Elsevier

Hormones and Behavior

Volume 50, Issue 4, November 2006, Pages 518-528
Hormones and Behavior

The neuroscience of affiliation: Forging links between basic and clinical research on neuropeptides and social behavior

https://doi.org/10.1016/j.yhbeh.2006.06.018Get rights and content

Abstract

Animal studies point to the role of two neuropeptides–oxytocin and vasopressin–in the regulation of affiliative behaviors including mating, pair-bond formation, maternal/parenting behavior, and attachment. These findings may have important implications for understanding and treating clinical disorders marked by social deficits and/or disrupted attachment. This review focuses on advances made to date in the effort to forge links between basic and clinical research in the area of neuropeptides and social behavior. The literature on oxytocin and its involvement in stress response, affiliation, and prosocial behavior is reviewed, and the implications of these findings for such disorders as autism as well as other social and stress-related disorders including social phobia, post-traumatic stress disorder, and some personality disorders are considered. Finally, unresolved issues and directions for future research are discussed.

Introduction

Noting the ubiquity of abnormal social attachments in “virtually every form of psychopathology” (p. 726), Insel (1997) called attention to the importance of research investigating the neurobiology involved in social bond formation. Animal studies support the role of two neuropeptides, oxytocin and vasopressin, in the regulation of affiliative behaviors including mating, pair-bond formation, maternal/parenting behavior, and attachment. This article reviews advances made to date in the effort to forge links between basic and clinical research in the area of neuropeptides and social behavior. Because Lim and Young (see our companion article in this issue) review the animal literature in this area in detail, this article will focus on the implications of the findings from animal studies as well as those from studies of healthy humans regarding neuropeptides and social behavior for clinical disorders. Moreover, although findings from animal studies point to the involvement of oxytocin and vasopressin in social behavior, we will concentrate primarily on oxytocin because most of the studies conducted thus far in humans have focused on oxytocin. In the first part of this review, we examine the involvement of oxytocin in stress response, affiliation, and prosocial behavior; we touch briefly on the findings from animal studies, but our primary focus is studies of healthy humans. In the second part of this review, we address the clinical implications of these findings as well as of the findings from animal studies. In particular, we address the relevance of oxytocin for such disorders as autism as well as other social and stress-related disorders including social phobia, obsessive-compulsive disorder (OCD), post-traumatic stress disorder (PTSD), and borderline personality disorder (BPD). Finally, we conclude with a discussion of unresolved issues and directions for future research.

Section snippets

Oxytocin, stress, and social affiliation

Before reviewing the evidence to date regarding the role of oxytocin in humans, it should be noted that research in this area has been hampered because of the methodological difficulties involved. Whereas animal researchers have had a number of tools at their disposal (e.g., the ability to centrally administer oxytocin and oxytocin antagonists, manipulate the expression of oxytocin by knocking out specific genes, and directly assess oxytocin mRNA), researchers investigating the role of oxytocin

Oxytocin and autism

According to the Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev.; DSM-IV-TR, American Psychiatric Association, 2000), autism is a developmental disorder characterized by abnormalities in speech and communication, impaired social functioning, and repetitive behaviors and restricted interests. A number of researchers have suggested that oxytocin and vasopressin may be implicated in the etiology of autism given that deficits in social interaction and affiliation are a

Unresolved issues and future directions

In conclusion, most of the studies investigating the neurobiology of social behavior and affiliation have used animal models; however, recent methodological advances have allowed researchers to begin to ask more rigorous questions concerning the neurobiology of human social behavior. The findings to date have been encouraging and suggest that oxytocin and possibly vasopressin, which have been implicated in animal studies, are also involved in human affiliation. In addition to shedding light on

Acknowledgments

Preparation of this article was supported by grants from the National Institute of Health 5 U54 MH066673-03 STAART Autism Centers of Excellence, Beatrice and Samuel A. Seaver Foundation, National Institute on Neurological Disorders and Stroke, National Institute on Drug Abuse, and the Orphan Products Division of the Food and Drug Administration. We gratefully acknowledge Evdokia Anagnostou for comments on an earlier version of this article. Dr. Hollander is listed as an inventor on a patent for

References (117)

  • L. Green et al.

    Oxytocin and autistic disorder: alterations in peptide forms

    Biol. Psychiatry

    (2001)
  • M. Heinrichs et al.

    Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress

    Biol. Psychiatry

    (2003)
  • T.R. Insel

    Oxytocin-a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies

    Psychoneuroendocrinology

    (1992)
  • T.R. Insel

    Is social attachment an addictive disorder?

    Physiol. Behav.

    (2003)
  • T.R. Insel et al.

    Central administration of oxytocin modulates the infant rat's response to social isolation

    Eur. J. Pharmacol.

    (1991)
  • T.R. Insel et al.

    Oxytocin, vasopressin, and autism: is there a connection?

    Biol. Psychiatry

    (1999)
  • K. Lieb et al.

    Borderline personality disorder

    Lancet

    (2004)
  • K.C. Light et al.

    More frequent partner hugs and higher oxytocin levels are linked to lower blood pressure and heart rate in premenopausal women

    Biol. Psychol.

    (2005)
  • M.M. Lim et al.

    Neuropeptides and the social brain: potential rodent models of autism

    Int. J. Dev. Neurosci.

    (2005)
  • Y. Liu et al.

    Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles

    Neuroscience

    (2003)
  • T. Lundeberg et al.

    Anti-nociceptive effects of oxytocin in rats and mice

    Neurosci. Lett.

    (1994)
  • M.M. McCarthy et al.

    Central nervous system actions of oxytocin and modulation of behavior in humans

    Mol. Med. Today

    (1997)
  • G. Meisenberg et al.

    Centrally mediated effects of neurohypophyseal hormones

    Neurosci. Biobehav. Rev.

    (1983)
  • C. Modahl et al.

    Plasma oxytocin levels in autistic children

    Biol. Psychiatry

    (1998)
  • I.D. Neumann

    Involvement of the brain oxytocin system in stress coping: interactions with the hypothalamo–pituitary–adrenal axis

    Prog. Brain Res.

    (2002)
  • J. Paris et al.

    Psychological risk factors for borderline personality disorder in female patients

    Compr. Psychiatry

    (1994)
  • D.E. Smith et al.

    Peptide and peptide analog transport systems at the blood–CSF barrier

    Adv. Drug Delivery Rev.

    (2004)
  • A. Tsuji

    Small molecular drug transfer across the blood–brain barrier via carrier-mediated transport systems

    NeuroRx

    (2005)
  • A. Tsuji et al.

    Carrier-mediated or specialized transport of drugs across the blood–brain barrier

    Adv. Drug Delivery Rev.

    (1999)
  • K. Uvnas-Moberg

    Neuroendocrinology of the mother–child interaction

    Trends Endocrinol. Metab.

    (1996)
  • K. Uvnas-Moberg

    Oxytocin may mediate the benefits of positive social interaction and emotions

    Psychoneuroendocrinology

    (1998)
  • K. Uvnas-Moberg et al.

    High doses of oxytocin cause sedation and low doses cause an anxiolytic-like effect in male rats

    Pharmacol. Biochem. Behav.

    (1994)
  • G. Adler

    Borderline Psychopathology and its Treatment

    (1986)
  • M. Altemus et al.

    Suppression of hypothalamic–pituitary–adrenal axis responses to stress in lactating women

    J. Clin. Endocrinol. Metab.

    (1995)
  • M. Altemus et al.

    Changes in cerebrospinal fluid neurochemistry during treatment of obsessive-compulsive disorder with clomipramine

    Arch. Gen. Psychiatry

    (1994)
  • American Psychiatric Association

    Diagnostic and Statistical Manual of Mental Disorders

    (2000)
  • E. Anagnostou et al.

    Factor analysis of the Y-BOCS in autistic disorder

    Neuropsychopharmacology

    (2005)
  • B.J. Aragona et al.

    Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds

    Nat. Neurosci.

    (2006)
  • L.S. Benjamin

    Interpersonal Diagnosis and Treatment of Personality Disorders

    (1993)
  • J.K. Bester-Meredith et al.

    Vasopressin and the transmission of paternal behavior across generations in mated, cross-fostered Peromyscus mice

    Behav. Neurosci.

    (2003)
  • I.F. Bielsky et al.

    Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice

    Neuropsychopharmacology

    (2004)
  • J. Born et al.

    Sniffing neuropeptides: a transnasal approach to the human brain

    Nat. Neurosci.

    (2002)
  • C.S. Carter

    Neuroendocrine perspectives on social attachment and love

    Psychoneuroendocrinology

    (1998)
  • C.S. Carter et al.

    Integrative functions of lactational hormones in social behavior and stress management

    Ann. N. Y. Acad. Sci.

    (1997)
  • F. Champagne et al.

    Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors

    Proc. Natl. Acad. Sci. U. S. A.

    (2001)
  • J.N. Ferguson et al.

    Social amnesia in mice lacking the oxytocin gene

    Nat. Genet.

    (2000)
  • J.N. Ferguson et al.

    Oxytocin in the medial amygdala is essential for social recognition in the mouse

    J. Neurosci.

    (2001)
  • D.D. Francis et al.

    Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences

    J. Neuroendocrinol.

    (2002)
  • A.B. Fries et al.

    Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior

    Proc. Natl. Acad. Sci. U. S. A.

    (2005)
  • J.G. Gunderson

    Borderline Personality Disorder

    (1984)
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