Cellular Mechanisms of Social Attachment
Abstract
Pharmacological studies in prairie voles have suggested that the neuropeptides oxytocin and vasopressin play important roles in behaviors associated with monogamy, including affiliation, paternal care, and pair bonding. Our laboratory has investigated the cellular and neuroendocrine mechanisms by which these peptides influence affiliative behavior and social attachment in prairie voles. Monogamous prairie voles have a higher density of oxytocin receptors in the nucleus accumbens than do nonmonogamous vole species; blockade of these receptors by site-specific injection of antagonist in the female prairie vole prevents partner preference formation. Prairie voles also have a higher density of vasopressin receptors in the ventral pallidal area, which is the major output of the nucleus accumbens, than montane voles. Both the nucleus accumbens and ventral pallidum are key relay nuclei in the brain circuits implicated in reward, such as the mesolimbic dopamine and opioid systems. Therefore, we hypothesize that oxytocin and vasopressin may be facilitating affiliation and social attachment in monogamous species by modulating these reward pathways.
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Oxytocin improves social affiliation and attachment and reduces anxiety and stress.
“the neuropeptide oxytocin (OT), which has been shown to improve social affiliation and attachment and to reduce anxiety and stress (Young et al., 2001;Donaldson and Young, 2008;Ross and Young, 2009;Insel, 2010).”
From Sex-specific effects of intranasal oxytocin on autonomic nervous system and emotional responses to couple conflict (2013) · cites this paper as Young et al., 2001
Prairie voles have higher densities of NAc oxytocin receptors than nonmonogamous vole species, and blocking NAc oxytocin receptors prevents partner-preference formation.
“prairie voles have higher densities of NAc oxytocin receptors than is found in nonmonogamous vole species, and blocking NAc oxytocin receptors prevents partner-preference formation [547].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [547]
In prairie voles, site-specific infusion of an oxytocin receptor antagonist into the nucleus accumbens or prefrontal cortex blocks partner preference formation.
“In prairie voles, site-specific infusion of an OXTR antagonist directly into the nucleus accumbens (NAcc) or the prefrontal cortex, two areas with dense OXTR binding, is sufficient to block the formation of a partner preference (18).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [18]
In prairie voles, OXTR is enriched in mesolimbic reward regions including the nucleus accumbens and prefrontal cortex, which are part of a neural network for pair bonding.
“In a socially monogamous rodent, the prairie vole (Microtus ochrogaster), OXTR is enriched in important MLR regions such as the nucleus accumbens (NAcc) and prefrontal cortex (PFC) that constitute part of a neural network for pair bonding (6, 8, 34).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [34]
The effects of OT on partner preference in female prairie voles could be located in the nucleus accumbens and prefrontal cortex, but these studies did not include males.
“the effects of OT on partner preference in females could be located in the nucleus accumbens and in the prefrontal cortex, but these studies did not include males”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Young et al., 2001
Partner preference formation in prairie voles is modulated by the VP system acting in the LS and ventral pallidum and by the OT system acting in the NAc and prefrontal cortex.
“partner preference formation in prairie voles is modulated by the VP system acting in the LS and ventral pallidum (Liu et al., 2001; Pitkow et al., 2001; Lim & Young, 2004) and by the OT system acting in the NAc and prefrontal cortex (Young et al., 2001; Liu and Wang, 2003).”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Young et al., 2001
OTR activation in the NAC and prefrontal cortex, but not the caudate-putamen, is necessary for pair bond formation in female prairie voles.
“OTR activation in the NAC and prefrontal cortex, but not the CP, is necessary for the formation of pair bonds in female prairie voles (Young et al 2001).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Young et al 2001
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 [14]
In female voles, OT plays a critical role in regulating the formation of a partner preference by activating OT receptors in the nucleus accumbens and prefrontal cortex.
“In female voles, OT plays a critical role in regulating the formation of a partner preference by activating OT receptors (OTR) in the nucleus accumbens (NAcc) and prefrontal cortex [10, 14].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [14]
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 [14]
A major advance in understanding mammalian prosocial behaviors came from seminal studies investigating the role of oxytocin in voles.
“A major advance in the current understanding of mammalian prosocial behaviors came from seminal studies that investigated the role of oxytocin (OXT) in voles, a neuropeptide that is well established to play critical roles in social and affiliative behaviors [9,10].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [10]
Direct infusion of an oxytocin receptor antagonist into the nucleus accumbens prevented pair bond formation in prairie voles.
“The critical importance of these receptors was subsequently established by demonstrating that direct infusion of an OXT receptor antagonist into the NAc prevented pair bond formation in prairie voles [10].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [10]
Blocking oxytocin receptors in the prefrontal cortex or nucleus accumbens prevents mating-induced partner preferences in female prairie voles.
“More specifically, blocking OTR in the prefrontal cortex (PFC) or nucleus accumbens (NA) prevents mating-induced partner preferences in females (Young et al., 2001).”
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 Young et al., 2001
Brain distribution of the oxytocin receptor significantly differs between monogamous prairie voles and polygamous montane voles, with high oxytocin receptor density in prelimbic cortex and nucleus accumbens being crucial for monogamous behavior.
“While the expression of OXT is similar among both species (11), brain distribution of the OXTR significantly differs between them, with high OXTR density in the prelimbic cortex and nucleus accumbens (NAcc) being crucial for the expression of monogamous behavior (12,13).”
From Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships (2016) · cites this paper as [13]
OXTR signaling in the nucleus accumbens plays a critical role for the formation of a preference for an individual.
“Furthermore, OXTR signaling in the NAc plays a critical role for the formation of a preference for an individual, and the density of NAc OXTR correlates with such preferences 27–29.”
From Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles (2022) · cites this paper as [27]
The density of NAc OXTR correlates with preferences for an individual.
“Furthermore, OXTR signaling in the NAc plays a critical role for the formation of a preference for an individual, and the density of NAc OXTR correlates with such preferences 27–29.”
From Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles (2022) · cites this paper as [27]
Application of oxytocin receptor antagonists into either the nucleus accumbens or prefrontal cortex can block mating-induced partner preferences in female prairie voles.
“Correspondingly, application of oxytocin receptor antagonists into either the nucleus accumbens or prefrontal cortex can block mating-induced partner preferences in female prairie voles (Young et al., 2001).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Young et al., 2001
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“Oxytocin, colloquially known as the “love hormone” has been associated with affiliative behavior between parents and infants, and between male and female partners (Young et al., 2001).”
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The oxytocin system in drug discovery for autism: Animal models and novel therapeutic strategies
Modi, M. E., & Young, L. J. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.010 · Cited by 218 · see citing works
Self-citationLife in groups: the roles of oxytocin in mammalian sociality
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Oxytocin and vasopressin: powerful regulators of social behavior
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Social Laughter Triggers Endogenous Opioid Release in Humans
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Variation in the Oxytocin Receptor Gene Is Associated with Pair-Bonding and Social Behavior
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Freeman, S. M., & Young, L. J. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12382 · Cited by 196 · see citing works
“Thus, it would be interesting to perform an experiment in marmosets analogous to the ones described above in prairie voles (18) demonstrating the prevention of pair-bond formation via site-specific blockade of OXTR in the NAcc.”
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Biological Aspects of Social Bonding and the Roots of Human Violence
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Deconstructing sociality, social evolution and relevant nonapeptide functions
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Selective amnesic effects of oxytocin on human memory
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King, L. B., Walum, H., Inoue, K., Eyrich, N. W., & Young, L. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.008 · Cited by 191 · see citing works
“In a key region of the MLR, the NAc, OXTR activation is necessary for prairie vole partner preference formation (34), and OXTR variation mediates individual differences in pair bonding behaviors (36–38).”
Self-citationOxytocin and mutual communication in mother-infant bonding
Nagasawa, M., Okabe, S., Mogi, K., & Kikusui, T. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00031 · Cited by 202 · see citing works
Synchrony as an Adaptive Mechanism for Large‐Scale Human Social Bonding
Launay, J., Tarr, B., & Dunbar, R. (2016) · Ethology · doi:10.1111/eth.12528 · Cited by 202 · see citing works
Triune ethics: The neurobiological roots of our multiple moralities
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Decision Making: The Neuroethological Turn
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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
Self-citationNeural circuits of social behaviors: Innate yet flexible
Wei, D., Talwar, V., & Lin, D. (2021) · Neuron · doi:10.1016/j.neuron.2021.02.012 · Cited by 186 · see citing works
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Borderline personality disorder, mentalization, and the neurobiology of attachment
Fonagy, P., Luyten, P., & Strathearn, L. (2011) · Infant Mental Health Journal · doi:10.1002/imhj.20283 · Cited by 179 · see citing works
Histone deacetylase inhibitors facilitate partner preference formation in female prairie voles
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Making room for oxytocin in understanding depression
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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
Self-citationLim, M. M., Murphy, A. Z., & Young, L. J. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.10973 · Cited by 163 · see citing works
Self-citationOxytocin 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
Individual Differences and Social Influences on the Neurobehavioral Pharmacology of Abused Drugs
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Keebaugh, A. C., & Young, L. J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.07.018 · Cited by 154 · see citing works
Self-citationAnatomy and neurochemistry of the pair bond
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Self-citationPoindron, P., Lévy, F., & Keller, M. (2006) · Developmental Psychobiology · doi:10.1002/dev.20192 · Cited by 158 · see citing works
2006 Curt P. Richter award winner
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Microbiota‐gut‐brain axis as a regulator of reward processes
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Self-citationIs Love Passion an Addictive Disorder?
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The Central Vasopressinergic System: Examining the Opportunities for Psychiatric Drug Development
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The social brain: Neurobiological basis of affiliative behaviours and psychological well-being
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Social circuits and their dysfunction in autism spectrum disorder
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Adult attachment style is associated with cerebral μ‐opioid receptor availability in humans
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Oxytocin and social functioning
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- Authors
- Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R.
- Affiliations
- Emory University (US)
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2001-09
- Volume
- 40
- Issue
- 2
- Pages
- 133-138
- ISSN
- 0018-506X (ISSN-L)
- OpenAlex
- W2108858366
- Cited by
- 523
- References
- 31
- Citations by year
- 2026: 11 · 2025: 25 · 2024: 20 · 2023: 6 · 2022: 17 · 2021: 19 · 2020: 8 · 2019: 29 · 2018: 24 · 2017: 32 · 2016: 43 · 2015: 37 · 2014: 23 · 2013: 25 · 2012: 21
- FWCI
- 21.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- National Institutes of Health (5r03mh058824-02)
- National Institute of Mental Health (R03 MH58824, R29MH056897, R01MH056539)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- social attachment, monogamy, oxytocin, vasopressin, Microtus ochrogaster, montane vole, oxytocin receptor, vasopressin receptor, nucleus accumbens, ventral pallidum, affiliation, mate preferences, reward pathways, mesolimbic dopamine system, opioid system, neuroendocrine mechanisms
- MeSH terms
- Animals, Fathers, Female, Hormones, Humans, Male, Mammals, Peptides, Pregnancy, Steroids
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