Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callithrix penicillata
Open accessAbstract
The establishment and maintenance of stable, long-term male-female relationships, or pair-bonds, are marked by high levels of mutual attraction, selective preference for the partner, and high rates of sociosexual behavior. Central oxytocin (OT) affects social preference and partner-directed social behavior in rodents, but the role of this neuropeptide has yet to be studied in heterosexual primate relationships. The present study evaluated whether the OT system plays a role in the dynamics of social behavior and partner preference during the first 3 weeks of cohabitation in male and female marmosets, Callithrix penicillata. OT activity was stimulated by intranasal administration of OT, and inhibited by oral administration of a non-peptide OT-receptor antagonist (L-368,899; Merck). Social behavior throughout the pairing varied as a function of OT treatment. Compared to controls, marmosets initiated huddling with their social partner more often after OT treatments but reduced proximity and huddling after OT antagonist treatments. OT antagonist treatment also eliminated food sharing between partners. During the 24-h preference test, all marmosets interacted more with an opposite-sex stranger than with the partner. By the third-week preference test, marmosets interacted with the partner and stranger equally with the exception that intranasal-OT treatments facilitated initial partner-seeking behavior over initial contact with the stranger. Our findings demonstrate that pharmacological manipulations of OT activity alter partner-directed social behavior during pair interactions, suggesting that central OT may facilitate the process of pair-bond formation and social relationships in marmoset monkeys.
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L-368,899 is a small-molecule OXTR antagonist employed in NHP research.
“The Merck compound L-368,899 is another small molecule OXTR antagonist that has been used in NHP studies (93), has excellent bioavailability after oral administration (94) and has been also reported to accumulate in limbic structures of the brains of rhesus macaques after peripheral injection (95).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [93]
Daily treatment of marmosets with 50 μg oxytocin for 30 days facilitated pair-bond formation.
“These results parallel those of an exogenous oxytocin study on marmosets where daily treatment of 50 μg for 30 days facilitated pair-bond formation (Smith et al., 2010).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Smith et al., 2010
Marmosets display a more flexible pattern of sociosexual preferences than prairie voles.
“marmosets display a more flexible pattern of sociosexual preferences (Cavanaugh et al., 2014; Smith et al., 2010).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Smith et al., 2010
Marmosets treated with a nonpeptide OTa (L-368,899) reduced huddling behavior and food sharing with their partner over the same time period.
“marmosets treated with a nonpeptide OTa (L-368,899) reduced huddling behavior and food sharing with their partner over the same time period (Smith et al. 2010).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Smith et al. 2010
Male and female marmosets treated with an IN Leu8-OT agonist showed enhanced affiliation toward pairmates during the first 3 weeks of cohabitation.
“Male and female marmosets treated with an IN Leu8-OT agonist showed enhanced affiliation toward pairmates during the first 3 weeks of cohabitation (Smith et al., 2010).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Smith et al., 2010
OT regulates the gain of pre-existing social preferences rather than changing their fundamental character.
“Taken together, these observations are consistent with the hypothesis that OT regulates the gain of pre-existing social preferences rather than changing their fundamental character.”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Smith et al., 2010
OXT modulates pair-bonding between opposite-sex partners.
“OXT modulates pair-bonding between opposite-sex partners (Cavanaugh, Mustoe, Taylor, & French, 2014; Smith, Agmo, Birnie, & French, 2010; Young & Wang, 2004)”
From Inequity aversion strategies between marmosets are influenced by partner familiarity and sex but not by oxytocin (2016) · cites this paper as Smith, Agmo, Birnie, & French, 2010
In newly-formed marmoset pairs, administration of an OXTA reduces measures of social proximity and food sharing.
“In newly-formed marmoset pairs, administration of an OXTA reduces measures of social proximity and food sharing (Smith et al., 2010).”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Smith et al., 2010
Marmosets display a flexible pattern of sociosexual preferences similar to those displayed by humans.
“However, unlike prairie voles, which display a consistently strong partner preference, marmosets display a flexible pattern of sociosexual preferences (Smith et al., 2010; Cavanaugh et al., 2014), similar to those displayed by humans (Buss and Schmitt, 1993).”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Smith et al., 2010
There is converging evidence that both the consensus-mammalian variant of OXT and the marmoset variant of OXT regulate affiliative and sociosexual behavior in marmosets.
“Thus, there is converging evidence that both the consensus-mammalian variant of OXT (Smith et al., 2010; Saito and Nakamura, 2011) as well as the marmoset variant of OXT (Cavanaugh et al., 2014; Mustoe et al., 2015) regulate affiliative and sociosexual behavior in marmosets.”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Smith et al., 2010
Well-established social relationships may be less sensitive to OXTA interventions, relative to the more dynamic social interactions during the establishment and development of new bonds.
“Thus, well-established social relationships may be less sensitive to OXTA interventions, relative to the more dynamic social interactions during the establishment and development of new bonds.”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Smith et al., 2010
Treatment with an OT agonist had a limited effect and only subtly augmented marmoset sociality during the early period of cohabitation.
“However, treatment with an OT agonist had a limited effect, and only subtly augmented marmoset sociality during the early period of cohabitation.”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Smith et al., 2010
The limited effect of the consensus mammalian OT agonist on marmoset sociality may be a consequence of the distinct amino-acid structure of the OT ligand in marmosets.
“Therefore, the limited effect of the consensus mammalian OT agonist on marmoset sociality (Smith et al., 2010) may be a consequence of the distinct amino-acid structure of the OT ligand in marmosets.”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Smith et al., 2010
Blocking endogenous OT activity in both males and females reduced measures of social proximity and food sharing with a new pair-mate.
“Blocking endogenous OT activity in both males and females reduced measures of social proximity and food sharing with a new pair-mate (Smith et al., 2010).”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Smith et al., 2010
Male and female marmosets (C. penicillata) interacted more with a stranger than a newly paired partner after 24 hours of cohabitation, but after three weeks of cohabitation, they interacted equally with both a partner and a stranger.
“Male and female marmosets (C. penicillata) interacted more with a stranger than a newly paired partner after 24 hours of cohabitation. However, after three weeks of cohabitation, male and female marmosets interacted equally with both a partner and a stranger (Smith et al., 2010).”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Smith et al., 2010
Treatment with an OTA has been shown previously to reduce proximity, huddling, and food sharing behavior with a recently formed partner in marmosets.
“This finding is surprising because treatment with an OTA has been shown previously to reduce proximity, huddling, and food sharing behavior with a recently formed partner in marmosets.”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Smith et al., 2010
Treatment with an OTA reduced the frequency, and increased the latency, to establish contact with a partner before engaging with a stranger, after three weeks of cohabitation and continuous treatment.
“Furthermore treatment with an OTA reduced the frequency, and increased the latency, to establish contact with a partner before engaging with a stranger, after three weeks of cohabitation and continuous treatment (Smith et al., 2010).”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Smith et al., 2010
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“Subsequent studies found that administration of the marmoset-specific variant of the OT ligand (Pro(8)-OT) reduced time that marmosets spent in close proximity to opposite-sex strangers (Cavanaugh, Mustoe, Taylor, & French, 2014).”
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Intranasal oxytocin enhances socially-reinforced learning in rhesus monkeys
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- Authors
- Smith, A. S., Ågmo, A., Birnie, A. K., & French, J. A.
- Affiliations
- University of Nebraska at Omaha (US)
- UiT The Arctic University of Norway (NO)
- Corresponding author
- Smith, Adam S.
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2010-02
- Volume
- 57
- Issue
- 2
- Pages
- 255-262
- ISSN
- 0018-506X (ISSN-L)
- PMC
- PMC2824532
- OpenAlex
- W2075098633
- Cited by
- 228
- References
- 64
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 7 · 2023: 9 · 2022: 17 · 2021: 18 · 2020: 14 · 2019: 12 · 2018: 24 · 2017: 10 · 2016: 18 · 2015: 24 · 2014: 20 · 2013: 20 · 2012: 10
- FWCI
- 11.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation
- Merck
- University Research Committee, Emory University
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD 42882, R01HD042882, R56HD042882)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- oxytocin, pair bonding, mate preferences, social behavior, Callithrix penicillata, marmoset, L-368,899, oxytocin receptor antagonist, intranasal oxytocin, food sharing, huddling, sociosexual behavior
- MeSH terms
- Animals, Camphanes, Callithrix, Central Nervous System Agents, Female, Housing, Animal, Male, Oxytocin, Pair Bond, Piperazines, Sexual Behavior, Animal, Social Behavior, Time Factors, Receptors, Oxytocin
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