vellian deceit. The brain of "the lizard" still broadcasts sure and modify such emotional strengths and weak
its selfish messages widely throughout our brains. We nesses of individuals without infringing on basic human
have layers of human nature that sociobiologists and rights and liberties.
It is a blessing that a modest sense of fair play has
evolutionary psychologists are only beginning to deci
pher with the conceptual tools of inclusive fitness and already been built into the value structures of our human
brains. As game-theory analysis has affirmed, the most
game theories.
If we take their evolutionary stories to heart,95 we etiective trading strategy is fairness: to punish your trad
can begin to grasp the nature of the psychopathic and ing partners only if they have cheated, but then to for
sociopathic personalities that can sprout from the vari give rapidly. This "tit-for-tat" strategy is also ingrained
eties of human SELVES. At some point in human evo in our best social traditions such as "honesty is the best
lution, it was probably adaptive for a certain number policy.'' Unfortunately, this strategy appears to be most
of individuals in each human society to have warrior effective in small groups where everyone knows each
temperaments-individuals who were highly pugna other and where shame can still motivate behaviors. In
cious and relatively insensitive to the pain of others. If our anonymous megasocieties, the ancient stricture
such adaptations thrived during human evolution, these do unto others as you would have them do unto you
traits probably remain with us, all too well prepared by may be gradually losing force. Wherever long-term
our evolutionary heritage to wreak havoc and violence social relationships are not stable, our commitments to
in social life, even during times of peace.96 To some traditional social contracts appear to weaken.99 Since
extent such urges may be rechanneled into sports and we are now so remote from the original evolutionarily
other forms of competition, or perhaps even modified adaptive environments where our brains were con
by new social and pharmacological strategies.97 How structed, our best option may be to understand as hon
ever, if we see the cortex as a neuronal playground estly as possible the varieties of nature that can be nur
where multiple, evolutionarily adaptive strategies, some tured within human minds.
323
Suggested Readings
Ardrey, R. ( 1 974). Social contract. New York: DelL
Barash, D. P. ( 1 986). The hare and the tortoise. New
York: Penguin.
Dennett, D. C. (199 1 ). Consciousness explained. Bos
ton: Little, Brown.
De Waal, F. ( 1 982). Chimpanzee politics: Power and
sex among apes. London: Jonathan Cape.
Edelrnan, G. M . ( 1992). Bright t1ir, brilliant fire. New
York: Basic Books.
Lumsden, D. J., & Wilson, E. 0. ( 1 983). Promethean
jtre: Reflections on the origin ofmind. Cambridge,
Mass.: Harvard Univ. Press.
Morris, R. (1983). Evolution and human nature. New
York: Putnam.
Plato (! 940). The republic. (B. Jowett, trans.). New
York: Graystone.
Searle, J. ( l 984). Minds, brains, and science. Cam
bridge, Mass.: Harvard Univ. Press.
Walker, S. ( 1 983).Animal thought. London: Routledge
and Kegan Paul.
Wilson, P. J. ( 1 983). Man, the promising primate: The
conditions ofhuman evolution. New Haven: Yale
Univ. Press.
Appendix A
Bones, Brains, and Human Origins
325
326
APPENDIX A
APPENDIX A
327
328
APPENDIX A
APPENDIX A
329
330
APPENDIX A
Once thinking had become a major factor in the also make tools with tools. We not only build but also
acquisition, distribution, and competition for resources, build models of buildings. We not only communicate
we might anticipate that there would also emerge evo but also communicate about communication. We nor
lutionary aberrations and excesses in these newfound only think but also think about thinking. We also take
skills. As with any natural process, the underlying special interest in the contents of other minds.
The constraints of traditional scientific languages pose
mechanisms can go to extremes, and the price of cer
tain evolutionary adaptations may be mental aberrations enormous dilemmas for discussing and describing the
in a certain percentage of the population. For instance, intrinsic internal processes of the brain/mind. To pursue
the emergence of self-centered types of thought, where evolutionary epistemology to the fullest, we will need to
individuals persist in pursuing very limited and special rethink some of the constraints we have imposed on our
ized lines of cognitive activity (should we call it "aca scientific endeavors. We must try to study ancient brain
demic autism?"), beneficial up to a point, might also processes that we cannot define. For such brain functions,
cascade into the excesses of obsessive-compulsive and the definitions will be achieved at the end of our scien
full-blown autistic disorders. The former appear to arise tific journey rather than at the outset. We may need to
from excessive frontal lobe activity,21 while the latter use metaphors more liberally, and we have to take seri
are characterized by a disconnection of lower process ously the types of brain processes that all the folks around
(such as cerebellar and limbic emotional ones) from us speak of so readily--our hungers and thirsts, our an
gers and fears, our ability to feel sadness and joy. We
higher ones.22
Obviously, we humans are the most creative of all have to be able to conceptualize first-person issues, us
species, a trait that is a consequence of our cerebral ing third-person languages. Without some linguistic and
evolution. We do not have to look to our opposable conceptual flexibility, we cannot fathom the hidden
thumbs to recognize the abilities that now distinguish realms of feelings that humans have discussed for mil
us from the other animals. We not only make tools but lennia around the campfires of their lives.
Appendix B
The Brain, Language, and A ffective Neuroscience
331
332
APPENDIX B
APPENDIX B
ing vernacular usages, may provide new insights more the other emotional systems that are covered in this text.
readily than the accepted strictures on scientific prose We decided not to cave in, for that would have com
would lead us to believe. For this reason I decided to promised the future development of a scientifically
credible affective neuroscience.
employ capitalized vernacular terms in this text.
Skepticism is certainly a beneficial tool, to the ex
It is sometimes easier to observe and think about new
phenomena if we have first categorized them under an tent that it yields a dialectic of ideas that can progress
appropriate general conceptual label. When it comes to toward empirical resolution of difficult issues, but at
a study of integrative brain functions, especially those present it is too commonly an attitude, a well-cultivated
that were created by evolutionary processes, we must academic pretense, that leads to the neglect of impor
remain open to the existence of what at first seem to be tant problems. Indeed, during the middle part of the 20th
fuzzy linguistic entities and to sustain a cautious flexi century, behavioral scientists asserted that we should
bility in our lexical and linguistic tools. For instance, ignore internal processes completely-a bias that is still
old emotional concepts need to be entertained in the common in behavioral neuroscience.
In light of the many unresolved problems that still
field of behavioral neuroscience, not simply rejected out
of hand. By entertaining novel interweaving of old con exist, debate and disagreement are bound to continue
cepts with new neuroscientific findings, we may gradu to outweigh consensus within the psychobehavioral
ally be able to overlay primal psychological functions neurosciences. Although we all agree thatevolution has
onto brain functions in credible ways. A relaxation of created many intrinsic functions within the brain "com
the traditional lexical constraints (i.e., you can't talk puter," there is presently little agreement on how we
about it unless you can define all your terms) may be should describe, discuss, and study those functions. We
justified simply on the basis of evolutionary considera do know that internal neuropsychological functions can
tions concerning the nature and sources of certain brain only be inferred from some combination of external
signs, such as behavior and other bodily changes, along
functions.
For instance, we obviously can never understand the with basic psychological insights, but we still do not
deep nature of emotions without neuroscientific inquiry, agree on how we can proceed in a coherent scientific
and since we cannot study emotions without some type fashion. Hopefully we will eventually reach a consen
of linguistic guidance, we must learn to use emotional sus on how we might begin to talk about these matters.
terms in ways that will further our experimental pur One hope of this text has been to systematize this im
suits. This requires identifying coherent systems in the portant area of knowledge so that a more open dialogue
brain, labeling them with affective terms that will pro can be initiated between psychologists, neuroscientists,
mote discussion and study, establishing operational and all other disciplines interested in human nature. To
behavioral definitions for the basic emotional processes this end, I used some plain emotional language in ways
so the underlying neural processes can be effectively that have never been attempted before, at least in a ba
investigated, and providing linkages for levels of dis sic science text.
course above (psychological) and below (physiologi
cal and biochemical) the neurobehavioral level of analy
sis. Obviously, a cross-species neural analysis can only The Brain Organization of Human
hope to specify the necessary neural substrates of cer Language and Comparable Functions
tain human emotions without making any claims about in Animals
sufficiency.
Our failure to develop a more flexible attitude to One of the greatest success stories of neuropsychology
ward the study of the hidden evolutionary entities in the has been the identification of the brain areas that typi
brain is partly due to the obvious linguistic difficulties, cally generate language, as well a<.; their relatively clear
but it it goes deeper into the lopsided manner in which division into areas for receptive and expressive skills,
scientists are educated-namely, to be skeptical about both of which are embedded in a broad field of neural
absolutely everything that is difficult to measure, as tissue that generates thought. Propositional language is
opposed to being optimistically open to all of the com the highest achievement of the human brain, and prob
plexities of the world. The proper focus of skepticism ably the most recent major achievement in mammalian
should be toward the end of inquiries, not at the begin brain evolution, probably having emerged with early
ning as it often tends to be in modern psychological and Homo sapiens perhaps a quarter of a million years ago.
neural sciences. For instance, many still do not believe It is puzzling to consider that this is the one function,
that a "social bond'' or "brain mechanisms for social more than any other, with which we must conceptual
affiliation and affect" exist as objective brain functions, ize the many other functions of the brain. Thus, we are
and, sadly, we originally experienced great difficulty in the paradoxical position of trying to clarify every
publishing some of our work on rough-and-tumble play thing that evolved before, using the most recent neural
because we used the wordplay. We were advised to sim instrument in our toolbox of cognitive skills.
The locations of the language areas in the left cere
ply describe the behavior we saw. We have had similar
experiences with distress vocalization (crying) and all brat hemisphere (Figure B . l ), have now been affirmed
Generating Words
333
Speaking Words
BROCA'S AREA
Hearing Words
Seeing Words
WERNICKE'S AREA
Fiur .1. Summary .of la?guage areas of the brain as determined by PET
scans
o mdtvtduals performmg
dtfferent aspects of language. Dark areas indicate
htghest lvels of metabolic activity. When one is speaki
ng words Broca's area s
mos ac1ve. When on is hearing words, Wernicke's
area is most' active. When 1
.
one IS silently gener tmg words or seeing words,
.
tensttcally tach coherent meaning. This suggests that
.
the sntatJc structures and basic urge to speak have
remamed mtact. Because the natural flow of Iincruistic
output appears to be an intrinsic function of Boca's
rea, hen this area is lost, one has great difficulty ar
tJcul ttng any coherent speech. However, the under
standmg of language is intact. When the large neural
334
APPENDIX B
APPENDIX B
335
APPENDIX C
Appendix C
Dualism in the Neurosciences
336
337
338
APPENDIX C
APPENDIX C
339
340
APPENDIX C
1I
APPENDIX C
vvays hy which emotional states effectively control fu
ture behaviors.
Although my view nffirms th<.ll the evolution of
ernotional feelings was linked. to a substantial degree.
to the special needs of brain memory systems that must
rapidly encode intrinsic biological values (sec Chapters
I and 2). I believe that the core of emotionality must
be sought in more fundamental terms than as a mere
subset of working memory, at least of tile type that is
typically conceptualized as a fairly high-level cortical
function. In my research experience. animals with es
sentially no neocortex remain behaviorally, and prob
ably internally, as emotional as ever, indeed more so.16
I have argued, in agreement with investigators such as
Paul MacLean. that the capacity to have affective feel
ings is an evolutionary birthright embedded within the
intrinsic and ancient organizational dynamics of the
mammalian brain, situated largely in subcortical realms
known as the extended limbic system. I feel confident
that this scheme remains a more defensible generaliza
tion than is suggested in LeDoux's severely critical
analysis of the concept.
In sum, I doubt if emotional feelings need to be
!earned or extracted from dynamic memory stores. I
think LeDoux is misguided, as was William James when
he suggested that the cortex is the storehouse for our
emotional feelings. Thus, while LeDoux asserts that we
should confine our efforts largely to traditional behav
ioral and physiological realms in our study of emotions
within the animal brain, I would advocate that we
should, in addition, begin to study emotional feelings,
indirectly, as essential foundation processes upon which
many unique aspects of the human mind-from art to
politics-have been created.
For those who would continue to deny the existence
of emotional feelings in other animals (dearly a popu-
341
Notes
Chapter 1
1. Watson, J. B. ( 1924). Psychologyfrom the stand
Press.
5. A great number of writers have addressed this is
sue from different perspectives, and many key articles
can be found in annual updates of Advances in AnimaL
Behavior. Works that cover most ofthe critical issues are:
Hogan, J. A., & Roper, T. J. ( 1 978). A comparison
of the properties of different reinforcers. Adv. Anim.
Behav. 8 : !55-255.
486.
42:780-786.
3 : 1 87-196.
York: Pantheon.
13. Two texts that cover most of the key issues are:
Posner, M. !., & Raichle, M. E. ( 1 994). Images of
mind. New York: Scientific American Library.
Roland, P. E. ( l 993). Brain activation. New York:
Wiley-Liss.
343
344
j_
345
346
347
348
Chapter 3
1. Taylor, G. J. ( 1 987). Alexithymia: History and
validation of the concept. Transcult. Psychiat. Res. Rev.
39:101-133.
24:85-95.
46:499-502.
349
350
precise nature of the brain mechanisms that mediate processes (for quotation see n. 26, p. 407). This view
can easily be criticized on the basis of evidence show
such processes.
ing how inaccurate introspection has been in generat
13. For a review of modern semantic analyses of the
use of emotional words, see: Russell, J. A. ( 1991 ). ing substantive explanations of behavior in the past, as
Culture and the categorization of emotions. Psych. Bull. well as by those who have demonstrated how exten
sively our behavior is controlled by unconscious pro
! ]0:426-450.
cesses (see chap. 2, n. 12). Although such viewpoints
14. For an energetic debate concerning the facial
analysis of emotions, see: Russell, J. A. ( 1 994). Is there are critically important, my support of the introspective
universal recognition of emotion from facial expres view is premised not on an explanatory level but on the
sion? A review of cross-cultural studies. Psych. Bull. initial descriptive level: We need a method to identify
fundamental psychobiological processes that can be
1 15: 102- 1 4 1 .
clarified only through brain research. The evidence for
For stinging rebuttals, see:
Ekman, P. ( 1994 ). Strong evidence for universals in certain types of emotional processes within the mam
facial expressions: A reply to Russell's mistaken cri malian brain is overwhelming, but the mannner in which
we should speak of them is by no means clear (see
tique. Psych. Bull. 1 15:263-287.
Izard, C. E. ( 1 994). Innate and universal facial ex n. 12). The problem goes as deep as the very nature of
pressions: Evidence from developmental and cross language. In this context, we also need to remember that
the speaking left hemisphere and the comparatively si
cultural research. Psych. Bull. ! ]5:288-299.
15. Rinn, W. E. ( 1 984). The neuropsychology of lent and more emotional right hemisphere have differ
facial expression: A review of the neurological and ent agendas in the control of psychobehavioral pro
psychological mechanisms for producing facial expres cesses (see Chapter 1 6 and Appendix B). Should we
believe that all the semantic distinctions that can be
sions. Psych. Bull. 95:52-77.
created by the left hemisphere (see n. 13) reflect basic
16. Andrews, R. J. ( 1963). The origin and evolu
tion of the calls and facial expressions of the primates. affective realities that exist in all mammals? Probably
not, even though such socially constructed semantic
Behaviour 20:1-109.
realities are obviously real and important aspects of
17. The classic distinction between feelings that
arise from emotions and those that arise from motiva human social life. However, they may be instantiated
tions is based on the existence of distinct bodily refer in the epigenetically derived software functions of the
ents for the latter (e.g., bodily energy, water, tempera brain rather than in the genetically coded hardware.
24. Changes in neural systems as a function of ex
ture), with no clearly regulated bodily states for the
former (also see discussion in Chapter 9). As we come perience have become a powerful force in conceptual
to recognize the neurochemical causes of emotions, izing the epigenetic construction of the nervous system
especially the specificity provided by neuropeptide and mind. Some of the earlier work on this topic is suc
systems (see Chapter 5), this distinction has become less cinctly summarized in: Rosenzweig, M. R., & Bennett,
E. L. ( 1 996). Psychobiology of plasticity: Effects of
defensible.
training and experience on brain and behavior. Behav.
18. Panksepp, J. ( 1 992). A critical role for "affec
tive neuroscience" in resolving what is basic about basic Brain Sci. 78:57-65.
More recent work that has probed the fine det:til of
emotions. Psych. Rev. 99:554--560. Quotation on p. 554.
such processes can be found in: Greenough, W. T.,
19. Kleinginna, P. R., & Kleinginna, A .M . (1981 ).
A categorized list of emotion definitions, with sugges Black, J. E., & Wallace, C. S. ( 1 987). Experience and
tions for a consensual definition. Motiv. Emot. 5:345- brain development, Child Devel. 58:539--559.
Direct evidence for long-term functional changes in
379.
emotional systems is available in: Adamec, R. E. (1993).
20. This neural defintion of emotion was first pro
posed in 1982 (see n. 26); to my knowledge, no one has Lasting effect ofFG-7142 on anxiety, aggression and lim
yet generated an alternative brain-based definition of bic physiology in the rat. J. Neurophysiol. 7:232-248.
Obviously, the genetically provided operating sys
emotions.
tems of the brain do not mature normally unless they
21. James, W. (1905). The place of affcctional facts
in a world of pure experience. J. ofPhil. Psych and Sci. receive abundant input from the environment. Thus, if
one keeps a young animal, such as a kitten, in a dark
Methods 2:281-282.
closet during the first months of life, it will never de
22. Obviously, there are many ways to carve up the
natural world scientifically. The manner in which physi velop proper visual capacity (see chap. 2, n. 53).
25. I first utilized this type of chaining maneuver
cists came to accommodate the wave and particulate con*
ceptions of subatomic particles is one of the most striking in: Panksepp, J. ( 1 98 1 ). Hypothalamic integration of
examples of the type of compromises that neuroscientists behavior: Rewards, punishments and related psycho
interested in the integrative functions of the brain will have logical processes. In Handbook of the hypothalamus.
to make in abundance. An intriguing assault on the claim Vol. 3, part B, Behavioral studies of the hypothalamus
that science can reveal absolute truth is to be found in: (P. J. Morgane & J. Panksepp, eds.), pp 289-43 1 . New
Johnson, G. (1995). Fire in the mind: Science,jaith, and York: Marcel Dekker.
The intent of the lexical chaining was to highlight
the search for order. New York: Knopf.
23. For many years, I have advocated the utility of the self-evident fact that all basic emotional system are
introspection in guiding our thinking about emotional bound to have many verbal referents.
351
352
Chapter 4
1. Glezer, I. 1., Jacobs, M. S., & Morgane, P. J.
I
I
Psycho!. 5 1 : 355-365.
7. Besides differences in the types of information
they collect (interoceptive versus exteroceptive), some
of the key differences between the visceral and somatic
nervous systems are anatomical location (visceral is
more medially situated in the brain stem), electrophysi
ological (visceral-limbic neurons fire at a slower rate
and hence consume less blood glucose), and neuro
chemical (many of the neuropeptide circuits that con
trol the emotions I will discuss in this book are much
more concentrated in the visceral-limbic nervous sys
tem). Finally, at an overall functional level, limbic and
somatic seizures tend to have different symptoms and
follow different channels of propagation within the
nervous system. Also, we can obtain many emotional
effects (both autonomic and behavioral) by electrically
stimulating brain areas subsumed within the limbic
system concept, but rarely from the higher reaches of
the brain. Of course, somatic and visceral-limbic pro
cesses are highly interactive within the brain, but the
distinction between limbic and somatic nervous systems
is not an arbitrary conceptualization, as recently argued
by some neuroanatomists, but one that is deeply in
grained within many organizational and functional pat
terns of the brain.
8. To my knowledge, such an experiment has never
been published, even though I measured this phenome
non more than 20 years ago (Panksepp, 1 974, unpub
lished data). Modulation of spinal reflexes by various
stimuli is a well-established neurological finding. For
instance, all one needs to do to intensify the patellar
retlex is to tense the upper body by pressing the hands
together in front of one's chest. For a recent demonstra
tion of this type of an effect, see: Bonnet, M., Bradley,
M. M., Lang, P. J., & Requin, J. (1 995). Modulation of
spinal reflexes: Arousal, pleasure, action. Psycho
Amer. 275:2-7.
1 :3 5 1 -360.
353
19:5 !4-520.
physiol. 32:367-372.
9. One way to conceptualize the evolution of higher
brain functions is as providing ever-increasing "openness"
to brain systems that control fairly stereotyped and rela
tively fixed behavior patterns. However, it must be remem
bered that all behaviors, even simple spinal reflexes, are
modulated from above (see n. 8). This is one reason the
classic study of reflexes has typically used decerebrate
animals, especially ones whose brains are transected at the
rnidcollicular level (i.e., thecerveau isole preparation), so
as to leave the tonic excitatory influences of the lower brain
stem intact, which facilitates the study of reflexes, since a
high spinal section leads gradually to a muscular flaccid
ity. For review see: Liddell, E. G. T. (1960). Discovery of
reflexes. New York: Oxford Univ. Press.
10. Cajal's famous summary of brain anatomy,
published in 1909 as a two-volume contribution in
354
27:362-404.
36. Kltiver-Bucy syndrome was first observed in
monkeys. See: Kltiver, H., & Bucy, P. C. ( 1 939). Pre
liminary analysis of functions of the temporal lobes in
monkeys. Arch. Neural. Psychiat. (Chicago) 42:979-
1000.
120:259-295.
Chapter 5
1. Caudill, M. ( 1 992). /n our own image: Building
an artificial person. New York: Oxford Univ. Press.
Jubak, l ( 1 992). In the image of the brain: Break
ing the barrier between the human mind and intelligent
machines. Boston: Little, Brown.
355
356
357
358
359
360
J.
Chapter 6
1. For a thorough review of genetics and develop
mental biology, see: Lewin, B . ( 1 993). Genes V. New
York: Oxford Univ. Press.
Michel, G. F., & Moore, C. L ( 1 995). Developmen,
tal Psychobiology. Cambridge, Mass.: MIT Press.
2. For a more thorough review of neurochemistry,
see: Cooper, J., Bloom, F., & Roth, R. ( 1 996). The bio,
chemical basis of neuropharmacology (7th ed.). New
York: Oxford Univ. Press.
3. It is noteworthy that the third neucleotide of the
"triplet code" is redundant and hence carries less infor
mation than the first two nucleotides, where a change
always specifies a different amino acid. Accordingly,
mutations of the third nucleotide are more neutral and
hence are less likely to be "seen by" the selection pro
cesses of evolution. In a similar vein, genes are func-
Press.
Neurotoxicology 15:535-544.
Olney, l. W., & Farber, N. B. (1995). NMDA an
Neuropsychopharmacology 13:335-345.
8. Olney, J. W., & Farber, N. B. ( 1 995). Glutamate
receptor dysfunction and schizophrenia. Arch. Gen.
Psychiat. 52:998-1007.
9. Only some peptides given peripherally do enter
the brain in amounts large enough to modify behavior.
See:
Banks, W. A., & Kastin, A. J. ( 1 985). Permeability
of the blood-brain banier to neuropeptides: The case
for penetration. Psychoneuroendocrinol. 4: 385-399.
Ermisch, A., Brust, P., Kretzschmar, R., & Ruhle,
H.-J. ( 1 993). Peptides and blood-brain barrier transport.
361
362
363
364
.1I
365
366
NOTES TO PAGES 1 1 8- 1 2 7
.J
367
368
NOTES TO PAGES 1 3 1 -1 34
369
370
371
372
1I
I
373
1
374
375
376
377
378
1.
I
I
'
379
I
380
381
382
383
384
j_
385
th
386
Chapter 1 0
1. See Lorenz, K . ( 1 966). On aggression. New
York: Harcourt, Brace, and World.
387
388
389
390
391
392
NOTES TO PAGES 2 1 1 -2 1 5
393
394
395
396
Chapter 1 2
All quotations from Tolstoy's Kreutzer Sonata in
this chapter are from L Tolstoy, The Kreutzer Sonata
and Other Tales, translated by Aylmer Maude (London:
Oxford University Press, 1889/1 924). Page numbers of
quotations are given in the text.
1. Even in species where reproduction occurs by
nonsexual parthogenesis, sexual activity continues,
apparently as a way to keep the reproductive apparatus
healthy. See: Crews, D. ( 1 992). Diversity of hormone
behavior relations in reproductive behavior. In Behav
ioral endocrinology (1. B. Becker, S. M. Breedlove, &
D. Crews, eds.), pp. 143-186. Cambridge, Mass.: M!T
Press.
2. Buss, D. M. ( ! 994). The strategies of human
mating. Amer. Sci. 82:238-249.
'j
l
397
398
399
400
(L. L.
401
402
403
404
hypotha
in
Fos-Lir
on
ce
Effects of maternal experien
Maternal behavior in the rat. London:
(1933).
M.
N.
lamic, limbic, and cortical structures in the postpartum
Oliver
and
Boyd.
82.
rat. Behav. NeUIosci. 1 10:567-5
When rediscovered, it was call "sensitization." See:
27. The olfactory memory appears to be mediated
Rosenblatt, l. S. ( 1967). Nonhormonal basis of mater
See:
bulbs.
y
olfactor
the
by norepinephrine within
nal behavior in the rat. Science 156:1512-1514.
Pissoinier, D., Thiery, J. C., Fabre-Nys, C., Poindron,
36. Soloff, M. S., Alexandrova, M., & Fernstrom,
olfac
of
nce
importa
The
985).
P & Keverne, E. B. ( 1
M.
J. ( 1 979). Oxytocin receptors: Triggers for parturi
tory bulbs and noradrenaline for maternal recognition
tion and lactation? Science 204: 1 313-1314.
63.
35:361-3
in sheep. Physiol. Behav.
37. Insel, T. R. (1986). Postpartum increases in brain
In animals like sheep, the social attraction becomes
oxytocin binding. Neuroendocrinol. 44:5 15-518.
to
tend
mothers
and
rapidly,
highly discriminating very
Insel, T. R. ( 1 992). Oxytocin: A neuropeptide for
reject other sheep soon after the bond has formed. On
affiliation--evidence
from behavioral, autoradiographic
bond
olfactory
their
develop
the other hand, mother rats
and comparative studies. Psychoneuroendocrinol. 17:
more to the nest than to the pups, which makes cross
3-35.
fostering of animals an easy manipulation.
38. Numan, M. (1988). Maternal behavior. ln The
28. For a summary of the confusion that accompa
physiology ofreproduction (E. Knobil & l. Neill, eds.),
mater
-induced
oxytocin
of
ion
nied the initial observat
pp. 1 569-1645. New York: Raven Press.
nal behavior, see page 59 in Pedersen, C. A., Caldwell,
39. Hansen, S., & Kohler, C. ( 1984). The impor
A.
G.
Mason,
&
H.,
C.
J. D., Peterson, G., Walker,
tance of the peripeduncular nucleus in the neuroendo
( 1992). Oxytocin activation of maternal behavior in the
crine control of sexual behavior and milk ejection in the
rat. Ann. N. Y. Acad. Sci. 652:58-69.
rat. Neuroendocrinol. 39:563-572.
In brief: The original groups of animals in which
40. Jirikowski, G. F., Caldwell,l. D., Stumpf, W. E.,
chronic
had
r
behavio
l
oxytocin precipitated materna
& Pedersen, C A. (1988). Estradiol influences oxytocin
respiratory ailments that reduced their olfactory acuity.
immunoreactive brain systems. Neuroscience 25:237Now we know that in animals whose ability to smell is
248.
impaired by the removal of the olfactory bulbs, oxyto
41. Numan, M. ( 1 990). Neural control of maternal
cin is quite effective in triggering maternal behavior.
behavior. I n Mammalian parenting (N. A. Krasnegor
See: Wamboldt, M. Z., & Insel, T. R. ( 1987). The ability
& R. S. Bridges, eds.), pp. 23 1-259. New York: Ox
of oxytocin to induce short-latency maternal behaviour
ford Univ. Press.
is dependent on peripheral anosmia. Behav. Neurosci.
42. Numan, M. ( 1 994). A neural circuitry analysis
1 0 1 :439-441 .
of maternal behavior in the rat. Acta Paediatrica 397
29. Fahrbach, S. E., Morrell, J. 1., & Pfaff, D. W.
( 1986). Effect of vary ing the duration of pretest cage (suppl.): 1 9-28.
An intriguing way to study nurturance circuits in
habituation on oxytocin induction of shortlatency
males has been through their tendency to exhibit "ma
maternal behavior. Physiol. Behav. 37: 1 35-139.
ternal" aggression following hormonal pretreatment.
30. Van Leengoed, E., Kerker, E., & Swanson, H. I-I.
( i 987). Inhibition of post-partum maternal behavior i n See: Rosenblatt, J. S., Hazelwood, S., & Poole, J.
.
I
I
405
406
407
l
408
vocalization (1. D. Newman, ed.), pp. 43-65. New (C. Magai & S. H. McFadden, eds.), pp. 3-26. San
Diego: Academic Press.
York: Plenum Press.
25. Seen. 24 and: Andrew, R. J. ( 1 969). The effects
Schuller, G., & Radtke-Schuller, S. ( 1 988). Neural
control of vocalization in bats at peripheral to midbrain of testosterone on avian vocalizations. In Bird vocal
levels. In The physiologicaL control ofmammalian vo izations (R. A. Hinde, ed.), pp. 97-130. Cambridge:
calization (1. D. Newman, ed.), pp. 67-85. New York: Cambridge Univ. Press.
We have also done a great deal of work on testoster
Plenum Press.
Buchwald, J. S., Shipley, C., Altafullah, !., Hinman, one modulation ofDVs in young chicks, but the results
C., Harrison, J., & Dickerson, L. ( 1 988). The feline are not published. One small experiment conducted just
isolation call. In The physiological control ofmamma for illustrative purposes is shown in Figure 14.5.
26. Rachman, S. (ed.) ( 1 996). Panic disorder: The
lian vocalization (J. D. Newman, ed.), pp. 1 19- 1 35.
facts. Oxford: Oxford Univ. Press.
New York: Plenum Press.
27, Herman, B . H., & Panksepp, J. ( 1 9 8 1 ). Ascend
19. Keverne, E. B., Martensz, N., & Tuite, B .
( 1989). B-Endorphin concentrations in CSF o f monkeys ing endorphin inhibition of distress vocalization. Sci
are influenced by grooming relationships. Psychoneuro ence 2 1 1 : 1 060-l 062.
Panksepp, J., Normansell, L., Heiman, B., Bishop, P.,
endocrinol. 14: 1 55-161.
Montagu, A. ( 1 978). Touching: The human signifi & Crepeau, L. (1988). Neural and neurochemical con
trol of the separation distress calL ln The physiological
cance of the skin. New York: Harper and Row.
control of mammalian vocalizations (1. D. Newman,
20. Although there is no direct evidence that such
chemical changes in the brain mediate human feelings ed.), pp. 263-299. New York: Plenum Press.
28. Panksepp, J. ( 1991). Affective neuroscience: A
of love and devotion, this theoretical proposal is bol
stered by a great deal of evidence in animals, such as conceptual framework for the neurobiological study of
emotions. In International reviews ofemotion research,
summarized in nn. 9, 19, and 2 1 .
vol. 1 . (K. Strongman, ed.), pp 59-99. Chichester, U.K.:
21. Panksepp, 1., Herman, B . H., Vilberg, T.,
Bishop, P., & De Eskinazi, F. G. ( 1980). Endogenous Wiley.
29. See n. 28 and: Panksepp, J., Siviy, S. M., &
opioids and social behavior. Neurosci. Biobehav. Revs.
Normansell, L. A. ( 1 985). Brain opioids and social
4:473-487.
emotion. In The psychobiology ofattachment and sepa
22. De Lanerolle, N. C., & Lang, F. F. ( 1 988). Func
tional neural pathways for vocalization in the domestic ration (M. Reite & T. Fields, eds.), pp 3-49. New York:
cat. In The physiologicaL control of mammalian vocal Academic Press.
30. Normansell, L. ( 1988). Effects of excitatory
ization (J. D. Newman, ed.), pp. 2 1-4 1 . New York:
amino acids on emotional and sensorimotor behaviors
Plenum Press.
JUrgens, U., & Ploog, D. ( 1 988). On the motor co in the domestic chick. Ph.D. diss., Bowling Green State
ordination of monkey calls. In The physioLogical con University.
Panksepp, J. ( 1 996). Affective neuroscience: A para
trol of mammalian vocaliz.ation (1. D. Newman, ed.),
digm to study the animate circuits for human emotions.
pp. 7-19. New York: Plenum Press.
Lloyd, R. L., & Kling, A. S. (1988). Amygdaloid In Emotions: Interdisciplinary perspectives (R. D.
electrical activity in response to conspecific calls in Kavanaugh, B . Zimmerberg, & S. Fein, eels.), pp 29-60.
squi!Tel monkey (S. sciureus): Influence of environmen Mahwah, N.J.: Lawrence Erlbaum.
31. See no. 8, 9, 2 1 , 28, 29, 32, and 66.
tal setting, cortical inputs, and recording site. In The
32. Panksepp, J., Bean, N. J., Bishop, P., Vi!berg,
physiological control ofmammalian vocalization (J. D.
Newman, ed.), pp. 137- 1 5 1 . New York: Plenum Press. T., & Sahley, T. L. ( 1 980). Opioid blockade and social
Robinson, B. W. ( 1 967). Vocalization evoked from comfort in chicks. Pharmacol. Biochem. Behav. 1 3 :
forebrain in Macaca mu!ata. Physio!. Behav. 2:345- 673-683.
33. Hofer, M. A. ( 1996). Multiple regulators of
354.
ultrasonic vocalization in the infant rat. Psychoneuro
23. In primates and birds, CRF increases DVs, but
endocrinol. 2 1 :203-2 17.
in infant rats it decreases them. See:
Panksepp, J., Newman, J., & lose!, T. ( 1 992). Criti
Panksepp, J. ( 1990). A role for affective neuro
science in understanding stress: The case of separation cal conceptual issues in the analysis of separation-dis
distress circuitry. In Psychobiology of stress. NATO tress systems in the brain. In International reviews of
ASI Series D: Behavioural and Social Sciences, Vol. emotion research, vol 2 (K Strongman, ed.), pp. 5 1-72.
54 (S. Puglisi-Allegra & A. Oliverio, eels.), pp. 41-57. Chichester, U.K.: Wiley.
For an analysis of the neurochemical substrates of
Dordrecht: Kluwer Academic.
Harvey, A. T., & Hennessy, M. B. ( 1 995). Corti rodent ultrasonic vocalizations, see:
Hard, E., & Engel, J. ( 1991). Ontogeny of ultrasonic
cotropin-releasing factor modulation of the ultrasonic
vocalization rate of isolated rat pups. Devel. Brain Res. vocalization in the rat: Int1uence of neurochemical
transmission systems. In Behavioral biology: Neuroen
87: 1 25-134.
docrine axis (T. Archer & S . Hansen, eds.), pp. 37-52.
24. For a summary of these unpublished findings
of T. Sahley and J. Panksepp, see: Panksepp, J., & Hillsdale, N.J.: Lawrence Erlbaum.
Miczek, K. A., Tornatzky, W., & Vivian, J. ( 1 991).
Miller, A. ( 1 996). Emotions and the aging brain. In
Handbook of emotion, adult development, and aging Ethology and neuropharmacology: Rodent ultrasounds.
409
410
411
412
413
414
415
41 6
41 7
41 8
Differ
994).
l
(
R.
Buck,
&
Ross, E. D., Homan, R. W.,
12. At the present time, most behavioral neurosci
ential hemispheric lateralization of primary and socml
l. entists remain unwilling to grant intangible conscious
emotions. Neuropsychiat. Neuropsych. Behav. Neura
processes such as perceptual awareness and internally
7 : 1-19.
l felt experience to their animal subjects. However, this
3. One of the startin g premises of cognitive psycho
is commonly done less on the basis of reasoned argu
oay was the scientifically problematic nature of emo
ments than habitual assertions that anthropomorphism
for
issues
e
Twelv
.
(1980)
ti nality. See: Norman, D. A.
is bad and the conviction that such internal processes
cognitive science. Cog. sci. 4: 1-32.
.
will never be "seen" or "weighed" with sufficient ac
psy
4. For some thoughts on the fragmentatiOn of
to be useful scientifically. In addition, the con
curacy
chology, see chap. 1, n. 8, as well as:
neglect of consciousness (at least at the neuro
tinuing
lpsycho
of
ntation
fragme
Bower, G. H. ( 1993). The
l level, if not the conceptual one) is partly due
empirica
ogy" Am. Psycho!. 48:905-907.
.
to the fact that many investigators of animal brain func
Koch, S. (1993 ). "Psychology" on "the psychologi
tions are not primarily interested in how their findings
cal studies'"! Am. Psycho!. 48: 902-904.
relate to human issues. Many are simply and justifi
may
affec
d
induce
ation5. The varieties of brain stimul
interested in animal behaviors and brain functions
ably
,
1
tive experiences in humans are summarized in chap.
for their own sake. However, for others who believe that
n. 20.
to much of the importance of animal brain research lies
6. The extent to which we have conscious access
in its ability to deeply clarify the human condition, the
ed
analyz
lly
critica
been
the causes of our behavior has
neglect of consciousness by neuroscientists often seems
by many, most prominently by: Nisbett, R. E., & Wil
be an irrational and uncourageous choice. Of course,
to
know:
can
we
than
son, T. D. ( 1 977). Telling more
much easier to talk about such matters than
remains
it
84:
Verbal reports on mental processes. Psych. Rev.
to do illuminating experiments on them. Most agree that
23 1-259.
the highest levels of human perceptual consciousness
However, the documented failures of introspective
closely linked to sensory analyzers of the cortex,
are
ive
cognit
of
is
analys
insight typically come from the
intentionality and conscious planning are closely
while
processes. It remains unclear whether such arguments
99. Knoll, J. ( 1988). The striatal dopamine depen
419
420
cal reaches of the brain that are very distinct from the
language cortex. However, the two processes may be
coordinated in motivational areas such as the anterior
cingulate cortex which seems to provide the psychic
energy for people to communicate linguistically (see
Appendix B). In this context, it is noteworthy that to a
substantial extent human speech may still serve primi
tive affective functions such as social grooming at a
distance, where "what matters is not what you say, but
how you say it," as expanded upon in: Dunbar, R. I. M.
( 1 993). Coevolution of neocortical size, group size and
language in humans. Behav. Brain Sci. 16:681-735.
For a full comparative view of communication, see:
Hauser, M. D. ( 1996). The evolution ofcommunication.
Cambridge, Mass.: MIT Press.
36. One of the great achievements in this realm is
the demonstration that the environmentally induced
neural patterns from waking states can be detected dur
ing sleep. See chap. 7, n. 1 5 .
37. Bekoff, M., & Jamieson, D . (eds.) ( 1 99S). Read
ing in animal cognition. Cambridge, Mass.: MIT Press.
38. George, M. S., Ketter, T. A., Kimbrell, T. A.,
Speer, A. M., Steedman, J. M., & Post, R. M. ( 1996).
What functional imaging has revealed about the brain
basis of mood and emotion. Advances in Biological
Psychiatry, vol. 2 (l Panksepp, ed.), pp. 63-1 13. Green
wich, Conn.: JAI Press.
39. Kelso J. A . (1995). Dynamic patterns. Cam
bridge, Mass.: MIT Press.
Turbes, C. C. (1 993). Brain self-organization dy
namics. Biomed. Sci. Instrwn. 29: 1 35-146.
40. For an example of how this is achieved at a fairly
low level of the neuroaxis, see: Kalesnykas, R. P., &
Sparks, D. L. ( 1996). The primate superior colliculus
and the control of saccadic eye movements. Neurosci
entist 2:284-292.
41. Strehler, B. 1. (1991). Where is the self? A neu
roanatomical theory of consciousness. Synapse 7:4491.
42. It is likely that several coordinated functions of
the brain stem are necessary for establishing a network
for the basic SELF, but I will limit the present discus
sion to a simplified outline of the relevant issues. The
issue of whether these low areas of the brain stem can
elaborate any form of conscious experience is debatable,
but the relevant experiments-namely, those in very
young organisms-remain to be done. I would suggest
that during early development these systems lie at the
heart of conscious experience and that only gradually
during development do these lower functions become
so automatized that they no longer are the focus of ac
tive attention. Attention may become more entranced
by the flow of information through the thalamic-neo
cortical axis that comes to constitute the contents of
consciousness. Still, I would hypothesize that the lower,
primary-process substrates of consciousness remain as
an essential neural scaffolding for the higher levels of
consciousness to be elaborated.
43. The entertaining notion of a Cartesian theater
is discussed by Dennett (see n. 33). Many eschew the
concept of a central agency within consciousness. For
421
422
423
424
425
426
427
428
Appendix C
1. For a summary of this interpretation of the ac
tions of Descartes, see chap. 16, n. 34.
2. For overviews of such approaches, see: Gaz
zaniga, M. S. (ed.) ( 1 995). The cognitive neurosciences.
Cambridge, Mass.: MIT Press.
3. Campbell, J. ( 1 982). Grammatical man: Infor
mation, entropy, language, and life. New York: Simon
and Schuster.
4. See the references to Chapter 1 6 and all issues
of the journal Consciousness and Cognition.
5. Penfield, W. ( 1 975). The mystery of the mind: A
critical study of consciousness and the human brain.
Princeton, N.J.: Princeton Univ. Press. Quotation on pp.
56, 79, 80, 8 1 (emphasis in original).
6. Sperry, R. W. ( 1969). A modified concept of con
sciousness. Psych. Rev. 76: 532-536.
Sperry, R. W. ( 1 970). An objective approach to
subjective experience: Further explanation of a hypoth
esis. Psycho/. Rev. 77:585-590.
Sperry, R. ( 1982). Bridging science and values: A
unifying view of mind and brain. In Mind and brain: The
many-faceted problem (J. Eccles, ed.), pp. 255-269.
Washington, D.C.: Paragon House. Quotation on p. 258.
7. For a full description of Sperry's social views, see:
Sperry, R. (1992). Science and moral priority: Merging
mind, brain, and human values. New York: Columbia
Univ. Press.
Also see:
Sperry, R. W. ( 1 993). Psychology's mentalist para
digm and the religion/science tension. In Brain, culture,
and the human spirit: Essaysfrom an emergent evolu
tionary perspective (J. B. Ashbrook, ed.), pp. I 09-128.
Lanham, Md.: Univ. Press of America.
Sperry, R. W. ( 1984). Consciousness, personal iden
tity and the divided brain. Neuropsychologia 22:661673.
429
Although I have tried earnestly to update relevant literature citations in the notes, work in
this area is moving at a rapid pace. There would be much to incorporate from the year and
a half since this manuscript was submitted to the publisher. Rather than attempt the impos
sible, I would like to symbolically select the one paper that I have found to be most impres
sive from this time period. It is a paper analyzing the cerebral consequences of social stress
by Kollack-Walker, S., Watson, S. J., & Akil, H. ( 1997) Social stress in hamsters: Defeat
activates specific neurocircuits within the brain . ./. Neurosci. 15:8842-8855.
I select this paper partially because I have been contemplating the possible existence of
a basic "DOMINANCE" system for some time, and this work provides the best evidence to
date (using cFos in situ hybridization) concerning how such a process might be elaborated
in the mammalian brain. This paper carefully analyzed genetic arousal of neural systems in
dominant and submissive animals after half an hour of social confrontation/aggression us
ing a resident-intruder paradigm in pairs of males who did not know each other well. It helps
highlight for us not only the powerful effect of social submission (and FEAR) on the brain,
but how much less the emotional systems of the dominant animals are aroused. The largest
increase in arousal seen in the victors was in the supraoptic nucleus of the hypothalamus,
where vasopressin systems are concentrated.
This paper again helps highlight for us the widespread consequences of emotional arousal
within the brain (also see, chap. 1 1 , n. 97). To some extent, such widespread effects may
seem inconsistent with the existence of fairly discrete emotional systems in the brain, but
such findings are, in fact, very compatible with the present thesis. The basic anatomical fact
about emotional systems is that they have remarkably widespread consequences in the brain
(Figure 3.3), and they also interact with many general modulatory systems (Figures 3.6,
6.5, and 6.6) of the brain. It must obviously be the case that emotions have diverse effects
on the brain-for the mental consequences of emotional arousal in humans affect essen
tially all other brain and bodily functions. It will be a most interesting chapter of future
research when we begin to dissect, anatomically and functionally, those subcomponents
within the brain that lead to the final integrated psychobehavioral response.
Author Index
Altafullah, L, 408
Altar, C. A., 352
Alvarado,
R.
394
R.,
359
Adams, N., 4 1 6
Adolphs,
Ambonetti, A., 3 5 1
R.,
396
Ambrose, J. A . , 4 1 4
Ames, C. D . , 384
Amoss, M. S . , 403
Andrade,
Al-Dokhayel, A . , 384
R.
Alexander
D., 397
R.
D., 260
R.,
Allegeier,
A., 245
R.
245
Andrew,
R.,
363
Andrews,
Appleton,
R.
E., 4 1 3
Appollonio, L, 394
Aquet, M., 387
R.,
323, 426
R.,
401
Allman, W. F., 4 1 2
Armstrong, T., 4 1 7
Almli, C.
Arndt, S . , 378
R.,
347
Alolis, 0., 4 1 3
R., 205,
387
Anderson, E., 80
R., 344
Aronson, L.
Aiendt, J., 37 l
Arnold, A . P . , 347
Arnold, S. E., 397
Axelrod,
Azumi,
R.,
K.,
426
379
Bagby,
R. M., 341
R. E., 395
Bagdon,
R., 400
R. R., 397
431
432
AUTHOR INDEX
AUTHOR INDEX
Bell, L R., 245, 359
Barakat, A. S . , 401
Bloom, $. R., 3 8 1
Bard, P, 354, 4 1 5
Barkow, J . , 2 3 , 343
Boccia, M. L., 4 1 9
Boer,
Benton, D., 4 1 1
Barfield, R . J . , 399
Barkley, R. A., 4 1 7
Barlow, G . W . , 397
Barnard,
K.
E., 409
K.,
367
Boice, R., 4 1 6
Baron-Cohen, S., 4 1 2
Berendse, H. W., 4 1 5
Barondes, S . H., 4 1 2
Barone, F. C . , 378
Bolk, L., 4 1 7
Bolles, R . C . , !86, 380, 393
Barresi, J., 4 1 9
Bonner, T . I . , 360
Bashinksi, M., 3 8 1
Baskin, D . G . , 3 8 1 , 382
Bordon, J. H ., 398
Born, J., 402, 4 1 3
Bateson, P., 4 1 4
Borod, J. C . , 424
Batini, C . , 369
Borowsk, T. B . , 379
Bauer, R M., 4 1 9
Bertolini, A., 40 I
Bevans, P. . 361
Bousfield, D., 1 19
Beak, S. A., 3 8 1
Bean, N. B., 407
Bean, N. J., 386, 408, 4 1 0
Beatty, W. W., 399, 4 13-415
Beaulieu, I., 370
Bierley, R. A., 4 1 5
Boyer, W. F., 4 1 1 , 4 1 2
Boysen, S . T . , 354
Bisette, G., 4 1 1
Bradley, C., 4 1 7
Blanchard, R . J . , 396
K . , 343
K.,
381
Britton, K. T. , 395, 4 1 1
Broda!, A., 80
Brodie, J., 4 1 6
Bronen, R . A . , 398, 403, 427
Bronowski, J., 359
Burgdorf, J., 4 1 5
Burger, H. , 401
V., 388
Castellanos, F. X., 4 1 7
Castelloe, P . , 427
K.
W, 383
Chapman, A. J., 4 1 5
Charms, R . C . , 355
Chase, T. N., 4 1 7
Chavez, M . , 383
Cannon, W. B., 3 5 1
Capelli, S . , 1 0 3
Capitanio, J. P., 379, 407, 4 1 1
Caplan, D., 427
Carden, S . E. , 407, 4 \ 0
Cardinal, D. N., 428
Cardinali, D. P., 368
433
Cloninger, C. R . . 422
434
AUTHOR INDEX
AUTHOR INDEX
Cousins, N., 4 1 7
Cowley, D. S . , 395
Couvering, J . V . , 426
Cox, J. F., 415-417
Cox, V. C., 376
Cox, W., 364
Ebert, P . D., 4 1 0
Fehm, H. L., 4 1 3
Fehm-Wolfsdorf, G . , 402, 4 1 3
Feighner, J. P., 4 1 2
Devos, M., 3 8 1
Feldman, H. M . , 402
D e VosFrerichs, T . P . , 388
Edelson, S. M . , 365
Feldman, R. S., 1 19
Edwards, C. M. B., 3 8 1
Eismann, C . H . , 423
Dickinson, A., 4 1 9
Dickstein, D . P., 4 1 7
Dierkes, T., 96
D.
A., 385
409, 4 1 4
Degueldre, C., 367
De Jonge, F. H., 401
De Kloet, E. R., 362, 366, 371, 380,
391
Daan, S. , 368
Cooper, B . R . , 383
Cooper, J., 360
Cooper, J. R., ! 1 9
Cooper, S . J., 163, 373, 3 8 1 , 384, 386
Cooper, T. B., 362
Einon, D. F., 4 1 3 , 4 1 4, 4 1 6
Connolly, K . , 4 1 4
Fernstrom, M. J ., 404
Einon, F . D . , 4 1 6
Eibl-Eibesfelt, I . , 4 1 5
Dewsbury, D. A., 4 1 4
Deyo, R . A . , 396
Feritag, M., 80
R.
D., 4 1 0
Ferchmin, P. A., 4 1 6
Field, E . G., 4 1 5
Diksic, M., 96
Doane, B. K., 4 1 9
Dodge, K. A . , 388
Dodge, L. J., 4 1 4
Doge, A. M . , 4 1 4
Dollard, J . , 205
Espezel, H., 4 1 3
Estall, L . B . , 386
Eterovic, V. A., 4 1 7
Etgen, A . M . , 399
Fiuglcwics, D. P., 3 8 1
Y .,
360
Flanagan, L M . , 401
Fleischhauer, A. E., 4 1 6
425
Falk, J. L, 378
Dugovic, C . , 369
Dum, J., 386
435
Farah, M. J., 4 1 8
Faravelli, C . , 351
Fonnsell, F., 3 5 1
Foot, H . C., 4 1 5
436
AUTHOR INDEX
AUTHOR INDEX
France, R. D., 4 1 1
R.
A., 345
Harmon, R . , 260
R.,
365
Ganten, D., 1 I 9
Harrington, A, 4 1 9
Harris, B. S . , 383
R.
GuillordBataille, M . , 4 1 2
Harris,
Gunn, I., 3 8 1
Guo, Q . , 404, 4 1 7
Our, R. C . , 397
Our, R. E., 397
Gurney, A., 382
B., 381
Gurski, J. C., 4 1 0
Gusella, J . F . , 348
Ghatel, M. A., 3 8 1
Ghosh, A . , 365
Gibo, D. M., 4 1 2
Gibson, G., 355
Girodias, V ., 370
Giriunas, L, 423
Giros, B., 362
Glennon, J. A., 3 8 1
Gray, T. S . , 394
R.,
366, 371
Grenhoff, J . , 378
Godbout,
R.,
370
Hagberg, B., 4 1 2
Hager, 1. L . , 343
Herren-Kohl, L . R . , 400
Herrnstein, R. J., 348
Herscovitch, P., 348, 356, 360, 396
Herting, R. L., 362
Hery, F., 372
Hodges, D. A., 4 1 3
Haymaker, W., 80
Halaas, J. L., 3 8 1
Heath,
R.
Hahni, K. A., 3 8 1
Hamburg, M . D . , 374
Hamburger, S . D., 4 1 7
R.,
R.,
358, 427
Hemsley, D.
Hamcdani, A. G . , 378
Hamilton, B. S . , 383
Heron, W., 4 1 9
Haith, M., 4 1 4
Halperin, J. M . , 373
Galpern, W.
369
375
R. M.,
Harre, R., 349
Greeenberg,
Harper,
Gajiwala, K. S., 3 8 1
Harlow, M. K . , 4 1 1 , 4 1 3
Groenewegen, H. J., 4 1 5
R.,
Harbaugh, C.
Gilbey, S . G . , 384
Giedd, J. N., 4 1 7
Harlow, E. M., 4 1 1
Gomez, M . , 401
Groos, K . , 298
Gaudilliere, 1. P., 3 8 1
R.
Gold,
424
Hamlin, P., 3 8 1
Henchel, A., 3 8 1
Hammer, N. J . , 383
Hole, G. J., 4 1 3
Holley, T. L., 389
Homan, R. W., 4 1 8
Hooks, M. S . , 359
437
Horn, C., 4 1 0
438
AUTHOR INDEX
AUTHOR INDEX
Juraska, J. M., 4 1 6
Knomura, S . , 369
JUrgens, U . , 408
Kerker, E . , 404
Kajimura, N . , 356
Jan, J. E., 4 1 3
Hunsperger, R. W ., 389
Koffel, B . , 422
Krain, A. L., 4 1 7
Karp, J. F., 4 ! !
Lassen, N. A, 356
Lasser, G., 38\
Katsuki, Y . , 186
Krishnan, K. R., 4 1 1
Klein, R G.,417
Klein, W. J., 373
Ishijima, B., 4 1 9
Johnson, W. A., 40 I
Jolicoeur, F. B., 384
Jacobs, B . , 428
Lanthier, D . , 386
Johnson, D. F., 3 8 1
Lange, N., 4 1 7
Ionescu, E . , 382
lsacson, 0., 365
Lambert, A. J., 4 1 9
Lambert, N . A . , 375
Kieffer, S . W . , 426
Kibb!er, C. C., 4 ! 6
Kaplan, J . , 4 1 1
Konopacki, J . , 395
Kapas, L . , 368
Kapitony, T., 3 7 1
Hupka, R. B . , 406
Kerdelhue, B . , 4 1 3
Hunag, Y. H . , 347
Kent, S,, 35 1
Kagel, J. H . , 344
Hunag, P . L., 3 9 1
Kenney, W. D., 41 J
Humphreys, G. W . , 4 1 8
Kagan, J., 3 5 1
Koch, S., 4 1 8
Hugspcth, K . , 423
Humphrey, T., 80
Kennedy, S. H., 38 1
Kennell, J. H., 260
Hughes, S. L., 4 1 5
425 , 429
Kaysen, D., 4 1 7
Keay, K. A., 39 1 , 395
Keble, E. D., 4 1 4
Keesey, R . E . , 374, 382
Keffer, J. E., 364
Kehoe, P., 407
Kling, A. , 354, 4 1 5
4!9, 429
439
440
AUTHOR INDEX
AUTHOR INDEX
Leon, A . , 353
Leon, M., 4 1 0
Macon, J . , 372
Leonard, B. E . , 120
Lloyd, R. L, 408
Malenka, R . C . , 359
Malgrange, B . , 394
Levitan, I. B . , 355
Levy, M. L, 360
R., 426
Lewis, J. K., 4 1 0
Lewis, M., 23, 343
Lum, H., 4 ! 9
Luria, A.
Lick, C . , 400
R.,
80
Liebet, B., 96
Line, B. S., 4 1 6
Linkowski, P., 3 7 1
Mackay, A. V. P., 3 5 1
Mathis, C. E., 3 8 1
Mathur, A . , 374
Mayanagi, Y., 4 1 9
Mesibov, G. B., 4 1 2
Mayberg, H. S . , 423
Mesquitae, B . , 425
Maxson, S. C . , 347
Morato, S . , 381
McCall, R. B . , 4 1 4
Louis-Sylvestre, J . , 381
Lewin,
Long, S. J., 4 ! 0
Levenson, R. W., 3 5 1
Locke, S. E., 3 5 1
Morgan, C., 3 8 1
Morgan, H. D . , 359
Morgensthalen, J., 4 1 7
Morgese, I . , 205
Manguin, G.
R., 420
Margolis,
R.
I.,
372
L., 4 1 2
Mark, G. P . , 376
R.,
423
Michell, R. W., 4 1 9
408
Morgan, J. M., 4 1 6
Morgane, P . J . , 80, 352, 366, 369,
370, 37 1 , 372, 379
Miller, R. J., 3 8 1
Miller, T . C . , 425
Morris,
McLaughlin, P. J., 4 1 2
McNamara, J. 0 . , 359
McNaughton, B. L., 356, 394
Meaney, M. J., 4 1 3 , 4 1 4
Mock, F. 1 ., 396
Mizuki, Y ., 356
R.,
323, 343
Muarer, K., 96
Moffat, S . D., 4 1 0
Mulder, G., 96
Mogenson, G. J . , 421
441
442
AUTHOR
AUTHOR
INDEX
Pel!ow, S . , 392
Penfield, W., 428
Pacak,
Nottebohm, F., 4 0 1
Novak, M. A., 4 1 3
Novin, D., 1 8 6 , 382
Noyes, R., Jr., 222
425
Prete, F. R., 4 1 9
Preuss!er, D . W . , 372
Pribram, K. H., 424
Price, J. L., 360, 423
Price, T. R., 424
Priestly, J. V., 394
Prins, B., 394
Provine, R. R., 4 1 5
Prusky, G. T., 4 1 5
Przybeck, T . R . , 422
Qiao, J. T., 4 1 5
K.,
361
Quitkin, F. M., 4 1 2
40 l , 403-405
Pe!Jegrini, V ., 400
Quenzer, L. F., 1 1 9
Plato, 323
Pecina, S . , 385
Qu, D . , 383
Oostwegel, S . , 388
Potter, H . , 355
Petursson, H . , 395
Pascual-Leone, P. A . , 348
Pert, C. B . , 376
Peters, J. M., 367, 368
Nigh, C. K., 4 1 0
Nisbett, R. E . , 345, 4 1 8
Palmiter, R. D . , 384
411
Nelson, J . , 401
Perrett, D. L, 358
Page, M., 4 1 1
K., 425
Owens, M. J., 4 1 l
Nonnan, D. A., 4 1 8
Normansell, L, 299
INDEX
443
444
AUTHOR INDEX
AUTHOR INDEX
Richelson, E., 4 1 2
Richter, P., 428
Rickels, K., 393, 395
Riddle, M. A., 4 1 7
Ridley, M . , 399
Shepherd, G. M., 80
Schwartz, W. W., 3 8 1
Shepherd, J. K., 4 1 0
Schwartz-Giblin, S . , 400
Sherin, J . E . , 367
Sherrington, C., 8 1
Sherry, D . F . , 343
Schader, R. L, 395
Rush, A. J., 4 1 1
Schalling, M . , 383
Seirafi, R. L, 384
Sekino, H., 4 1 9
Self, D . W . , 365
Schneider, L H., 3 8 1
Smith, D. M., 3 8 1
Smith, E. 0 . , 299
Smith, G. P., 380
Smith, G. S. T., 393
Smith, J. B., 4 1 0
Smith, M . E., 357
Smith, P. K., 299, 4 1 3 , 414, 4 1 6
Smith, S . E . , 376
Smith, T., 344
Sorenson, J. A, 396
Simon, T., 4 1 6
Simonov, P. V . , 120
Sessarego, A., 3 5 1
Salans, L. B . , 3 8 1
Schouwink, G . , 369
Sexton, T . , 407
SaUanon-Moulin, M . , 372
Schneirla, T . C . , 349
Saitoh, 0 . , 427
Sloboda, J., 4 1 3
Slotnick, B. M., 352, 403, 405
Sahley, T. L., 4 1 2
Semple, W . E . , 421
Selseth, K. J., 4 1 4
Schmidt, D. E., 4 1 1
Schmidt, H. S., 367
Sacks, 0 . , 375
Saegert, S., 406
Schleidt, W. M . , 347
410, 4 13, 4 1 5 , 4 1 6
Skaggs, W. E., 356
Schipper, J., 3 9 1
Seck!, J. R., 40 I
410
Shepher, J., 406
Sarich, V ., 426
Sarfatti, S. E., 4 1 7
Sapolsky, R. M., 4 1 1
Sims, E. H. A., 3 8 1
445
446
AUTHOR INDEX
AUTHOR INDEX
Taylor, G. T., 4 1 6
Suarez, S., 3 5 1
Troost, J ., 369
Spyraki, C . , 385
Stahl, S. M., 393, 395
Stahle-Backdahl, M., 422
Staib, L. H., 427
Stanford, S. C., 366
Stanhope, R., 370
Stanley, B. G., 384, 386
Stanzel, K., 400
Stark-Adamec, C., 359, 393
Starr, L. B., 424
Steedman, J. M., 345, 357, 421
Stehle, J., 367, 368
Stein, E. A., 4 1 6
Stein, J . , 393
Stein, L., 373
Stein, M. A., 364
Stein, P. L, 347
Taylor, H. L., 3 8 1
Teitelbaum, P., 385
Tel!egan, A., 343, 347, 349, 375
Tennyson, V. M., 366
Terenius, L., 402, 4 1 2
Terpstra, J., 429
Terrace, H. S., 343, 346
Teskey, G. C., 359
Tessier-Lavigne, M., 365
Teuber, H. L., 372
Tharp, G., 390
Theelen, M., 40 I
Thiery, J. C., 404
Thompson, W. G., 4 1 2
Thompson, W. W . , 348
Thor, D. H., 405, 413-4!5
Thoren, P., 373
Thornton, J. E., 401
Thorpe, S. J., 389
Thorpy, M., 143
Tidey, J., 388
Sterns, F. R., 4 1 5
Tager-Flushberg, H., 4 1 2
Stewart, J . W . , 4 1 2
Stewart, M . A., 427
Stinus, L., 395
Stoll, C. J., 400
Stone, E., 358
Tomkins, S. S., 58
Tonegawa, S., 347
Tancer, M., 4 1 0
Strzelczuk, M . , 365
Studdert-Kennedy, M., 427
Studhof, C., 365
Stumpf, W. E., 400, 404
Stunkard, A. J., 186
Tan-Nguyen, L. T. L., 4 1 7
Tanne, D., 372
Towbin, K. E., 4 1 7
D., 378
Vaituzis, A. C., 4 1 7
Townsend, J . , 427
Traksman, L., 373
Tranque, P., 353
Traub, R. D., 422
Traylor, K L., 4 1 4
Treit, D . , 393
Vecera, S . P., 4 1 8
Vela, E. A., 399
Verbaten, M. N., 96
Verfaellie, M., 4 1 9
Veridiano, N . P., 398
Verleger, R., 96, 357
Vernino, S., 363
Vernon, P. A., 40
Vertes, R. P., 356, 367, 375
Vervaet, N., 386
Vetulani, J., 405
Vickers, J., 373
Videen, T. 0., 396
Vidnyanszky, Z., 362
Vigneri, R., 370
Vigue, L. C., 347
Vilberg, T., 405, 407, 408
423
Straube, E. R., 3S I
Torgersen, S . , 4 1 0
Turbes, C. C . , 421
Turner, R. A., 429
Talmadge, J., 4 1 7
Steppe!, J . , 358
4!6
Vauss, Y. C., 4 1 7
Tweney, R .
Thomposon, L. , 37 1
Thomas, E. M., 4 1 9
Turton, M. D . , 3 8 1
Sydall, S., 4 !6
Voigt, K. H. J., 4 1 3
Volke, V., 379
Vollrath, L., 367
Volrnan, S. F., 401
Wang, Z . X . , 409
D.
S., 381
Weijnen, F . G . , 403
Weiler, M. A., 379
Voogd, J., 80
Weinberg, U., 37 I
Voss, L, 370
Weintraub, S . , 355
447
""1
448
AUTHOR INDEX
White, B. D . , 384
White, D. J., 353
Whittington, M . A . , 422
Widerlov, E., 384
Wiegant, V. M., 4 1 6
Wightman,
R. M . , 362
Wing, L., 4 1 7
Wins, P . , 372
Winslow, J. T., 401, 405, 409, 4 1 0
Winson J . , 367
Wirsching, P ., 365
Wirtshafter, D., 364
Young, P. T . , 186
Wise,
R.
WittEngerstom, 1., 4 1 2
Wlakup, J. T., 4 1 7
Wolf, G . , 363
Zaccho, A . , 353
Zagon, E., 4 1 2
and arousal, 49
irritable, 193
Zagon, I. S . , 4 1 2
Zajonc,
Wolf, D. P., 4 1 3
R.
stimulus-bound, 193-196
Zhdanova, L V ., 368
Zhou, J. N., 398
Adrenal hormones
Zellner, D . , 406
Adjunctive behavior, 1 6 1
Zelazo, P., 4 1 4
Subject Index
gluconeogenesis, 137
territorial, 193
and benzodiazepines, 2 1 9
Alexithymia, 42
and rage, 1 8 8
Alkaloids, 103
Affective neuroscience
Alpha-blocking, 87, 95
A1pha-fetoprotein, 225, 232
aims of, 1 4
Altruism
bonding, 259
feelings as causes, 14
goals of, 301-302
Amphetamine
and ADHD, 320
345n. 4
and feeding, 1 7 1
central nucleus, 2 1 5
sexuality, 241
Anabolism, 98
Analogies, 1 7
Anandamide, 264, 36ln. 16
Angel dust, 3 J 5
449
450
SUBJECT INDEX
SUBJECT INDEX
Anger
behavior, 1 0
cognitive substrates, 1 9 1
and energy homeostasis, 166, 197
frustration aggression hypothesis, 1 66, 1 9 1 - 1 9 2
nature of, 7, 1 87-205
neurochemistries of, 190
personality trait, 149
restraint, 32
sources of, 45-46
species differences, 190
Angiotensin, 1 0 1 - 1 02, 186
Animal models
and emotions, 3, 1 0
as active agents, 6
cognitions, 30
decline in research, 6
hypnosis, 1 9 0
rights of, 6-7
Biogenic mnincs
Cartesian theatre, 3 l l , 3 1 2
Auras, 94
Autism
receptors, 41 6n. 6 1
apoptosis, 276
biological sources, 246, 249 262, 274
355n. 2
Bitterness, 182
Avarice, 301
Anthropomorphism, 9, 50-5 1 , 1 9 1
Boxing, 285
Bovet, D . , 109
Bradykinin, 1 0 1
Axons, 63-66
anatomy, 59-80
Baboons, 326
Aplysia
conditioned responses, 35-36
unconditioned responses, 36
Apomorphine, 1 62, 298
Apoptosis, 6 1 , 276
Appetitive
Axon hillock, 83
Barbiturates, 2 1 7 , 2 1 9
Baroreceptors, 198, 204
Basal ganglia, 40, 42, 67, 70, 177
Basic rest activity cycle, 129, 1 3 1
3-blockers
and aggression, 202
3-carbolines, 2 1 7
Beauty, 230
Bed nucleus of the stria terminalis, 227, 234, 267
B-endorphin
demasculinization, 238
discovery, 1 0 1
Artificial intelligence, 20
Attachment bonds
brain controls, 2.42, 244
and human personality, 277
insecurely attached, 265
securely attached, 265
timid, 265
morphology, 67
open systems, 6 1-62
operating systems, 20, 24--40
sections, 7 I , 75, 78
See also neuroanatomy, neurophysiology, and
neurochemistry
Brain rhythms
alpha, 87-89
beta, 87
theta, 87
Arteries, 68
Area postrema, 1 82
delta, 87
disinhibition, 2 1 0
Brain
mup of, 1 1 2
opiate effects, I 03
endocrinology, 344n. 2
genetics, 347n. 47
neuroscience, 6, 122, 332, 340
Biofeedback, 95
Carbamazepine, 2 1 2
and depression, 1 1 7
C<mnon, W., 56
gamma, 87
Breathing, 165-166
Broca's area, 333
Bulbocavernosus, 237
Bulimia, 1 1 7, 1 8 1 , !84
Bursting, 155-156
Buspirone, 206, 220
cFos
and aggression, 199
and imprinting, 4 1 0n. 56
and kindling, 358n. 53
attention, 1 07-109, 2 1 3
biochemistry, 99
choline acetyltransferasc, 99
cholinesterase, 99
and play, 294
Cingu1ate cortex
affective experience 34
and depression, 3 1 6
and panic, 267, 3 1 6
and play, 291
Caffeine, 130-131
social emotions, 6 1
Cajal, S . R., 65
Cannabis
and brain, 361n. 1 6
and play, 298
and separation distress, 264
451
452
SUBJECT INDEX
SUBJECT INDEX
Circle of Willis, 68
Circuits, 63
Circular explanations, 13
Classical conditioning
of Aplysia, 36
brain areas, 2 1 5
eye-blink, 75
feeling states, 6
and glutamate, 3 1 4
Cycles
circadian, 129
infradian, 129
ultradian, 129
neuroanatomy of, 3 1 3
primary-process, . 303, 3 1 0
and . quantum pqysics, 336
Cionidine, 268
and thalamus, 3 14
Dale's law, 1 1 1
Distress, 1 8 2
DNA
Darwin's finches, 29
nucleotidcs, 98
neuroscience, 20
nurturance, 249
and play, 294
reproductive, 228
circular, l 3
of emotions, 47-49, 150
role of, 330
D6jll vu, 260
Delinquency, 202
science, 5
Cormac, A., 90
skills, 4
Coropora quadrigmenia, 77
Delusional
styles, 2 1
Corpus callosum
Companionship, 255
Cortex
Dependence, 2 1 9
Deprenyl, 245, 298
hand representation, 1 6
Depression
plasticity, 1 6
fear, 2 1 5-217
speech, 332-333
responses, 36
taste aversions, 1 7 1 , 182
Confirmation bias, 378n. 83
Connectivities
of aggression, 197
anterograde, 63-65, 197
retrograde, 63-65, 197
Consciousness
affective, 303
Cruising, 239
evolution of, 34
Culture, 14, 5 1 , 188, 205, 245, 247, 259, 283, 301, 306, 329
interest, 150
map, 107, 1 10
mesocortical system, 54
mesolimbic system, 54
neuronal firing, 1 8 0
frontal cortex, 95
Determinism, 348n. 50
Dopamine
Crocodiles, 250
Cartesian theatre, 3 1 1, 3 1 2
in children, 35 1 n. 27
cingulate cortex, 3 1 6
cholinergic influences, 3 1 4
Conditioned
incentives, 155-156
multimodal association, 3 1 0
hierarchies, 1 8 8
Dendrites, 63-66
Dominance
Dollard, J., 1 9 1
Dolphins, 329, 334, 353n. 1 9
Definitions
Contracts, 3 1 9
Defensive burying, 2 1 1
revolution, 1 0
Cognitive
neglect o f emotions, 20
Darwin, C, 1 1 , 1 2 1 , 327
Dishabituation, 35
Displacement behavior, 1 6 1
Contact comfort
Discrimination studies, 1 5 3
Distress vocalizations
Cognitions
evolution, 328
Digital computers, 20
Cockroaches, 37
of Aplysia, 36
Diazepam, 274
Cytokines, 182
motorvs. sensory, 3 1 3
and sexuality, 3B
Diabetes, 6, 173, 1 8 3
Diazepam binding inhibitor, 218, 394n. 7 0
and personality, 56
DSM-IV, 207
Dynorphins, 1 0 1 , 1 8 1
II
453
454
SUBJECT I NDEX
SUBJECT INDEX
executive systems, 49
Ecdysis, 25
facial analysis, 46
Echidna, 6 1 , 370n. 69
EEG
and affect, 3 1 7
beta, 88, 3 1 3
ontogeny of, 55
physiology of, 46
desynchronization, 87
discovery of, 87
pseudoaffective, 7
gamma, 3 1 3, 422n. 57
i n society, 320-323
as psychological measure, 85
species differences, 5
rhythms, 3 1 3
triggers, 190
types of responses, 1 4
visce!'al sensations, 57
Empathy, 262
and emotions, 94
and fear, 2 1 3
freezing, 214
and quiet-biting attack, 198-199
Eltoprazine
energostatic, 175
aggression, 202
and play, 286, 414n. 28
glucostatic, 175
lipostatic, 175
Embarrassment, 27, 30 l
Emotion theories
categorical, 44, 76
classification of, 4 1
regulation, 164-179
componential, 45, 76
social constructivist, 44, 76
Emotional controls
brain circuits, 17, 7 1 , 75
cerebral asymmetries, 3 1 7
and cognitions, 3 1 8
command circuits, 3 1 0
conditioning of, 3 1 7
development, 26
distress, 45, 250
BEG arousal, 3 1 7
feelings, 3
and mood, 3 1 7
operating systems, 3, 24
pain, 261
plasticity, 27
power of, 42
and rTMS, 3 1 7
varieties of, 4 1
Emotions
autonomic responses, 56-57
cognitive type, 301
conventions, 5 1
definitions, 47-49
and development, 26
dimensional attributes, 46
thermostatic, 175
Enkephalins, l 0 I
Enteric nervous system, 1 1 9
Epigenesis, 16, 56, 123, 3 1 1 , 350n. 24 , 420nn. 26, 30
Epilepsy, 70, 88, 94-95, 212, 337, 352n. 7, 357n. 33
Erections, 227, 241, 257, 405n. 66
Erlanger and Gasser, 83
Evoked potentials, 88
Evolution
of anger, 190
of dreaming, 134-135
Feeding
and amino acids, 1 8 0
of humans, 325-330
behavior, 1 68- I 69
of learning, 55
selection, 12
biogenic amines, 1 8 1
effect of poisons, 1 8 1
and fear, 169
gastric factors, 185
long-tenn satiety, 179- \ 8 1 , 185
minerals and vitamins, 1 8 1
neuropeptides, I 79, 1 8 1
NPY antagonists and, 1 8 1
nutrient effects, 170
opioids, 184-185
palatability effects, 1 7 1 , 183
and pleasure, 1 7 1 , 182-185
Feelings
acetylcholine, 227
of anger, 1 87-205
Facial expressions
cerebral readout, 33
behavior, 1 0
childhood, 221
contextual cues and, 22
Flumazenil, 2 1 7 , 2 1 9
!MRI, 29
Folk psychology, 12, 32, 302, 306
Foot shock, 2 1 0
and defecation, 2 1 1
Fos, 28, 93
DB!, 206
Fear-potentiated startle, 33
and reward, I 97
303
455
456
SUBJECT INDEX
SUBJECT INDEX
Frustration
and aggression, 166, 190, 192
feelings of, 192
Guillemin, R., 10 l
Guilt, 27, 301
Gulf War syndrome, 27
Habituation, 35
Hallucinations, 142
Happiness, 1 3 , 45-46, 224, 303, 308
Galilee, 420n. 34
Hate, 1 9 1 , 3 0 1
Galvani, 83
Health
and consciousness, 3 1 5
and fear, 2 1 7
Hedonics, 1 8 1-185
inhibition, 49
Hemiplegia, 308
Hemispheric specializations
communciation, 307
synthesis, 104
Gambling, 1 1 8
Heritability, 1 6
Heterostasis, 164
Genetic influences
Hierarchical organization
on behavior, I I
on mental life, 97
of aggression, 196
in brain, 28, 77
obesity, 182-183
Hilarity, 290
Hippocampus
receptor diversity, 99
anatomy, 7 1-72
Gibbons, 227
and fear, 2 1 7
Glia, 63
Glucocorticoids, 2 1 1
histology, 63
Glutamate
6-Hydroxydopamine, 296
Hyenas, 189, 229, 234
aggression, 193-199
anatomy, 70-71
and erections, 227
fear, 2 1 3 , 208
feeding, 174-180
interstitial nuclei, 235
maternal behavior, 253-254
nutrient infusions, 169
osmoreceptors, 167
self-stimulation, 152-160
and separation distress, 268
sexuality, 227, 235-237, 242
thermoreceptors, 167
Hypovolemia, 1 8 6
conditioned fears, 2 1 7
and consciousness, 3 1 4
spatial maps, 22
Hoarding, 328
Hobbes, T., 287
and fear, 2 1 7
Hodgkin, A., 84
Homeostasis
MSG, 40
energy, 182, 1 8 3
Homer, 263
Hormones
feeding, 174
metamorphosis, 25, 28
and sleep, !37
Guevedoces, 233
and Lorenz, 1 2 1
measured with 2-DG, 90
and opioids, 272
and oxytocin, 272
fn vivo voltametry, 1 1 5
Homogenic, 344n. 22
Homologies, 9, 17, 60, 282, 304, 325
stress, 25, 1 1 9
Hounsfield, 90
Hubel, D., 86
Humanism, 2 1
Human
nature, 1 5 , 1 8 , 45, 332
psyche, 329
Humor
in play, 281
in rats, 18
Insulin
cephalic phase, 174
discovery, 1 0 1
fat deposition, 174
Imprinting
exploration, 52
explanations of, 1 0
o f fear, 207, 2 1 1
conditioning of, 1 3
Incentives
defined, 168
and dopamine, 156
Inclusive fitness, 228
lndoleamines, 1 1 1
Induction, 29
in animals, 332
in cats, 38
457
458
SUBJECT INDEX
Language (continued)
SUBJECT INDEX
Lordosis, 230, 239, 240
Loyalty, 301
of emotions, 5 1-52
and fear, 2 1 6
Laughing
Masculinization, 225
Materialism, 2 1
Maternal behavior
BNST, 253
evolutionary sources, 250
experience effects, 252-253
experience-induced, 257
neural circuitry, 253-254
olfaction, 252, 204n. 28
in disease, 288
Learning
s;
birdsong, 244
Marriage, 226-227
and aggression, 1 9 5
based on feelings,
MachiaveUianism, 322
14
social, 23 1 , 256-257
prosody, 334
and SEEKING, 145
semantic, 74
in autism, 277
circadian rhythms 1 3 7
and sleep, 1 2 9 - 1 3 1
synthesis, 129- 1 3 1
Memory
declarative, 74
and dreams, 129
and emotional arousal, 55
evolutionarily prepared, 139, 1 86
and long-term potentiation, 95
mood congruent, 3 1 0 , 424n. 80
olfactory, 404n. 27
and self-stimulation, 55, 374n. 1 6
neurochemistries, 260
social attraction, 406n. 86
s"Oeial policies, 260
unconsious mediation, 259
Mesencephalic locomotor region, 3 1 2
Mesotocin, 230
Metabolic information, 177
Metaphors in science, 33 1
Methylphenidate, 297, 320
Methysergide, 298
Micronutrients, 1 8 1
Mimicry, 361n. 1 0
Mind
and brain dynamics, 336
computer analogy, 20
Naloxone, 103
and gregariousness, 272
grooming, 272
Naltrexone
effects on EEG, 89
gregariousness, 272
and imprinting, 273
and pleasure, 1 84
treatment of autism, 89, 277
Narcolepsy, 369n. 62
relations to brain, 59
Netrins, 1 14
Neural firing
Mind-body problem
Mirrors, 268-269
Neuroectoderm, 85
Money, 3 1 9
Neuromodulators, 34
Neuroethology, 5, 122
Neurophysiology, 8 1 -96
Neurotransmitters, 97- 1 1 9
Neuronal growth factors, 1 14, 28 1 , 3 1 1 , 334
Neuron doctrine, 59, 64
Neurons
induction, 3 1 8
ion channels, 84
nodes of Ranvier, 84
Mother-offspring play, 2 1 8
Mothers, 262, 28 1 , 283, 397n. 7
Motivations, distinguished from emotions,
228
myelin, 84
resting membrane potential, 84
Neuropeptide Y, ! 0 1 , I 17, 1 8 1
Mounting, 239
Music
Neurotensin, 1 0 1 , 156
Neurosubjectivity, 29
459
460
SUBJECT INDEX
SUBJECT INDEX
Ovulation, 240
Oxytocin
and aggression, 20 I , 257
behavioral integration, 77
Norepinephrine
erections, 257
arousal, 49, 1 1 0, 2 1 3
attention, 133, 364n. 4 1
evolution of, 1 1 0
map of, 107
synthesis, 105, 1 10
NPY anatgonists. See feeding
Nuclei. See Neuroanatomy
Nurturance
circuits for, 54
in crocodiles, 250
relations to sex systems, 227, 246
sex differences in, 249
and social loss, 263
and society, 321
and stress, 238
Obesity, 165, 169, 174-179, 384n. 68
ob/.Qb mice, 174, 178
discovery of, 1 0 1 - 1 02
functions of, 250
in female sexuality, 241-243
and gregariousness, 271
in male sexuality, 241-243
map of 1 1 2
and attention, 3 1 3
emotional energies, 3 I 7
and the SELF, 3 1 2
Pain
and hippocampus, 95
Play (rough-and-tumble)
sources, 5 I , 166
PANIC circuits
anatomy of, 267
cats, 267
chickens, 267
description, 5 1 , 54
depriVation, 282
overview, 261
grooming, 271
primates, 267
receptor map, 1 1 6
Papez circuit, 57
fighting, 189
Paracrine, 68
playfulness, 250
Periaqueductal gray
Oxygen, 165
as instinct, 287
211
in mammals, 282
Pavolovian conditioning, 1 9
Preganancy
461
462
SUBJECT INDEX
Pride, 301
Prolactin
discovery, 1 0 1
during gestation, 248, 250-25 1
SUBJECT INDEX
Rapid transcranial magnetic stimulation
(r!'MS)
and aggression, 205
and depression, 95, 204, 3 1 7
Roosters
castration, 228
and testosterone, 228
rTMS. See rapid transcranial magnetic stimulation
Saccharin, 184
Sadness, 7, 1 3 , 288, 303
Sakmann, B., 85
Schally, A., 1 0 1
Reinforcement
Schedules o f reinforcement
Prosody, 334
Proteins
postranslational processing, 98
translation, 98
piece work, 22
variable-ratio schedules, 22
Protooncogenes, 93
Proximal causes, 14
Psychiatric disorders
anxieties, 2 12
as process, 1 2 , 38
Religion, 425n. 94
REM deprivation
as discipline 5, 15, 40
medicines, 1 1 7
antidepressants, 138, 1 4 1
atonia, 1 2 9
schizophrenia, 9 1
and cortisol, 1 3 7
Psychobehavioral controls, 25
Psychology
and depression, 1 4 0
effects of stress, 128
and behaviorism, 23
and emotionality, 1 3 9
neglect of emotions, 20
372n. 99
personality, 142
RAGE system
amygdala, 187
brain circuits, 1 9 \ - 1 9 9
glutamate, 148
glycine, 1 1 3
and L-dopa, ! 5 0
SEEKING system, 5 3 , ! 4 5 , !62
and self-stimulation, 157, 160
septal area, 227
stimulants, 374n. 20
types of, 35 ln. 29
School phobia, 274
SCN, 130
SDN-POA, 235
Secure base
and play, 281
neurochemical nature of, 266, 403n. 1 3
SEEKING circuits
429n. 14
SELF
RNA
drive-decay theory, I S
glutamate, 1 47
heritability of, 40
and homeostasic imbalances, 1 67
learning, 157-161
paradoxes of, 152
psychiatric disorders, 148
reinforcement, 146-148
and schizophrenia, 1 62-163, 378n. 82,
379n. 103
and SEEKING system, 53
as unitary process, 152-153
Sensitization
behavioral, 35
and fear, 207
human implications, 258
matemal, 238
psychostimulant, 1 62, 3 19
sexual eagerness, 242
in young animals, 258
Sentic cycles, 89
Separation anxiety
and amines, 276
380n. I I
Representations, 3 1
relations t o LSD, 1 27
theta during, 129
200 mapping, 9 J
inhibiton by RAGE, 1 9 1
Raphe
and frustration, 1 9 I
RAMs, 20
protein synthesis, 3 7 1
Rhinencephalon, 7 1
hypothalamus, 1 87
cerebellum, 203
Schizophrenia
and anger, 1 9 1
309
Racoons, 1 1
token economies, 22
serotonin, 1 4 1
Self-stimulation
antipsychotics, 148
nurturance, 248
Prosapagnosia, 307
Selfishness, 278
Self-reflection, 34
Self-representation, 309
behavioral coherence, 3 1 1
body representations, 3 1 3
calls, 261
effect of mirrors, 268
effect of music, 270
sleep, 262
Septal area
Serotonin
PAG, 312-314
periventricular gray, 31 I
superior col!iculi, 3 1 2
Self-fertilization, 229
Self-injurious behavior, 277
IlI
463
464
SUBJECT INDEX
SUBJECT INDEX
Set-point, 164
Sex differences
in aggression, 230
oxytocin, 226
in play, 230, 2 8 1
vasopressin, 226
Sexual behavior
bonding, 242, 255
contact and aggression, 257
evolution of, 223
preoptic area, 226
varieties of, 229-230
Sexual desire
galanin, 244
Social attachments
attractiveness and play, 294
bonds, 227, 246, 2 8 1
brain systems for, 254
conventional rewards, 262
neurochemistries of, 254
and opiate addiction, 261
in females, 244
Sexual differentiation
dihydrotestosterone, 232-233
estrogen, 232-233
genetic effects, 231-233
hormonal effects, 232-236
organizational effects, 23 1, 234
XYY males, 234
Sexual motivation
Sherrington, C., 83
Sign-stimuli, 3 1 , 1 2 1
Single-gene deletions, 39
Skinner, B. F., 1 1 , 1 2 1
Sleep
in echidna, 135
EEG indicators, 125, 128, 132
effects of melatonin, 129- 1 3 1
growth hormone, 136
and sChizophrenia, 127
and survival, 135-136
Sleep deprivation
and biogenic amines, 133-134,
142
and growth, \36
wagging, 271
Taxonomies
of aggression, 193-194
of emotions, 4 1-55, 349nn. 4, 12
of fear, 2 1 2-213
Strange attracrors, 3
Stress
and adrenal, 1 19
and gender identitiy, 237-238
higher brain functions, 3 1 5
neurotoxic effects, 4 1 1n. 78
of play, 283
Tears, 283
Temperament
and oxytocin receptors, 272
in voles, 272
stimulus-bound behaviors, 198, 388n. 27
Temporal lobes
emotional circuits, 3 1 6
and experiences, 337
Testis-determining factor, 232
Testosterone
and anger, 198, 200
aromatization, 225
female libido, 244
in hyenas, 189
functions of, 32
homeostatic imbalances, 1 8 t
instrumental behavior, 34
nature of, 14
detachment, 267
pinching, 1 6 1
SEEKiNG, 153-155
measurement of, 34
deprivation, 282
functions of, 25
attraction, 406n. 86
Tails
masculinization, 238
and play, 286, 4 l 4n. 27
power-urges, 259
and social dominance, 245
and vasopressin, 200
and vasotocin, 230
dominance, 229
power of, 42
homeostasis, 276
of thirst, 165
and values, 55
Thirst
in brain, 261-279
Stalking, 194
Subjectivity
difficulties in study of, 6, 9
as distinguished from objectivity, 49
nature of, 300-323
objectification of, 45
angiotensin, 186
anguish from, 165
drinking pleasure, 182
hypothalmic ESB, 153
organum vasculosum, 185
regulatory response, 32
visualization of, 29
Submission, 196
Substance P
discovery, 1 0 1
Thyroxine, 177
Substantia nigra, 70
Subtractive autoradiography, 1 1 5
Suckling, 251-252
Suffocation alarm response, 166, 2t2, 275
Suicide, 142, 390n. 87
Superior colliculi, 7 1 , 75, 77, 307
Supplementary motor area, 86, 339
in rats, 288
Tinbergen, N., 1 2 1
Surprise, 46
465
466
SUBJECT
I NDE,
Tools of consciousness,
Touch
Traits, 149
Transsexual, 234
TRH, 1 0 ! -102
Trk receptors, 1 14
Trinucleotide repeats, 40
Triune brain
!i.mbic system, 70
neomammalian brain, 7 1
overview of, 42-43, 62, 70--72
pathways, 72, 75
reptilian brain, 70
Trk receptors, 1 14
Trojan War, 263
Turtles, 250
Tyrosine hydroxylase, I 05
. --
p<:::l t::fCOCC,
256
in turtles, 250
Ventral tegmental area, 70, 145, 156, 167, 253, 265
Ventricles, 68
Ventromedial hypothalamus
in aggression, 79, 195, 197
effects of GTG, 179
insulin sensitivity, 179
local energy stores, 179-180
metabolic information, 179-180
nutrient infusions, 179
Waggle dance, 1 2 1
Waking
EEG indicators, 1 3 1--133
and norepinephrine, 1 3 3
anatomy, 69
Wiesel, T., 86
Vagus, 170, ! 7 1
Valium. See benzodiazepines
Values. See Biological values
Vasopressin
Xenophobia, 301
Xylocaine, 290
Yawning, 4 ! 4n. 28
map of, 1 1 2
Yerkes-Dodson law, I J O
Yohimbine
and anxiety, 2 1 8
Zoo animals
Binti's nurturance, 259
taming of, 2 1 9
Zoophobia, 6
,..