Oxytocin Administered Centrally Facilitates Formation of a Partner Preference in Female Prairie Voles (Microtus ochrogaster)
Abstract
Prairie voles (Microtus ochrogaster) are monogamous mammals that form male‐female pair bonds. Partner preference formation, one component of the pair bond in prairie voles, occurs following male‐female cohabitation and is facilitated by mating. The peptide hormone oxytocin is released during physical contact and particularly following vaginal stimulation. Oxytocin has been implicated in mother‐infant bond formation. The present study tested the hypothesis that oxytocin participates in the partner preference component of pair bond formation in adult prairie voles. Ovariectomized female prairie voles were implanted with osmotic mini‐pumps releasing oxytocin (1–100 ng/h) or artificial cerebrospinal fluid (CSF). Pumps were implanted intracerebroventricularly or subcutaneously and females then were housed for 6 h with a male partner, followed by a preference test in which females could elect to spend time with either the partner or an unfamiliar male. Females in groups that received centrally‐administered oxytocin (10 or 100 ng/h), but not CSF, exhibited a significant preference for the partner present during infusion. The induction of a partner preference after oxytocin administration appeared specific for central oxytocin pathways as peripheral oxytocin administration was ineffective. Moreover, central administration of a selective oxytocin receptor antagonist inhibited the behavioral effect of exogenous oxytocin. These results suggest that oxytocin may be one factor contributing to the development of partner preferences in this monogamous rodent.
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Infusion of oxytocin into the brains of female prairie voles and vasopressin in males facilitated pair-bonding even in the absence of actual mating.
“Infusion of oxytocin into the brains of female prairie voles and vasopressin in males, for instance, facilitated pair-bonding even in the absence of actual mating (Cho et al. 1999; Insel and Hulihan 1995; Williams et al. 1994; Winslow et al. 1993).”
From Natural Selection, Childrearing, and the Ethics of Marriage (and Divorce): Building a Case for the Neuroenhancement of Human Relationships (2012) · cites this paper as Williams et al. 1994
The hormone-driven process of dopamine imprinting might be possible to trigger artificially, as has been demonstrated in voles.
“This hormone-driven process might be possible to trigger artificially, as has been demonstrated in voles (Williams et al. 1994).”
From Natural Selection, Childrearing, and the Ethics of Marriage (and Divorce): Building a Case for the Neuroenhancement of Human Relationships (2012) · cites this paper as Williams et al. 1994
In rats, 1-2 ng of oxytocin given intracerebroventricularly facilitates suckling-induced bursting, while maternal behavior requires about 400 ng; partner preference in voles requires 10-100 ng/h, and maternal behavior in sheep requires 5 μg intracerebroventricularly.
“In lactating rats, suckling evokes bursts of action potentials in oxytocin cells that result in pulsatile oxytocin secretion, and this bursting is facilitated by 1-2ng oxytocin i.c.v.(26).Effects on maternal behavior in the rat need much higher doses (~400ng) (4).Partner preference effects in voles require infusions of oxytocin at 10-100ng/h (5), and, to stimulate maternal behavior in sheep, it”
From Intranasal Oxytocin: Myths and Delusions (2016) · cites this paper as [5]
The findings are consistent with those in other mammals, particularly monogamous rodent species where oxytocin plays a critical role in pair-bond formation.
“These findings are consistent with those reported for other mammals, particularly monogamous rodent species in which OT has shown to play a critical role in the formation of pair-bonds (Cho et al., 1999; Insel and Hulihan, 1995; Williams et al., 1994).”
From Oxytocin during the initial stages of romantic attachment: Relations to couples’ interactive reciprocity (2012) · cites this paper as Williams et al., 1994
OT fibers are present in the NAcc of the naked mole rat.
“A recent study in the naked mole rat has shown OT fibers are present in the NAcc of this eusocial species as well [136].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [136]
ICV OT administration facilitated partner preference formation in female, but not male, prairie voles.
“ICV OT administration facilitated partner preference formation in female (Williams et al., 1994; Insel and Hulihan, 1995), but not in male (Winslow et al., 1993) prairie voles.”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Williams et al., 1994
OT plays a stronger role in partner preference in female prairie voles compared to males.
“OT plays a stronger role in partner preference in female prairie voles compared to males (Winslow et al., 1993; Williams et al., 1994; Insel and Hulihan, 1995; Liu et al., 2001).”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Williams et al., 1994
Female prairie vole mate preferences can be formed by oxytocin infusion and blocked by an oxytocin agonist.
“In terms of pair bonding, female prairie vole mate preferences can be formed by oxytocin infusion (Williams et al., 1994) and blocked by an oxytocin agonist (Insel and Hulihan, 1995).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Williams et al., 1994
Oxytocin is associated with maternal behavior and adult pair-bond formation (partner preference) behavior in rodents.
“Oxytocin (OT), a neuropeptide hormone found exclusively in mammals, is associated with maternal behavior (1,2) and adult pair-bond formation (partner preference) behavior (3,4) in rodents.”
From Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles (2013) · cites this paper as [3]
Oxytocin is primarily responsible for pair-bonding in female voles, while arginine vasopressin is responsible for pair-bonding in males.
“OT is primarily responsible for pair-bonding in female voles, with the related peptide arginine vasopressin (AVP) responsible for pair-bonding in males (3,30–33).”
From Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles (2013) · cites this paper as [3]
In prairie voles, oxytocin has extensive sex-specific effects, although in both sexes it is intimately involved in social behavior.
“In prairie voles, OT has been shown to have extensive sex-specific effects, although in both sexes it is intimately involved in social behavior.”
From Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles (2013) · cites this paper as [3]
Sex differences in responses to OT are pervasive in both adult voles and in single-dose developmental studies.
“While sex differences in responses to OT are pervasive in both adult voles (3,72) and in single-dose developmental studies (37,38,73)”
From Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles (2013) · cites this paper as [3]
Infusion of OT into the brain during cohabitation with a male accelerates the development of a partner preference.
“Infusion of OT into the brain during cohabitation with a male accelerates the development of a partner preference, while blocking OTR in the NAcc during mating prevents this behavior [14, 15].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [15]
Blocking OTR in the NAcc during mating prevents partner preference formation.
“Infusion of OT into the brain during cohabitation with a male accelerates the development of a partner preference, while blocking OTR in the NAcc during mating prevents this behavior [14, 15].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [15]
The brain OT system significantly contributes to pair bond formation, initially demonstrated in females.
“The brain OT system is significantly contributing to pair bond formation as has been demonstrated initially in females by Sue Carter’s group”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Williams et al. 1994
Oxytocin receptor signaling in the brain is critical for partner preference formation in female prairie voles.
“Early pharmacological studies revealed that OTR signaling in the brain is critical for partner preference formation in female prairie voles (Insel and Hulihan, 1995; Williams et al., 1994).”
From Central oxytocin receptors mediate mating-induced partner preferences and enhance correlated activation across forebrain nuclei in male prairie voles (2016) · cites this paper as Williams et al., 1994
Seminal studies in male-male and male-female rodent pairs have contributed to the notion of OT as a facilitator of affiliative behaviors.
“While seminal studies in male-male and male-female rodent pairs have contributed to the notion of OT as a facilitator of affiliative behaviors (Lukas et al., 2011, Williams et al., 1994, Witt et al., 1992), recent findings also provide evidence of antisocial effects of OT (van Anders et al., 2013, Bartz et al., 2011, Beery, 2015).”
From Wireless Optogenetic Stimulation of Oxytocin Neurons in a Semi-natural Setup Dynamically Elevates Both Pro-social and Agonistic Behaviors (2020) · cites this paper as Williams et al., 1994
Central administration of OXT reduces the duration required to form a stable pair bond.
“Central administration of OXT reduces the duration required to form a stable pair bond (Williams et al., 1994), while administration of an OXT antagonist (OXTA) inhibits pair-bond formation in prairie voles (Williams et al., 1994).”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Williams et al., 1994
Administration of an OXT antagonist inhibits pair-bond formation in prairie voles.
“Central administration of OXT reduces the duration required to form a stable pair bond (Williams et al., 1994), while administration of an OXT antagonist (OXTA) inhibits pair-bond formation in prairie voles (Williams et al., 1994).”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Williams et al., 1994
OT has been shown to regulate fundamental mechanisms underlying mate fidelity.
“OT has been shown to regulate fundamental mechanisms underlying mate fidelity.”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Williams et al., 1994
Central infusion of OT reduced the duration required to form a stable pair-bond in the socially monogamous prairie vole.
“Furthermore, central infusion of OT reduced the duration required to form a stable pair-bond in the socially monogamous prairie vole (Microtus ochrogaster; Williams et al., 1994).”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Williams et al., 1994
This behavioral pattern is consistent with findings in prairie voles that OT increases preferential associations with a pair-mate.
“This behavioral pattern is consistent with findings in prairie voles that OT increases preferential associations with a pair-mate (Williams et al., 1994; Cho et al., 1999).”
From Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers (2014) · cites this paper as Williams et al., 1994
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- Authors
- Williams, J. R., Insel, T. R., Harbaugh, C. R., & Carter, C. S.
- Affiliations
- University of Maryland, College Park (US)
- National Institute of Mental Health (US)
- Venue
- Journal of Neuroendocrinology
- Publisher
- Wiley
- Published
- 1994-06
- Volume
- 6
- Issue
- 3
- Pages
- 247-250
- ISSN
- 0953-8194 (ISSN-L)
- 1365-2826
- OpenAlex
- W1976495588
- Cited by
- 483
- References
- 26
- Citations by year
- 2026: 16 · 2025: 16 · 2024: 11 · 2023: 10 · 2022: 16 · 2021: 12 · 2020: 7 · 2019: 21 · 2018: 14 · 2017: 23 · 2016: 25 · 2015: 26 · 2014: 22 · 2013: 23 · 2012: 26
- FWCI
- 11.17
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- National Institutes of Health (5r01mh045836-03)
- National Institute of Mental Health (NIMH MH45836)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- oxytocin, mate preferences, pair bonding, Microtus ochrogaster, monogamy, intracerebroventricular administration, oxytocin receptor antagonist, social bonding
- MeSH terms
- Amino Acid Sequence, Animals, Arvicolinae, Female, Injections, Intraventricular, Injections, Subcutaneous, Male, Molecular Sequence Data, Ovariectomy, Oxytocin, Sexual Behavior, Animal, Receptors, Oxytocin
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