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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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.
In the citing paper
“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.
In the citing paper
“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]
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.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“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
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The Physiology of Reproduction
Legendre, M., & Jalabert, B. (1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-109-2-176_1 · Cited by 7,876
Massagué, J. (1998) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.67.1.753 · Cited by 7,571
Social Relationships and Health
House, J. S., Landis, K. R., & Umberson, D. (1988) · Science · doi:10.1126/science.3399889 · Cited by 7,073
Ecology, Sexual Selection, and the Evolution of Mating Systems
Emlen, S. T., & Oring, L. W. (1977) · Science · doi:10.1126/science.327542 · Cited by 6,230
Handbook of Chemical Neuroanatomy
Stern, C. D. (1986) · Neurochemistry International · doi:10.1016/0197-0186(86)90021-5 · Cited by 4,160
Oxytocin increases trust in humans
Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005) · Nature · doi:10.1038/nature03701 · Cited by 3,690
Dopamine receptors: from structure to function
MISSALE, C., NASH, S. R., ROBINSON, S. W., JABER, M., & CARON, M. G. (1998) · Physiological Reviews · doi:10.1152/physrev.1998.78.1.189 · Cited by 3,633
The Neuroendocrinology of Stress: A Never Ending Story
Lightman, S. L. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01711.x · Cited by 3,588
Dopamine, learning and motivation.
Wise, R. A. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1406 · Cited by 3,379
Blair, W. F., Hall, E. R., & Kelson, K. R. (1959) · The Southwestern Naturalist · doi:10.2307/3669094 · Cited by 2,485
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
Cited by
Sorted by citations
Oxytocin pathways and the evolution of human behavior
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
Oxytocin enhances brain reward system responses in men viewing the face of their female partner
Scheele, D., Wille, A., Kendrick, K. M., Stoffel-Wagner, B., Becker, B., Güntürkün, O., Maier, W., & Hurlemann, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314190110 · Cited by 340
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307
Dichter, G. S., Damiano, C. A., & Allen, J. A. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-19 · Cited by 299
Deconstructing sociality, social evolution and relevant nonapeptide functions
Goodson, J. L. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.12.005 · Cited by 206
Neurobiological mechanisms of social attachment and pair bonding
Johnson, Z. V., & Young, L. J. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.01.009 · Cited by 169
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
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
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
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
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
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
Oxytocin modulation of neural circuits for social behavior
Marlin, B. J., & Froemke, R. C. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22452 · Cited by 130
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
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
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
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
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
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
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
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
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
Antisocial oxytocin: Complex effects on social behavior
Beery, A. K. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.11.006 · Cited by 74
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
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
The oxytocin receptor impairs ethanol reward in mice
Bahi, A. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.11.046 · Cited by 55
Endocrine Disruption of Vasopressin Systems and Related Behaviors
Patisaul, H. B. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00134 · Cited by 54
“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
Kenkel, W. M., Gustison, M. L., & Beery, A. K. (2021) · Current Protocols · doi:10.1002/cpz1.175 · Cited by 52
Beyond “oxytocin = good”: neural complexities and the flipside of social bonds
van Anders, S. M., Goodson, J. L., & Kingsbury, M. A. (2013) · Archives of Sexual Behavior · doi:10.1007/s10508-013-0134-9 · Cited by 52
Kingsbury, M. A., & Wilson, L. C. (2016) · Integrative and Comparative Biology · doi:10.1093/icb/icw122 · Cited by 48
Horie, K., Inoue, K., Nishimori, K., & Young, L. J. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.08.023 · Cited by 46
“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
Cavanaugh, J., Huffman, M. C., Harnisch, A. M., & French, J. A. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00251 · Cited by 36
Young, K. A., Liu, Y., Gobrogge, K. L., Dietz, D. M., Wang, H., Kabbaj, M., & Wang, Z. (2011) · Brain Research · doi:10.1016/j.brainres.2010.09.109 · Cited by 27
Self-citationDay, N. F., Saxon, D., Robbins, A., Harris, L., Nee, E., Shroff-Mehta, N., Stout, K., Sun, J., Lillie, N., Burns, M., et al. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.191510 · Cited by 27
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
Wang, J., Tai, F., & Lai, X. (2014) · Neuropeptides · doi:10.1016/j.npep.2013.10.016 · Cited by 20
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
Chun, E. K., Donovan, M., Liu, Y., & Wang, Z. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100427 · Cited by 18
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
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
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review