The DOI matches its Crossref record; 249 of the 249 references it cites were found in a registry or an index.
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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“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“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]
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“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]
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“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]
In the citing paper
“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]
In the citing paper
“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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Citations
Cites
Items 201–249 of 249
Lonstein, J. S. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00952-8 · Cited by 68
Lei, K., Cushing, B. S., Musatov, S., Ogawa, S., & Kramer, K. M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008931 · Cited by 67
Parent-Young Contact in Prairie and Meadow Voles
Wilson, S. C. (1982) · Journal of Mammalogy · doi:10.2307/1380642 · Cited by 67
The Study of Mammalian Cooperative Breeding
Solomon, N. G., & French, J. A. (1996) · Cambridge University Press eBooks · doi:10.1017/cbo9780511574634.002 · Cited by 66
Dudley, C. A., Rajendren, G. V., & Moss, R. L. (1992) · Molecular and Cellular Neuroscience · doi:10.1016/1044-7431(92)90034-y · Cited by 65
A Quantitative Description of Copulatory Behavior in Prairie Voles (Microtus ochrogaster)
Gray, G. D., & Dewsbury, D. A. (2008) · Brain Behavior and Evolution · doi:10.1159/000124368 · Cited by 65
Hume, J. M., & Wynne‐Edwards, K. E. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.04.001 · Cited by 65
Nesting Patterns of Adult Voles, Microtus montanus, in Field Populations
Jannett, F. J. (1982) · Journal of Mammalogy · doi:10.2307/1380450 · Cited by 64
Movement Indicators of Reproductive Events among Female Meadow Voles as Revealed by Radiotelemetry
Madison, D. M. (1978) · Journal of Mammalogy · doi:10.2307/1380147 · Cited by 62
Jansson, A., Goldstein, M., Tinner, B., Zoli, M., Meador‐Woodruff, J. H., Lew, J., Levey, A. I., Watson, S. J., Agnati, L. F., & Fuxé, K. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00317-0 · Cited by 61
Curtis, J. T., & Wang, Z. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00226-9 · Cited by 61
Self-citationCrenshaw, B. J., Vries, G. J. D., & Yahr, P. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903220412 · Cited by 59
Villalba, C., Boyle, P. A., Caliguri, E. J., & Vries, G. J. D. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1420 · Cited by 59
Hnatczuk, O. C., Lisciotto, C. A., DonCarlos, L. L., Carter, C. S., & Morrell, J. I. (1994) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1994.tb00558.x · Cited by 56
A Comparison of Living Singly and in Male‐female Pairs in the Prairie Vole, Microtus ochrogaster
Getz, L. L., & McGuire, B. (1993) · Ethology · doi:10.1111/j.1439-0310.1993.tb00444.x · Cited by 53
Wolff, J. O., & Dunlap, A. S. (2002) · Behavioural Processes · doi:10.1016/s0376-6357(02)00022-0 · Cited by 48
Schellinck, H. M., Smyth, C. E., Brown, R. E., & Wilkinson, M. (1993) · Developmental Brain Research · doi:10.1016/0165-3806(93)90094-q · Cited by 48
Inamura, K., Kashiwayanagi, M., & Kurihara, K. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00646.x · Cited by 48
Almond, R. E. A., Brown, G. R., & Keverne, E. B. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.009 · Cited by 47
Northcutt, K. V., Wang, Z., & Lonstein, J. S. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21148 · Cited by 46
Self-citationSocial Modulation of Corticosteroid Responses in Male Prairie Voles
DeVries, A. C., Taymans, S. E., & Carter, C. S. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51949.x · Cited by 45
Opposing Regulation of Pair Bond Formation by cAMP Signaling within the Nucleus Accumbens Shell
Aragona, B. J., & Wang, Z. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3216-07.2007 · Cited by 42
Self-citationWang, Z., & Insel, T. R. (1996) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60338-1 · Cited by 41
Self-citationElectrical activity of prefrontal cortex and ventral tegmental area during rat maternal behavior
Hernández-González, M., Navarro-Meza, M., Prieto-Beracoechea, C. A., & Guevara, M. Á. (2005) · Behavioural Processes · doi:10.1016/j.beproc.2005.06.002 · Cited by 40
Estrus induction in four species of voles (Microtus).
Taylor, S. A., Salo, A. L., & Dewsbury, D. A. (1992) · Journal of comparative psychology · doi:10.1037/0735-7036.106.4.366 · Cited by 40
Ophir, A. G., Phelps, S. M., Sorin, A. B., & Wolff, J. O. (2007) · Journal of Mammalogy · doi:10.1644/06-mamm-a-250r.1 · Cited by 40
Mitchell, J. B., & Gratton, A. P. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90687-3 · Cited by 39
Intraspecific aggression of Peromyscus leucopus
Rowley, M. H., & Christian, J. J. (1976) · Behavioral Biology · doi:10.1016/s0091-6773(76)90580-0 · Cited by 34
Ziegler, T. E., Jacoris, S., & Snowdon, C. T. (2004) · American Journal of Primatology · doi:10.1002/ajp.20061 · Cited by 33
Estrogen and the induction of lordosis in female and male prairie voles (Microtus ochrogaster)
Carter, C. (1987) · Hormones and Behavior · doi:10.1016/0018-506x(87)90031-6 · Cited by 32
Cushing, B. S., Okorie, U., & Young, L. J. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01097.x · Cited by 31
Piovanotti, M. R. A., & Vieira, M. L. (2004) · Behavioural Processes · doi:10.1016/j.beproc.2004.01.007 · Cited by 29
Terminals from the Rat Prefrontal Cortex Synapse on Mesoaccumbens VTA Neurons
CARR, D. B., & Sesack, S. R. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09299.x · Cited by 27
Curtis, J. T., & Wang, Z. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.04.012 · Cited by 24
Self-citationCavanaugh, B. L., & Lonstein, J. S. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.01958.x · Cited by 23
Lansing, S. W., & Lonstein, J. S. (2005) · Journal of Neurobiology · doi:10.1002/neu.20212 · Cited by 22
Hastings, N. B., Orchinik, M., Aubourg, M. V., & McEwen, B. S. (1999) · Endocrinology · doi:10.1210/endo.140.10.7050 · Cited by 21
YOUNG, L. J., WAYMIRE, K. G., NILSEN, R., MACGREGOR, G. R., WANG, Z., & INSEL, T. R. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51955.x · Cited by 20
Self-citationKramer, K. M., Perry, A. N., Golbin, D., & Cushing, B. S. (2009) · Behavioral Neuroscience · doi:10.1037/a0016927 · Cited by 19
Wang, Z., LIU, Y., Young, L. J., & Insel, T. R. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51954.x · Cited by 19
Self-citationUrocortin II increases spontaneous parental behavior in prairie voles (Microtus ochrogaster)
SAMUEL, P., Hostetler, C. M., & Bales, K. L. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.08.015 · Cited by 14
Vasopressin, maternal behavior, and pup well-being
Wideman, C. H., & Murphy, H. (1990) · Current Psychology · doi:10.1007/bf02686866 · Cited by 11
Roberts, R. L., & Carter, C. S. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51968.x · Cited by 9
The evolution and function of adult attachment: A comparative and phylogenetic analysis
Brumbaugh, C. C., Fraley, R. C., & Marks, M. (2005) · PsycEXTRA Dataset · doi:10.1037/e529412014-123 · Cited by 8
Neuronal activation in the caudal brainstem associated with mating by voles
Curtis, J. T., Berkley, K. J., & Wang, Z. X. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00175-7 · Cited by 7
Self-citationDevelopmental Exposure to Vasopressin Increases Aggression in Adult Prairie Voles
Stribley, J. M., & Carter, C. S. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/3077.003.0069 · Cited by 2
WOLF–BISON INTERACTIONS IN YELLOWSTONE NATIONAL PARK
Smith, D. W., Mech, L. D., Meagher, M., Clark, W. E., Jaffe, R., Phillips, M. K., & Mack, J. A. (2000) · Journal of Mammalogy · doi:10.1644/1545-1542(2000)081
Wang (1996) · doi:10.1002/(sici)1096-9861(19960318)366:4
Research works printed but not linked: 1
- [162]Miczek KA Winslow JT Greenshaw AJ Dourish CT Psychopharmacologic research on aggressive behavior Experimental Psychopharmacology Humana Press Clifton, NJ 1987 27 113
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Carter, C. S. (2014) · Annual Review of Psychology · doi:10.1146/annurev-psych-010213-115110 · Cited by 714
Olff, M., Frijling, J. L., Kubzansky, L. D., Bradley, B., Ellenbogen, M. A., Cardoso, C., Bartz, J. A., Yee, J. R., & van Zuiden, M. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.019 · Cited by 620
The neural mechanisms and circuitry of the pair bond
Walum, H., & Young, L. J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0072-6 · Cited by 353
Oxytocin, motivation and the role of dopamine
Love, T. M. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.06.011 · Cited by 369
Numan, M., & Young, L. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.015 · Cited by 355
Metadata
- 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
- 249
- 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
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › 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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