The Integrative Neurobiology of Affiliation

631 Pages·1997·37.81 MB·English

by  Carol Sue Carter

ANNALS of THE NEW YORK
ACADEMY OP SCIENCES
The Integrative Neurobiology of Affiliation
Volume 807 Pages xiii-xviii, 1-612
January 1997
@ The New York Academy of Sciences
cr.html(3/5/2015 5:42:03 PM]
Series: Annals of the New York Academy of Sciences (Book 807)
Hardcover: 614 pages
Publisher: New York Academy of Sciences (December 1996)
Language: English
ISBN-10: 1573310581
ISBN-13: 978-1573310581
Contents
Introduction
INTRODUCTION (pages xiii–xviii)
C. SUE CARTER, I. IZJA LEDERHENDLER and BRIAN KIRKPATRICK
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51909.x
Part 1. Ultimate Causation
Species Diversity and the Evolution of Behavioral Controlling Mechanisms (pages
1–21)
D. CREWS
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51910.x
Ecological Constraints and the Evolution of Hormone-Behavior Interrelationships
(pages 22–41)
JOHN C. WINGFIELD, JERRY JACOBS and NIGELLA HILLGARTH
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51911.x
Evolutionary Perspectives on Primate Mating Systems and Behavior (pages 42–
61)
ALAN F. DIXSON
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51912.x
Emotion: An Evolutionary By-Product of the Neural Regulation of the Autonomic
Nervous System (pages 62–77)
STEPHEN W. PORGES
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51913.x
Part 2. Proximate Causation
Brain Systems for the Mediation of Social Separation-Distress and Social-Reward
Evolutionary Antecedents and Neuropeptide Intermediaries (pages 78–100)
JAAK PANKSEPP, ERIC NELSON and MARNI BEKKEDAL
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51914.x
Neuroanatomical Circuitry for Mammalian Maternal Behavior (pages 101–125)
MICHAEL NUMAN and TEIGE P. SHEEHAN
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51915.x
Oxytocin Control of Maternal Behavior Regulation by Sex Steroids and Offspring
Stimuli (pages 126–145)
CORT A. PEDERSEN
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51916.x
Physiological and Endocrine Effects of Social Contact (pages 146–163)
KERSTIN UVNÄS-MOBERG
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51917.x
Integrative Functions of Lactational Hormones in Social Behavior and Stress
Management (pages 164–174)
C. SUE CARTER and MARGARET ALTEMUS
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51918.x
Social Facilitation, Affiliation, and Dominance in the Social Life of Spotted Hyenas
(pages 175–184)
STEPHEN E. GLICKMAN, CYNTHIA J. ZABEL, SONJA I. YOERG, MARY L.
WELDELE, CHRISTINE M. DREA and LAURENCE G. FRANK
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51919.x
Hormonal Modulation of Sexual Behavior and Affiliation in Rhesus Monkeys
(pages 185–202)
KIM WALLEN and PAMELA L. TANNENBAUM
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51920.x
Attachment Relationships in New World Primates (pages 203–209)
SALLY P. MENDOZA and WILLIAM A. MASON
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51921.x
Psychobiological Consequences of Social Relationships (pages 210–218)
S. LEVINE, D. M. LYONS and A. F. SCHATZBERG
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51922.x
Specific Neuroendocrine Mechanisms Not Involving Generalized Stress Mediate
Social Regulation of Female Reproduction in Cooperatively Breeding Marmoset
Monkeys (pages 219–238)
DAVID H. ABBOTT, WENDY SALTZMAN, NANCY J. SCHULTZ-DARKEN and TESSA
E. SMITH
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51923.x
Mating-Induced c-fos Expression Patterns Complement and Supplement
Observations after Lesions in the Male Syrian Hamster Brain (pages 239–259)
SARAH WINANS NEWMAN, DAVID B. PARFITT and SARA KOLLACK-WALKER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51924.x
Peptides, Steroids, and Pair Bonding (pages 260–272)
C. SUE CARTER, A. COURTNEY DeVRIES, SUSAN E. TAYMANS, R. LUCILLE
ROBERTS, JESSIE R. WILLIAMS and LOWELL L. GETZ
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51925.x
Brain Sexual Dimorphism and Sex Differences in Parental and Other Social
Behaviors (pages 273–286)
GEERT J. De VRIES and CONSTANZA VILLALBA
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51926.x
Regulatory Mechanisms of Oxytocin-Mediated Sociosexual Behavior (pages 287–
301)
DIANE M. WITT
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51927.x
Molecular Aspects of Monogamy (pages 302–316)
THOMAS R. INSEL, LARRY YOUNG and ZUOXIN WANG
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51928.x
Part 3. Cognition and Communication
Conflict Resolution and Distress Alleviation in Monkeys and Apes (pages 317–
328)
FRANS B. M. De WAAL and FILIPPO AURELI
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51929.x
Early Learning and the Social Bond (pages 329–339)
ERIC B. KEVERNE, CLAIRE M. NEVISON and FRANCES L. MARTEL
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51930.x
Affiliative Processes and Vocal Development (pages 340–351)
CHARLES T. SNOWDON
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51931.x
Audio-Vocal Learning in Budgerigars (pages 352–367)
WILLIAM S. HALL, KELLY K. COOKSON, JAMES T. HEATON, TODD ROBERTS,
STEPHEN D. SHEA and STEVEN E. BRAUTH
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51932.x
Functional Anatomy of Forebrain Vocal Control Pathways in the Budgerigar
(Melopsittacus undulatus) (pages 368–385)
STEVEN E. BRAUTH, JAMES T. HEATON, STEPHEN D. SHEA, SARAH E. DURAND
and WILLIAM S. HALL
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51933.x
Neural Correlates of Sensitive Periods in Avian Song Learning (pages 386–400)
KATHY W. NORDEEN
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51934.x
Part 4. Clinical and Societal Issues
Psychobiology of Early Social Attachment in Rhesus Monkeys Clinical
Implications : Clinical Implications (pages 401–418)
GARY W. KRAEMER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51935.x
Psychological and Neuroendocrinological Sequelae of Early Social Deprivation in
Institutionalized Children in Romania (pages 419–428)
MARY CARLSON and FELTON EARLS
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51936.x
Role of Psychosocial Factors in the Onset of Major Depression (pages 429–439)
DAVID J. KUPFER and ELLEN FRANK
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51937.x
Social Behavior in Autism (pages 440–454)
JAMES B. GROSSMAN, ALICE CARTER and FRED R. VOLKMAR
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51938.x
Affiliation and Neuropsychiatric Disorders: The Deficit Syndrome of
Schizophrenia (pages 455–468)
BRIAN KIRKPATRICK
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51939.x
Part 5. Poster Papers
Vagal Reactivity and Affective Adjustment in Infants (pages 469–471)
OLGA V. BAZHENOVA and STEPHEN W. PORGES
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51940.x
Prolactin and Modulation of Social Processes in Domestic Chicks (pages 472–474)
MARNI Y. V. BEKKEDAL and JAAK PANKSEPP
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51941.x
Effects of Serotonin Depletion on the Play of Juvenile Rats (pages 475–477)
B. KNUTSON and J. PANKSEPP
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51942.x
Effects of Vasotocin on Aggressive Behavior in Male Japanese Quail (pages 478–
480)
LAUREN V. RITERS and JAAK PANKSEPP
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51943.x
Communicative Genes and the Evolution of Empathy : Selfish and Social
Emotions As Voices of Selfish and Social Genes (pages 481–483)
ROSS BUCK and BENSON GINSBURG
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51944.x
Innateness of Communicative Behaviors (pages 484–485)
BENSON E. GINSBURG and ROSS BUCK
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51945.x
Male Influence on Interbirth Interval in the Monogamous California Mouse When
Required to Forage for Food (pages 486–489)
DEBORA CANTONI and RICHARD E. BROWN
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51946.x
Effects of Prenatal Stress on Behavior in Adolescent Rhesus Monkeys (pages
490–491)
A. S. CLARKE and AND M. L. SCHNEIDER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51947.x
Serotonergic Intervention Increases Affiliative Behavior in Humans (pages 492–
493)
B. KNUTSON, S. COLE, O. WOLKOWITZ, V. REUS, T. CHAN and E. MOORE
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51948.x
Social Modulation of Corticosteroid Responses in Male Prairie Voles (pages 494–
497)
COURTNEY DEVRIES, SUSAN E. TAYMANS and C. SUE CARTER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51949.x
The Emergence of Affiliative Behavior in Infant Spotted Hyenas (Crocuta crocuta)a
: (Crocuta crocuta) (pages 498–500)
CHRISTINE M. DREA, JASON E. HAWK and STEPHEN E. GLICKMAN
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51950.x
Neurohumoral Brain Dynamics of Social Group Formation Implications for Autism
(pages 501–503)
WALTER J. FREEMAN
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51951.x
Differential Fos Expression Following Microinjection of Oxytocin or Vasopressin
in the Prairie Vole Brain (pages 504–505)
B. S. GINGRICH, R. L. HOUT, Z. WANG and T. R. INSEL
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51952.x
Are There Oxytocin Receptors in the Primate Brain? (pages 506–509)
D. M. TOLOCZKO, L. YOUNG and T. R. INSEL
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51953.x
Developmental Changes in Forebrain Vasopressin Receptor Binding in Prairie
Voles (Microtus ochrogaster) and Montane Voles (Microtus montanus) (pages
510–513)
ZUOXIN WANG, YUE LIU, LARRY J. YOUNG and THOMAS R. INSEL
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51954.x
The 5’ Flanking Region of the Monogamous Prairie Vole Oxytocin Receptor Gene
Directs Tissue-Specific Expression in Transgenic Mice (pages 514–517)
L. J. YOUNG, K. G. WAYMIRE, R. NILSEN, G. R. MACGREGOR, Z. WANG and T. R.
INSEL
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51955.x
Neurobiology of Avian Social Organization Effects of Lateral Septum Lesions in a
Territorial Songbird, the Field Sparrow (Spizella pusilla), and a Colonial Songbird,
the Zebra Finch (Taeniopygia guttata) (pages 518–521)
JAMES L. GOODSON, RICHARD EIBACH, ANNA DUKES, MICHELLE FRIEDMAN,
JON SAKATA, RICHMOND THOMPSON and ELIZABETH ADKINS-REGAN
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51956.x
Patterns of Ovulation, Reactivity, and Family Emotional Process (pages 522–524)
VICTORIA HARRISON
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51957.x
Characterization of Adrenal Hormone Binding Sites in the Prairie Vole (pages 525–
529)
N. B. HASTINGS and B. S. McEWEN
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51958.x
Heterosexual Interactions Promote Oxytocin Secretion in Sexually Naive, but Not
Experienced, Male Wistar Rats (pages 530–533)
VIVEKA HILLEGAART, PAWEL ALSTER, KERSTIN UVNÄS-MOBERG and SVEN
AHLENIUS
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51959.x
Competition and Chemical Communication in Wild Groups of Common Marmosets
(Callithrix jacchus) (pages 534–537)
C. LAZARO-PEREA, C. T. SNOWDON and D. P. SANTEE
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51960.x
Socioemotional Behavior in Adult Rhesus Monkeys after Early versus Late
Lesions of the Medial Temporal Lobe (pages 538–540)
LUDIŠE MÁLKOVÁ, MORTIMER MISHKIN, STEPHEN J. SUOMI and JOCELYNE
BACHEVALIER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51961.x
Does Estrogen Facilitate Social Behavior by Reducing Anxiety? (pages 541–542)
MARGARET M. McCARTHY, SUSAN SCHWARTZ-GIBLIN and SUE-MAY WANG
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51962.x
Oxytocin-Induced Paw Sucking in Infant Rats (pages 543–545)
ERIC NELSON and JEFFREY R. ALBERTS
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51963.x
The Affiliative Vocal Subsystem of Squirrel Monkeys (pages 546–548)
JOHN D. NEWMAN and DEBORAH E. BERNHARDS
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51964.x
Intra- and Extra-Pair Behavior and Initial Clutch Success in Captive Zebra Finch
Colonies (pages 549–551)
JOANNE OLIVA-PURDY and CHERYL F. HARDING
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51965.x
Mice Show Strain Differences in Social Affiliation Implications for Open Field
Behavior (pages 552–554)
J. O. PIEPER, D. C. FORESTER and G. I. ELMER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51966.x
Female Reproductive Status and Male Pairmate Behavior in Cotton-Top Tamarins
(pages 556–558)
T. A. PORTER and C. T. SNOWDON
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51967.x
Intraspecific Variation and the Presence of a Father Can Influence the Expression
of Monogamous and Communal Traits in Prairie Voles (pages 559–562)
R. LUCILLE ROBERTS and C. SUE CARTER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51968.x
Perinatal Hormone Exposure Alters the Expression of Selective Affiliative
Preferences in Prairie Voles (pages 563–565)
R. LUCILLE ROBERTS, ERIC A. GUSTAFSON and C. SUE CARTER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51969.x
Escape from Social Suppression of Sexual Behavior and of Ovulation in Female
Common Marmosets (pages 567–570)
WENDY SALTZMAN, NANCY J. SCHULTZ-DARKEN, JESSICA M. SEVERIN and
DAVID H. ABBOTT
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51970.x
The Role of Contact Calls in the Social Behavior of the Budgerigar (Melopsittacus
undulatus) (pages 571–573)
STEPHEN D. SHEA, KRISTIN J. HEATON, JAMES T. HEATON, WILLIAM S. HALL and
STEVEN E. BRAUTH
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51971.x
Social Stress, Depression, and Brain Dopamine in Female Cynomolgus Monkeys
(pages 574–577)
CAROL A. SHIVELY, KATHLEEN A. GRANT, RICHARD L. EHRENKAUFER, ROBERT
H. MACH and MICHAEL A. NADER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51972.x
Sexually Initiated Affiliation Facilitates Rhesus Monkey Integration (pages 578–
582)
PAMELA L. TANNENBAUM and KIM WALLEN
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51973.x
Attachment Representations and Sexual Behavior in Humans (pages 583–586)
REBECCA TURNER, BEVERLY JANUSZEWSKI, AMY FLACK and BRUCE COOPER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51974.x
Aggressive Youth: Healing Biology with Relationship (pages 587–589)
J. ERIC VANCE
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51975.x
Postestrus Anogenital Swelling in Female Barbary Macaques The Larger, the
Better? (pages 590–592)
B. WALLNER and J. DITTAMI
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51976.x
Circulating Oxytocin in Male Guinea Pigs Affected by the Female Cohabitation and
Reproductive Condition (pages 593–595)
R. BARTH, B. WALLNER, J. DITTAMI and D. SCHAMS
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51977.x
Relationship between Oxytocin and the Biphasic Effects of Progesterone in the
Control of Hamster Sexual Receptivity (pages 596–598)
D. CAROL WHITMAN and H. ELLIOTT ALBERS
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51978.x
Role of Prolactin in Paternal Care in a Monogamous New World Primate, Saguinus
oedipus (pages 599–601)
TONI E. ZIEGLER and CHARLES T. SNOWDON
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51979.x
The Effects of Electrical Stimulation of the Medial Preoptic Area and the Medial
Amygdala on Maternal Responsiveness in Female Rats (pages 602–605)
HYWEL D. MORGAN, JASON A. WATCHUS and ALISON S. FLEMING
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51980.x
Hypothalamic Paraventricular Nucleus, Oxytocin, and Maternal Aggression in Rats
(pages 606–609)
M. GIOVENARDI, M. J. PADOIN, L. P. CADORE and A. B. LUCION
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51981.x
Exploratory Behavior Correlates with Social Organization and Is Responsive to
Peptide Injections in Prairie Voles (pages 610–612)
ASHWIN DHARMADHIKARI, YEUN S. LEE, R. LUCILLE ROBERTS and C. SUE CARTER
Article first published online: 17 DEC 2006 | DOI: 10.1111/j.1749-6632.1997.tb51982.x
INTRODUCTION
C. SUE CARTER,” I. IZJA LEDERHENDLER,b AND
BRIAN KIRKPATRICK‘
aDepartment of Zoology
University of Maryland
College Park, Maryland 20742
bSystems Neuroscience Program
National Institute of Mental Health
National Institutes of Health
Rockwell, Maryland 20857
‘Maryland Psychiatric Research Center
Department of Psychiatry
University of Maryland School of Medicine
Baltimore, Maryland 21228
This volume of the Annals of the New York Academy of Sciences represents the
proceedings of a conference sponsored by The National Institute of Mental Health
with additional support from The National Institute for Child Health and Human
Development and the National Science Foundation. The conference was held in
Washington, DC, in March 1996. The central purpose and theme of this meeting
was to examine the biological and especially the neural substrates of affiliation and
related social behaviors. It was particularly appropriate that one way The National
Institute of Mental Health chose to celebrate its fiftieth anniversary was through this
optimistic theme-striving to improve our understanding of human interactions.
Affiliation refers to social behaviors that bring individuals closer together, This
includes such forms of positive association as attachment, parent-offspring interac-
tions, pair-bonding, and coalitions. Affiliations provide a social matrix within which
other behaviors, including reproduction and aggression, may occur. Reproductive
and aggressive behaviors also reduce the distance between individuals, but their
expression is regulated, in part, by a positive social fabric based on affiliations.
Affiliation, treated as an independent topic, received little attention prior to 1990.
However, a review of recent Medline citations revealed a 10-fold increase in research
on “affiliation” between 1971 and 1994, while studies of “aggression” declined
slightly during that period (Levine et al.). Since a variety of terms may be used to
describe social behavior, it is likely that this analysis underestimates contemporary
interest in this topic.
Social behavior and, to a lesser extent, affiliation previously have been described
in the context of psychology, sociology, anthropology, psychiatry, and evolutionary
biology. However, little attention has been directed at the regulatory physiology and
neural processes that subserve affiliative behaviors. In fact, scientists have only
recently recognized a set of biological substrates frequently associated with the
expression of such behaviors.
Because research on social behavior does not fall within well-defined scientific
boundaries, one goal of this conference was to bring together scientists with interdisci-
xiii
xiv ANNALS NEW YORK ACADEMY OF SCIENCES
plinary and integrative perspectives on the neurobiology of affiliation. The integrative
framework facilitates interactions between researchers who study behavior in the
context of natural history with those who study the nervous system. We sought to
provide an open forum which could strengthen integrative research by discussing
both analytic and synthetic findings and by discussing not only what is known, but
also what may be absent in our understanding of affiliative behaviors.
It has been argued that affiliative behaviors evolved from reproductive behaviors
(Crews) and indeed, affiliative behaviors must serve the purposes of reproduction.
The interdependence of these classes of behavior was further emphasized in cases
in which behaviors aimed at providing for self-defense and immediate survival must
be inhibited to permit sexual and parental behaviors. From the individual's point of
view, the need for increased proximity associated with mating may be regarded as
potentially dangerous. Monogamy, or other forms of social bonds or coalitions, may
be significant in providing comparatively secure social environments for reproduction
and other positive social behaviors such as parental behavior.
Complex behavior systems capable of reducing conflict and maximizing coopera-
tion have been observed in animals as diverse as spotted hyenas (Glickman et al.)
and chimpanzees (De Waal and Aureli). The evolutionary importance of such systems
is powerfully illustrated by the fact that physiological processes, such as the production
of gonadal sex steroids (Wingfield et al.) or sperm (Dixson), are correlated with
social organization in diverse species of birds and mammals.
Social experiences can affect the subsequent expression of affiliative behaviors
and can alter various physiological processes. Documentation of the effects of early
social experiences is abundant in the nonhuman primate and human literature (Levine
et al.; Kraemer; Keverne et al.; Carlson and Earls; Grossman et al.; Kupfer and
Frank). For example, in primates, early attachment experiences with a mother or
other caregiver may 'nave long-lasting consequences for the development of both
cognitive and emotional systems (Kraemer). Research with squirrel monkeys reveals
striking increases in activity within the adrenal axis following separation from either
a parent or peer and conversely has demonstrated the capacity of social companionship
to buffer these physiological effects (Levine et al.; Mendoza and Mason).
Dramatic examples of the physiological consequences of the social environment
in adult animals come from studies in nonhuman primates. In rhesus monkeys,
sexual experience with females in the group may allow males to develop affiliative
relationships (Wallen and Tannenbaum). The importance of social behavior for repro-
ductive success also is illustrated in the common marmoset. This species usually
exhibits a social system built around a monogamous breeding pair where ovulation
is inhibited in socially subordinate females. The mechanisms for this social inhibition
of reproduction remain unknown, but increased stress or suppression of gonadotropin-
releasing hormone have been excluded (Abbott et al.).
Physiological studies of social, sexual, parental, and aggressive behavior typically
have emphasized the role of the central nervous system (CNS) in these behaviors.
An emergent theme in these studies is the role of specific neural tissues in approach
and avoidance behaviors in the presence of social stimuli. Neuroanatomical systems
for maternal behavior in domestic rats are particularly well characterized. Based on
research in rats, it has been proposed that parental behavior requires the suppression
of fearful or aversive responses in the presence of infants and a concurrent approach