Table Of ContentEMOTION
Theory, Research, and Experience
EDITED BY
Robert Plutchik Henry Kellerman
Albert Einstein College of Medicine Postgraduate Center for Mental Health
Bronx, New York New York, New York
Volume 1: Theories of Emotion
Volume 2: Emotions in Early Development
Volume 3: Biological Foundations of Emotion
EMOTION
Theory, Research, and Experience
Volume 3
Biological Foundations of Emotion
Edited by
Robert Plutchik
Albert Einstein College of Medicine
Bronx, New York
Henry Kellerman
Postgraduate Center for Mental Health
New York, New York
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LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA
Main entry under title:
Biological foundations of emotion.
(Emotion: theory, research, and experience ; v. 3)
Includes bibliographies and index.
1. Emotions —Physiological aspects. 2. Psychology,
Physiological. I. Plutchik, Robert. II. Kellerman,
Henry. III. Series.
BF561.E48 vol. 3 [BF531] 152.4 s [152.4] 85-13471
ISBN 0-12-558703-1 (alk. paper)
ISBN 0-12-531953-3 (paperback)
PRINTED IN THE UNITED STATES OF AMERICA
86 87 88 89 987654321
CONTRIBUTORS
Numbers in parentheses indicate the pages on which the authors' contributions begin.
JOHN P. AGGLETON (281), Department of Psychology, University of Durham,
Durham DH1 3LE, England
FRANK R. ERVIN (145), Department of Psychiatry, McGill University,
Montreal, Quebec H3A 1A1, Canada
ELZBIETA FONBERG (301), Department of Neurophysiology, Limbic System
Laboratory, Nencki Institute of Experimental Biology, 02-093 Warsaw,
Poland
JOHN L. FULLER (199), Department of Psychology, State University of New
York at Binghamton, Binghamton, New York 13901
ROBERT G. HEATH (3), Department of Psychiatry and Neurology, Tulane
University School of Medicine, New Orleans, Louisiana 70112
JAMES P. HENRY (37), Department of Psychiatry, Loma Linda University
School of Medicine, Loma Linda, California 92350
JAMES G. HERNDON (265), Division of Neurobiology, Yerkes Regional
Primate Research Center, Emory University, Atlanta, Georgia 30322
ROY KING (363), Department of Psychiatry and Behavioral Sciences, Stanford
University Medical Center, Stanford, California 94305
xin
XIV Contributors
ARTHUR S. KLING (237), Veterans Administration Medical Center, Sepulveda,
and Department of Psychiatry, UCLA School of Medicine, Los
Angeles, California 91343
PAUL D. MACLEAN (61), Laboratory of Brain Evolution and Behavior,
National Institute of Mental Health, Bethesda, Maryland 20205
JOHN MARTIN (145), Department of Psychology, McGill University, Montreal,
Quebec H3A 1B1, Canada
MORTIMER MISHKIN (281), Laboratory of Neuropsychology, National
Institute of Mental Health, Bethesda, Maryland 20205
BRUCE E. MORTON (381), Department of Biochemistry and Biophysics, John
A. Burns School of Medicine, University of Hawaii at Manoa, Honolulu,
Hawaii 96822
KENNETH E. MOYER (219), Department of Psychology, Carnegie-Mellon
University, Pittsburgh, Pennsylvania 15213
JAAK PANKSEPP (91), Department of Psychology, Bowling Green State
University, Bowling Green, Ohio 43403
ADRIAN A. PERACHIO (265), Departments of Otolaryngology, and Physiology
and Biophysics, University of Texas Medical Branch, Galveston, Texas
77550
DETLEV PLOOG (173), Max Planck Institute for Psychiatry, Clinical Institute
and Department of Primate Behavior, Munich, Federal Republic of
Germany
EDMUND T. ROLLS (125), Department of Experimental Psychology, Oxford
University, Oxford OX1 3UD, England
HERMAN M. VAN PRAAG (335), Department of Psychiatry, Albert Einstein
College of Medicine, Montefiore Medical Center, Bronx, New York
10461
PREFACE
This is the third volume in a series on emotion, entitled Emotions: Theory,
Research, and Experience. The first volume, Theories of Emotion, placed the
concept of emotion in a historical context. Some of the contributors to that
volume represented modern derivatives of the evolutionary concepts of Charles
Darwin that emphasized the expressive aspects of emotion. From this point
of view, emotional displays are considered to be forms of communication
designed to increase the likelihood of survival. Other contributors reflected
the psychophysiological tradition that was originated largely by William James
and Walter Cannon. In this context, the theories attempted to explain the
relations between physiological or neural events and the subjective feeling states
called emotions. The dynamic theories of émotif are largely derivative from
the conceptions of Sigmund Freud. Implicit in these theories is the idea that
emotions are part of a biological heritage, but that they can undergo a large
variety of transformations in the course of an individual's life. From this
viewpoint, subjective feelings reflect only some aspects of emotion. Other
aspects are revealed by personality traits and ego-defenses. By examining these
various theories and approaches to emotion, the beginning of a synthesis of
the field could be discerned.
The second volume, Emotions in Early Development, was concerned with
emotion as seen or inferred during neonatal and infant development in both
animals and humans. Different contributions were concerned with a variety
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XVI Preface
of important theoretical issues. For example, how it it possible to infer the
existence of emotions in infants? What is the relation between cognitive
development in the Piagetian sense and emotional development? How are
emotions and personality related? What is the role of parent-child interactions
in the appearance and development of emotions?
The contributions revealed that emotions are a central aspect of neonatal
experience in all organisms, and they serve subtle communication and
biological regulatory functions. For example, the view is developed that feeling
states are elicited by the expressions of others and also act as regulators of
behavior. The point is made that cognitive development is generally inferred
on the basis of emotional indicators such as crying and smiling, and that such
reactions signal advances in the development of concepts about objects, spatial
relations, causality, and similarity. Attachment behavior is recognized as
having homeostatic, regulatory functions.
The present volume, Biological Foundations of Emotion, is designed to allow
a detailed consideration of the relations between brain structure, functions,
and emotions. Contributors to this volume represent internationally known
researchers in this field. These authors present their experimental work and
theoretical models and focus on integration of ideas. All authors were asked
to address one or more of certain key issues in their chapters. These include
whether there are structures, circuits, or biochemical events in the brain that
control emotional expressions or experience; what effects lesions and electrical
stimuation have on emotions; and what role genetics plays in the expression
of emotion.
Although it is obvious that the organism functions as a unit, different
authors focus on different aspects of functioning. Some direct attention to
certain structures in the brain that have been shown to be related to emotions,
such as the limbic system in general, or the amygdala in particular. Others
focus attention on neurotransmitters that occur in the brain that influence
emotions, particularly depression. Several direct their attention to anger or
aggression, an emotion of particularly great concern to humans, and attempt
to identify its biological basis. A few authors take an evolutionary approach
and look at emotions from the point of view of genetics and ethology. Of
course, some overlap of these themes and issues is inevitable and, indeed,
is desired in the different chapters.
The level of presentation also varies but is accessible primarily to graduate
students. For all those interested in the biological bases of emotions, this book
reflects the state of the art.
INTRODUCTION
The brain is the central integrating structure of the body. As such it provides
the coordinating substrate for the complex chain of events that we call
emotions. This is obvious. What is not so obvious is exactly how the integration
process works. To what extent is there differentiation of structure and
function? To what extent is the process of coordination electrical or chemical?
To what extent are emotions determined by learning or by schemata built deep
within our genes?
The eminent contributors to this volume, Biological Foundations of Emotion,
examine these and other related questions in depth. They approach these issues
sometimes from the point of view of particular brain structures, sometimes
from the point of view of brain chemistry and the electrical manifestation
of brain function, and sometimes from the viewpoint of genetics. In every
case, these indices of brain structure and function are related to behavior.
The approaches and themes of the authors may be organized in the
following way. Six contributors present general models of brain functioning
(Part I, this volume). Two examine ethological and evolutionary factors in
emotion. Three others present different but overlapping brain models of
aggression. Two focus their attention on a particularly important structure
in emotions, the amygdala. The final three authors examine the role of
xvii
xviii Introduction
biochemistry in understanding emotions. The following remarks present an
overview of these contributions.
GENERAL MODELS OF BRAIN FUNCTIONING
The first chapter by Heath provides evidence that the conventional concept
of a limbic system underlying all emotions is not adequate. Not only do
structures within the limbic lobe influence emotions, but so too do other brain
structures. Electrical studies reveal synchronized activity in many parts of the
brain that are associated with the behavioral manifestations of emotion.
Evidence is presented for both an aversive system and a pleasure system in
humans based on self-reports of humans and self-stimulation studies in
animals. Reciprocal relations between pleasure and pain were substantiated.
Similarly, activation of the pleasure system had a strong anticonvulsant effect
in cases of epilepsy. Stimulus-bound reactions of fear and rage could be
produced by electrical stimulation. It was found that some of the regions
important for emotions are also involved in memory. Heath concludes that
the concept of a limbic system is questionable since sites within the limbic
lobe are not the sole neural sites, or even the principal ones, subserving
emotion.
Chapter 2 by Henry cites the universal facial expressions of emotion, the
rituals and threat displays in animals and humans, and the consistent infant
patterns of emotion, and interprets them in terms of inherited physiological
mechanisms, or "archetypes." He identifies the structures in the limbic system
and the brainstem that are triggered by hormones and suggests that both
endorphins and catecholamines are involved. He also provides evidence that
different patterns of neuroendocrine response occur in the emotions of anger,
fear, elation, and depression. Each of these emotions has neocortical, limbic,
and brainstem components. Adrenocortical and pituitary hormones are also
involved in triggering the differential patterns seen in different emotions.
A unique approach to the problem of brain-emotion interrelations is
presented by MacLean in Chapter 3. He reviews the reports in the world
literature dealing with the subjective feelings associated with psychomotor
epilepsy. Six major types of emotions have been described, which are the
following: feelings of affection, pleasure, desire, anger, fear, and sadness. The
clinical data suggest that such feelings have a genetic basis since patients reveal
the same types of feelings regardless of race or social background. The parts
of the brain most involved in psychomotor epilepsy are the amygdala, the
hippocampus, and the thalamocingulate part of the limbic system. These
Introduction XIX
connections suggest both a limited number of basic emotions and the probable
structures related to them.
Chapter 4 by Panksepp proposes that brain systems can be identified for
four basic emotive systems; namely, fear, rage, separation-distress, and
investigation. These systems are conceptualized as sensory-motor command
systems that are genetically based and that are designed to respond to stimuli
arising from major life-challenging situations such as pain, threat, restraint,
and loss. These circuits organize behavior by activating or inhibiting motor
subroutines and hormonal changes that are adaptive. The action of emotive
circuits can be conditioned to environmental stimuli, can be reinforced or
inhibited, and can provide feedback to brain mechanisms associated with
cognitions.
Brain structures most probably involved with the four command systems
are the following: basal ganglia structures (investigation), amygdala and
temporal lobe (fear and rage), and the cingulate gyrus (separation-distress).
However, since memory and cognition are related to emotion, other brain
structures also are involved. Panksepp's chapter illustrates these concepts
through a detailed analysis of the investigative-expectancy system.
In contrast to the model presented in the previous chapter, Rolls, in Chapter
5, focuses on the role of reinforcing stimuli in producing emotions. He believes
that studies of primates have provided strong support for the role of amygdala,
prefrontal cortex, and hypothalamus in the learning of emotional responses.
The research cited is of two types: effects of lesions of these brain structures,
and the nature of the electrical signals obtained from single neurons in these
structures during stimulus-reinforcement associations. Lesions of the
amygdala, for example, apparently change the capacity of the organism to
recognize and respond to reinforcing stimuli. Recordings from single neurons
also support the idea that the amygdala responds to the aversive or reinforcing
properties of stimuli.
Of great interest is the observation that certain neurons of the amygdala
respond primarily to faces, presumably a direct reflection of the importance
of facial displays in primate behavior. Finally, Rolls describes a conception
of reinforcement-punishment contingencies that might account for the many
labels that exist in our languages for describing emotions.
The final chapter on general models of brain function (Chapter 6) examines
the neurophysiological bases of the primary emotions. Ervin and Martin review
evidence designed to show that there are relatively discrete neuronal assemblies
in the brain that, when activated, give rise to emotions. Based on the
psychoevolutionary model proposed by Plutchik, which postulates eight basic
affects, Ervin and Martin provide evidence for brain structures involved in
the emotions of anger, fear, joy, sadness, acceptance, disgust, surprise, and
