Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys

Winslow, James T; Noble, Pamela L; Lyons, Casie K; Sterk, Sheila M; Insel, Thomas R

doi:10.1038/sj.npp.1300128

Cited by 345Neuroendocrine regulation and behaviorPrimate Behavior and EcologyStress Responses and Cortisol

Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys

Winslow, James T, Noble, Pamela L, Lyons, Casie K, Sterk, Sheila M, Insel, Thomas R·2003·Neuropsychopharmacology

DOI 10.1038/sj.npp.1300128

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Abstract

Mother-reared (MR) and nursery-reared (NR) male rhesus monkeys exhibit profound and persistent differences in social and emotional behavior. Compared to MR animals, NR monkeys show reduced reciprocal social behaviors and increased agonistic behavior and high levels of stereotypy. Cerebrospinal fluid oxytocin (CSF OT) in NR monkeys was significantly reduced compared to MR monkeys measured at 18, 24, and 36 months of age. Correlations between OT and individual social behavioral profiles measured across rearing conditions also revealed a significant association between OT and the expression of affiliative social behaviors including allogrooming and reciprocal intermale mounting at each age examined. In contrast, CSF vasopressin levels did not differ according to rearing history, but did correlate with fearful behaviors independent of rearing history. Differential rearing was not associated with differences in basal or stress-related plasma cortisol, although these levels did progressively decline as monkeys matured. MR but not NR monkeys were able to use a social companion to buffer their response to a stressor, but OT levels did not appear to be sensitive to the presence of a social companion in either group. These results are consistent with earlier reports from studies of rodents suggesting an important role for central OT pathways in the development of social affiliation.

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In rhesus monkeys, CSF oxytocin was associated with social behaviour, whereas plasma oxytocin was not, and plasma oxytocin did not track same-session CSF oxytocin.
“while CSF oxytocin correlated with social behaviour, plasma levels did not, nor did they correlate with CSF levels collected in the same session (88).”
From Intranasal Oxytocin: Myths and Delusions (2016) · cites this paper as [88]
Both types of lesions produced a loss in caudate OT content.
“Important for our investigation, both types of lesions produced a loss in caudate OT content.”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [139]
Lesions of the PVN and SON affect different populations of OT fibers, using radioimmunoassay.
“Lesions of the PVN and SON effect different populations of OT fibers, using radioimmunoassay [139].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [139]
Oxytocin plays a key role in social bonding, having both short-term and long-term effects.
“Oxytocin is known to play a key role in social bonding (Ross and Young, 2009), having both short-term and long-term effects (Winslow et al., 2003).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Winslow et al., 2003
In rhesus macaques, adolescents raised in a nursery by human caregivers had lower cerebrospinal fluid (CSF) oxytocin concentrations than those raised by their mother.
“Also of note, in rhesus macaques, adolescents raised in a nursery by human caregivers had lower cerebrospinal fluid (CSF) oxytocin concentrations than those raised by their mother (Winslow et al., 2003).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Winslow et al., 2003

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Authors: Winslow, J. T., Noble, P. L., Lyons, C. K., Sterk, S. M., & Insel, T. R.
Affiliations: Emory University (US)
Corresponding author: Winslow, James T
ORCID: Insel, Thomas R
Venue: Neuropsychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2002-12-19
Volume: 28
Issue: 5
Pages: 910-918
ISSN: 0893-133X (ISSN-L)
1740-634X
DOI: 10.1038/sj.npp.1300128
OpenAlex: W2120350428
Cited by: 345
References: 75
Citations by year: 2026: 3 · 2025: 6 · 2024: 9 · 2023: 7 · 2022: 11 · 2021: 19 · 2020: 35 · 2019: 21 · 2018: 12 · 2017: 23 · 2016: 31 · 2015: 24 · 2014: 26 · 2013: 17 · 2012: 14
FWCI: 7.05
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Neuropsychopharmacology (publishedVersion)
PubMed (publishedVersion)
Funders: National Science Foundation (9876754)
Emory University
National Institutes of Health (RR‐00165)
National Institute of Mental Health (MH 57704, P50MH058922, MH58922, R01MH057704)
National Center for Research Resources (RR-00 165, P51RR000165)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: social buffering, rhesus monkeys, nursery rearing, vasopressin, cortisol, allogrooming, agonistic behavior, stereotypy, social development (developmental psychology), stress response
MeSH terms: Animals, Macaca mulatta, Male, Maternal Deprivation, Oxytocin, Social Behavior, Stress, Physiological

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Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys

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