The neurobiology of pair bonding: Insights from a socially monogamous rodent
Open accessAbstract
The formation of enduring relationships between adult mates (i.e., pair bonds) is an integral aspect of human social behavior and has been implicated in both physical and psychological health. However, due to the inherent complexity of these bonds and the relative rarity with which they are formed in other mammalian species, we know surprisingly little about their underlying neurobiology. Over the past few decades, the prairie vole (Microtus ochrogaster) has emerged as an animal model of pair bonding. Research in this socially monogamous rodent has provided valuable insight into the neurobiological mechanisms that regulate pair bonding behaviors. Here, we review these studies and discuss the neural regulation of three behaviors inherent to pair bonding: the formation of partner preferences, the subsequent development of selective aggression toward unfamiliar conspecifics, and the bi-parental care of young. We focus on the role of vasopressin, oxytocin, and dopamine in the regulation of these behaviors, but also discuss the involvement of other neuropeptides, neurotransmitters, and hormones. These studies may not only contribute to the understanding of pair bonding in our own species, but may also offer insight into the underlying causes of social deficits noted in several mental health disorders.
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The bonding effects of oxytocin and vasopressin in prairie voles are mediated by dopamine release, particularly in the VTA and NAcc.
“Their effects on bonding are mediated via interactions with dopamine (DA) release, particularly in the ventral tegmental area (VTA) and nucleus accumbens (NAcc).”
From Oxytocin enhances brain reward system responses in men viewing the face of their female partner (2013) · cites this paper as [2]
Section 8, “Neurochemical/hormone interactions,” reports that oxytocin and vasopressin interact with dopamine systems in partner-preference formation, including oxytocin–dopamine receptor interactions in the NAcc. Section 4.3 reports increased NAcc dopamine during mating. The paper does not establish that both hormones’ bonding effects are mediated by dopamine release in the VTA and NAcc; its VTA discussion concerns other neurotransmitters, and its vasopressin–dopamine example involves the ventral pallidum. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn prairie voles, mating releases oxytocin or vasopressin, and these neuropeptides promote partner bond formation.
“In prairie voles, partner bonds are formed after the neuropeptides oxytocin (OXT) or arginine vasopressin (AVP) are released in the brain during mating.”
From Oxytocin enhances brain reward system responses in men viewing the face of their female partner (2013) · cites this paper as [2]
Section 4.2 reports increased oxytocin in the nucleus accumbens during sociosexual experience and evidence that both oxytocin and vasopressin promote partner preferences. It says mating-related changes in males *suggest* vasopressin release, rather than establishing that release as a fact; the claim also specifies mating where the oxytocin finding says sociosexual experience. (LLM, conf=0.83)
Experimental — accuracy not yet measuredThe parvocellular AVP/OT system is sexually dimorphic, steroid hormone sensitive, and fundamental for the coordination of affiliative and social behaviors including courtship, pair bonding, empathy, reciprocity, trust, and context-specific aggression.
“The parvocellular system sends projections to the median eminence and throughout the brain and is sexually dimorphic, steroid hormone sensitive, and fundamental for the coordination of affiliative and social behaviors including courtship, pair bonding, empathy, reciprocity, trust, and context-specific aggression (1–4).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [3]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredThe density of ERα markedly differs across prosocial and asocial species and is directly related to the degree to which individuals and species are prosocial.
“This view is consistent with the observation that the density of ERα markedly differs across prosocial and asocial species and is directly related to the degree to which individuals and species are prosocial (3, 137, 138).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [3]
Section 7 reports that increased ERα expression in male prairie voles was associated with reduced social affiliation and describes an inverse relationship between regional ERα expression and social behavior. It does not report marked ERα-density differences between prosocial and asocial species; the cross-species receptor comparisons in Section 3 concern other receptors. Page numbers are unavailable in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIn some mammalian species, oxytocin is involved in forming partner bonds through interaction with brain dopamine reward systems.
“The evolutionarily conserved neuropeptide oxytocin (OXT) is associated with the formation of partner bonds in some species via interactions with brain dopamine reward systems.”
From Oxytocin enhances brain reward system responses in men viewing the face of their female partner (2013) · cites this paper as [2]
Studies aimed at modeling the core phenotypes associated with ASDs in animals have focused on studying social and repetitive behaviors in mice and pair-bonding behaviors in the prairie vole.
“Studies aimed at modeling, in animals, the core phenotypes associated with ASDs have focused on studying social and repetitive behaviors in mice [530-532] and pair-bonding behaviors in the prairie vole (Microtus ochrogaster) [533,534].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [534]
There is abundant evidence to suggest that AVP neural circuits are crucial to pair bonding in male prairie voles.
“In addition to the role of OXT in the modulation of social behavior between pair-mates, there is abundant evidence to suggest that AVP neural circuits are crucial to pair bonding in male prairie voles (Lim and Young, 2004; Young et al., 2011).”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Young et al., 2011
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Individual Differences and Social Influences on the Neurobehavioral Pharmacology of Abused Drugs
Bardo, M. T., Neisewander, J. L., & Kelly, T. H. (2013) · Pharmacological Reviews · doi:10.1124/pr.111.005124 · Cited by 167 · see citing works
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
Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues
Yao, S., Bergan, J., Lanjuin, A., & Dulac, C. (2017) · eLife · doi:10.7554/elife.31373 · Cited by 151 · see citing works
Developmental experiences and the oxytocin receptor system
Bales, K. L., & Perkeybile, A. M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.013 · Cited by 142 · see citing works
Burkett, J. P., Spiegel, L. L., Inoue, K., Murphy, A. Z., & Young, L. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.117 · Cited by 133 · see citing works
Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships
Hurlemann, R., & Scheele, D. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.05.013 · Cited by 136 · see citing works
<scp>O</scp>xytocin modulation of neural circuits for social behavior
Marlin, B. J., & Froemke, R. C. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22452 · Cited by 130 · see citing works
Oxytocin, vasopressin, and the motivational forces that drive social behaviors
Caldwell, H. K., & Albers, H. E. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_390 · Cited by 129 · see citing works
Vasopressin, oxytocin, and social odor recognition
Wacker, D. W., & Ludwig, M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.08.014 · Cited by 112 · see citing works
Donovan, M., Mackey, C. S., Platt, G. N., Rounds, J., Brown, A. N., Trickey, D. J., Liu, Y., Jones, K. M., & Wang, Z. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100278 · Cited by 85 · see citing works
Self-citationSong, Z., Borland, J. M., Larkin, T. E., O’Malley, M., & Albers, H. E. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.09.001 · Cited by 101 · see citing works
Young, K. A., Liu, Y., Gobrogge, K. L., Wang, H., & Wang, Z. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4275-13.2014 · Cited by 99 · see citing works
Self-citationSalubrious effects of oxytocin on social stress-induced deficits
Smith, A. S., & Wang, Z. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.11.010 · Cited by 88 · see citing works
Self-citationModi, M. E., Inoue, K., Barrett, C. E., Kittelberger, K. A., Smith, D. G., Landgraf, R., & Young, L. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.35 · Cited by 82 · see citing works
Hicks, C., Jorgensen, W., Brown, C., Fardell, J., Koehbach, J., Gruber, C. W., Kassiou, M., Hunt, G. E., & McGregor, I. S. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02311.x · Cited by 73 · see citing works
Horie, K., Inoue, K., Suzuki, S., Adachi, S., Yada, S., Hirayama, T., Hidema, S., Young, L. J., & Nishimori, K. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.10.011 · Cited by 77 · see citing works
Antisocial oxytocin: Complex effects on social behavior
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Oxytocin and vasopressin: signalling, behavioural modulation and potential therapeutic effects
Rae, M., Lemos Duarte, M., Gomes, I., Camarini, R., & Devi, L. A. (2022) · British Journal of Pharmacology · doi:10.1111/bph.15481 · Cited by 72 · see citing works
Neuropeptide diversity and the regulation of social behavior in New World primates
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.004 · Cited by 66 · see citing works
The oxytocin receptor impairs ethanol reward in mice
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Endocrine Disruption of Vasopressin Systems and Related Behaviors
Patisaul, H. B. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00134 · Cited by 54 · see citing works
“In a study done in collaboration with Andrea Gore’s laboratory, we found that Wistar rats perinatally exposed to BPA research in voles has uncovered the significance of neuropeptidergic regulation of social behaviors including paternal care, pair bonding, and maternal aggression (3, 45).”
BackgroundResultA Neuroscientist’s Guide to the Vole
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Beyond “oxytocin = good”: neural complexities and the flipside of social bonds
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“The prairie vole (Microtus ochrogaster) is a monogamous rodent species showing enduring pair bonding between mates, biparental care, and the consoling behavior toward a distressed partner (Young and Wang, 2004; Aragona et al., 2006; Gobrogge et al., 2009; Young et al., 2011; Johnson and Young, 2015; Burkett et al., 20…”
BackgroundMarmosets treated with oxytocin are more socially attractive to their long-term mate
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Arai, A., Hirota, Y., Miyase, N., Miyata, S., Young, L. J., Osako, Y., Yuri, K., & Mitsui, S. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.08.022 · Cited by 21 · see citing works
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Wardwell, J., Watanasriyakul, W. T., Normann, M. C., Akinbo, O. I., McNeal, N., Ciosek, S., Cox, M., Holzapfel, N., Sujet, S., & Grippo, A. J. (2020) · Stress · doi:10.1080/10253890.2020.1724950 · Cited by 16 · see citing works
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Self-citationInducing partner preference in mice by chemogenetic stimulation of CA2 hippocampal subfield
Cymerblit-Sabba, A., Smith, A. S., Williams Avram, S. K., Stackmann, M., Korgan, A. C., Tickerhoof, M. C., & Young, W. S. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00061 · Cited by 14 · see citing works
Stetzik, L. A., Sullivan, A. W., Patisaul, H. B., & Cushing, B. S. (2018) · BMC Research Notes · doi:10.1186/s13104-018-3934-0 · Cited by 10 · see citing works
- Authors
- Young, K. A., Gobrogge, K. L., Liu, Y., & Wang, Z.
- Affiliations
- Florida State University (US)
- Corresponding author
- Wang, Zuoxin
- Venue
- Frontiers in Neuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2011-01
- Volume
- 32
- Issue
- 1
- Pages
- 53-69
- ISSN
- 0091-3022 (ISSN-L)
- PMC
- PMC3012750
- OpenAlex
- W2153712825
- Cited by
- 389
- References
- 251
- Citations by year
- 2026: 5 · 2025: 15 · 2024: 22 · 2023: 27 · 2022: 34 · 2021: 21 · 2020: 40 · 2019: 19 · 2018: 26 · 2017: 22 · 2016: 40 · 2015: 26 · 2014: 30 · 2013: 27 · 2012: 18
- FWCI
- 26.67
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Frontiers in Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R21MH083128, R21-MH83128, R01MH058616, F31-MH79600, F31MH079600, R01-MH-58616)
- National Institute on Drug Abuse (R01-DA19627, K02DA-23048, F31DA025570, K02DA023048, F31-DA25570, R01DA019627)
- 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
- pair bonding, Microtus ochrogaster, mate preferences, biparental care, vasopressin, oxytocin, dopamine, neuropeptides, neurotransmitters, hormones, social behavior
- MeSH terms
- Adult, Animals, Arvicolinae, Humans, Models, Biological, Nervous System Physiological Phenomena, Neurobiology, Pair Bond, Rodentia, Sexual Behavior, Animal, Social Behavior, Models, Animal
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