A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles
Abstract
Previous studies have demonstrated that central administration of vasopressin but not oxytocin facilitates pair bonding in the monogamous male prairie vole. This study tested vasopressin and oxytocin in the formation of the female vole's preference for a particular male partner. Initial studies showed that in monogamous female prairie voles (but not in nonmonogamous congeners), mating was followed by a partner preference that endured for at least 2 weeks. Nonmating prairie vole females developed a partner preference following oxytocin infusions, but not after vasopressin or cerebrospinal fluid infusions. Females given a selective oxytocin antagonist showed normal mating behavior, yet failed to develop a partner preference. The vasopressin antagonist failed to block partner preference formation in mated females. These results suggest that oxytocin, released with mating, may be critical to formation of a partner preference in the female prairie vole; this contrasts to vasopressin, which appears to be more important for pair bonding in the male of this species.
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Sex differences in behavioral or brain responses were found after manipulations of the OXT brain system in voles and after intranasal OXT application in humans.
“Sex differences in behavioral or brain responses were also found after manipulations of the OXT brain system in voles (Insel & Hulihan, 1995) and after intranasal OXT application in humans (Kubzansky et al., 2012; Lische et al., 2012).”
From Sex-specific modulation of juvenile social play by vasopressin (2013) · cites this paper as Insel & Hulihan, 1995
Activation of D1-like dopamine receptors inhibits partner preference formation induced by either mating or by D2 activation.
“Activation of D1-like DA receptors inhibits partner preference formation induced by either mating or by D2 activation [63, 64].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [63]
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 Insel and Hulihan 1995
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 Insel and Hulihan, 1995
Sex-specific responses to AVP and OXT manipulations in rodents have been reported for behaviors other than juvenile social play, including aggression, partner preference, alloparental behavior, and social recognition.
“Sex-specific responses to AVP and OXT manipulations in rodents have been reported for behaviors other than juvenile social play, including aggression (Ferris and Potegal, 1988; Gutzler et al., 2010), partner preference (Insel and Hulihan, 1995; Cho et al., 1999; Bales et al., 2013), alloparental behavior (Bales et al., 2004), and social recognition (Bluthé and Dantzer, 1990; Engelmann et al., 1998”
From Sex-specific modulation of juvenile social play behavior by vasopressin and oxytocin depends on social context (2014) · cites this paper as Insel and Hulihan, 1995
In rodents, the VP system regulates partner preference in prairie voles in sex-specific ways.
“In rodents, sex-specific regulation of partner preference in prairie voles, social recognition in rats, social play in rats, and aggression in hamsters has been found”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Insel & Hulihan, 1995
ICV V1aR antagonist administration impaired partner preference in male voles only.
“ICV V1aR antagonist administration impaired partner preference in male voles only (Winslow et al., 1993; Insel & Hulihan, 1995)”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Insel & Hulihan, 1995
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 Insel and Hulihan, 1995
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 Insel and Hulihan, 1995
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 [72]
AVP, OT, and DA, along with their respective receptors, act within specific brain circuitry to facilitate social attachment in a gender-specific manner.
“These studies have demonstrated that arginine vasopressin (AVP), oxytocin (OT), and dopamine (DA), along with their respective receptors, act within specific brain circuitry to facilitate social attachment in a gender-specific manner [9].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [9]
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 Insel and Hulihan, 1995
Previous work suggested that the central OT system may modulate pair bonding in prairie voles in a sex-specific manner, with central OTRs modulating pair bonding in females but not in males.
“Previous work has suggested that the central OT system may modulate pair bonding in prairie voles in a sex-specific manner (Insel and Hulihan, 1995; Winslow and Insel, 1993), with central OTRs modulating pair bonding in females but not in males.”
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 Insel and Hulihan, 1995
The neuropeptide oxytocin (OT) is implicated in the modulation of many social responses.
“The neuropeptide oxytocin (OT) is implicated in the modulation of many social responses (Ross and Young, 2009; Insel and Hulihan, 1995; Ferguson et al., 2001; Dölen et al., 2013).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Insel and Hulihan, 1995
Gender-specific effects of OT have been documented numerously in prairie voles (Microtus ochrogaster) and are centrally-mediated based on ventricular peptide manipulation experiments.
“Such gender-specific effects of OT have been documented numerously in prairie voles (Microtus ochrogaster), and are verified to be centrally-mediated based on ventricular peptide manipulation experiments.”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Insel and Hulihan, 1995
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Bales, K. L., van Westerhuyzen, J. A., Lewis-Reese, A. D., Grotte, N. D., Lanter, J. A., & Carter, C. S. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.05.004 · Cited by 192 · see citing works
Johnson, Z. V., Walum, H., Jamal, Y. A., Xiao, Y., Keebaugh, A. C., Inoue, K., & Young, L. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.11.011 · Cited by 190 · see citing works
Crockford, C., Deschner, T., Ziegler, T. E., & Wittig, R. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00068 · Cited by 187 · see citing works
Choleris, E., Little, S. R., Mong, J. A., Puram, S. V., Langer, R., & Pfaff, D. W. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700670104 · Cited by 183 · see citing works
Wang, Z., Yu, G., Cascio, C., Liu, Y., Gingrich, B., & Insel, T. R. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.3.602 · Cited by 205 · see citing works
Histone deacetylase inhibitors facilitate partner preference formation in female prairie voles
Wang, H., Duclot, F., Liu, Y., Wang, Z., & Kabbaj, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3420 · Cited by 173 · see citing works
Making room for oxytocin in understanding depression
McQuaid, R. J., McInnis, O. A., Abizaid, A. B., & Anisman, H. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.07.005 · Cited by 172 · see citing works
Oxytocin, Vasopressin, and the Neuroendocrine Basis of Pair Bond Formation
Insel, T. R., Winslow, J. T., Wang, Z., & Young, L. J. (1998) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4871-3_28 · Cited by 170 · see citing works
Choleris, E., Ogawa, S., Kavaliers, M., Gustafsson, J.-Α., Korach, K. S., Muglia, L. J., & Pfaff, D. W. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00203.x · Cited by 173 · see citing works
The neurobiology of social recognition, approach, and avoidance
Young, L. J. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01268-9 · Cited by 172 · see citing works
Lim, M. M., Murphy, A. Z., & Young, L. J. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.10973 · Cited by 163 · see citing works
Oxytocin receptor density is associated with male mating tactics and social monogamy
Ophir, A. G., Gessel, A., Zheng, D.-J., & Phelps, S. M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.007 · Cited by 161 · see citing works
Sex-specific modulation of juvenile social play by vasopressin
Veenema, A. H., Bredewold, R., & De Vries, G. J. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.002 · Cited by 166 · see citing works
“Sex differences in behavioral or brain responses were also found after manipulations of the OXT brain system in voles (Insel & Hulihan, 1995) and after intranasal OXT application in humans (Kubzansky et al., 2012; Lischke et al., 2012).”
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Oxytocin and Social Relationships: From Attachment to Bond Disruption
Bosch, O. J., & Young, L. J. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_10 · Cited by 162 · see citing works
Anxiolytic-like effect of oxytocin in the simulated public speaking test
de Oliveira, D. C., Zuardi, A. W., Graeff, F. G., Queiroz, R. H., & Crippa, J. A. (2012) · Journal of Psychopharmacology · doi:10.1177/0269881111400642 · Cited by 154 · see citing works
Bredewold, R., Smith, C. J. W., Dumais, K. M., & Veenema, A. H. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00216 · Cited by 157 · see citing works
Endogenous oxytocin is involved in short-term olfactory memory in female rats
Engelmann, M., Ebner, K., Wotjak, C. T., & Landgraf, R. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00084-3 · Cited by 156 · see citing works
Bales, K. L., & Carter, C. S. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.4.854 · Cited by 155 · see citing works
- Authors
- Insel, T. R., & Hulihan, T. J.
- Affiliations
- National Institute of Mental Health (US)
- ORCID
- Insel, Thomas R.
- Venue
- Behavioral Neuroscience
- Published
- 1995-08
- Volume
- 109
- Issue
- 4
- Pages
- 782-789
- ISSN
- 0735-7044 (ISSN-L)
- 1939-0084
- OpenAlex
- W4236841827
- Cited by
- 528
- References
- 0
- Citations by year
- 2026: 13 · 2025: 16 · 2024: 20 · 2023: 16 · 2022: 20 · 2021: 12 · 2020: 27 · 2019: 12 · 2018: 26 · 2017: 23 · 2016: 30 · 2015: 19 · 2014: 30 · 2013: 21 · 2012: 22
- FWCI
- 17.73
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioral Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- oxytocin, pair bonding, mate preferences, monogamy, voles, sexual monogamy, social bonding, sex differences
- MeSH terms
- Animals, Copulation, Arvicolinae, Female, Male, Oxytocin, Pair Bond, Sexual Behavior, Animal, Sex Factors, Species Specificity, Vasopressins
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