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Cited by 487Neuroendocrine regulation and behaviorNeuropeptides and Animal PhysiologyRegulation of Appetite and Obesity

Oxytocin — A neuropeptide for affiliation: Evidence from behavioral, receptor autoradiographic, and comparative studies

Insel, Thomas R.·1992·Psychoneuroendocrinology
DOI 10.1016/0306-4530(92)90073-g
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Abstract

Oxytocin (OT) is a nine amino acid peptide synthesized in hypothalamic cells which project either to the neurohypophysis or to sites within the central nervous system. Although neurohypophyseal OT release has long been associated with uterine contraction and milk ejection, the function of intracerebral OT remains unclear. On the basis of behavioral, cellular, and comparative studies, this review suggests that brain OT influences the formation of social bonds. The first part of this review examines evidence linking central OT to several forms of affiliation. Central administration of OT induces maternal and reproductive behaviors in rats primed with gonadal steroids. OT antagonists and hypothalamic lesions block the initiation of maternal and reproductive behaviors but have no effects on these behaviors once established. Our new studies in rat pups demonstrate that central OT selectively decreases the separation response, an effect which mimics social contact. These studies of parental, reproductive, and attachment behaviors suggest that exogenous OT has "prosocial" effects and that endogenous OT may be essential for initiating social interaction. In a second series of experiments, we investigated the cellular mechanisms for OT's effects on social behavior by means of autoradiographic receptor binding. In the rat forebrain, OT receptors are expressed in several limbic regions believed to be involved in the integration of sensory processing. The regulation of these receptors is surprisingly resistant to either ablation of OT cells or repeated central administration of OT. However, receptors in two regions, the bed nucleus of the stria terminalis (BNST) and the ventromedial nucleus of the hypothalamus (VMN), appear selectively induced by exogenous or endogenous increases in gonadal steroids. At parturition, binding to OT receptors increases 84% in the BNST, and at estrus, binding increases 35% in the VMN. These results demonstrate that physiologic changes in gonadal steroids can alter receptor expression in anatomically discrete target fields and thereby direct responsiveness to endogenous neuropeptide release. A model for OT's effects on social behavior is proposed, which relies on the heterologous regulation of the brain OT receptor. A third series of experiments tested the hypothesis that brain OT influences affiliation by comparing prairie and montane voles, two closely related species with dichotomous systems of social organization. Although no differences appear in the presynaptic expression of the neuropeptide, OT receptors are distributed in complementary patterns in the two species. In the highly affiliative prairie vole, receptors are most evident in the BNST and one of its primary afferents, the lateral amygdala, highlighting a circuit previously implicated in maternal behavior.(ABSTRACT TRUNCATED AT 400 WORDS)

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Authors
Insel, T. R.
Affiliations
National Institute of Mental Health (US)
Corresponding author
Insel, Thomas R.
ORCID
Insel, Thomas R.
Venue
Psychoneuroendocrinology
Publisher
Elsevier BV
Published
1992-03
Volume
17
Issue
1
Pages
3-35
ISSN
0306-4530 (ISSN-L)
DOI
10.1016/0306-4530(92)90073-g
OpenAlex
W2002969394
Cited by
487
References
142
Citations by year
2026: 4 · 2025: 12 · 2024: 18 · 2023: 5 · 2022: 5 · 2021: 7 · 2020: 9 · 2019: 19 · 2018: 13 · 2017: 14 · 2016: 16 · 2015: 18 · 2014: 22 · 2013: 12 · 2012: 12
FWCI
37.10
Type
journal article
Language
en
Open access
closed
Licence
Locations
  • Psychoneuroendocrinology (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords
oxytocin, social affiliation, social bonding, maternal behavior, reproductive behavior, attachment behavior, oxytocin receptor, bed nucleus of the stria terminalis, ventromedial hypothalamus, sex steroids, Microtus ochrogaster, montane vole, social organization, limbic system, neuropeptide regulation, prosocial behavior
MeSH terms
Animals, Autoradiography, Behavior, Animal, Humans, Oxytocin, Receptors, Angiotensin, Sexual Behavior, Social Behavior, Receptors, Oxytocin

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