The DOI matches its Crossref record; 77 of the 77 references it cites were found in a registry or an index.
The neurobiology of pair bonding.
Abstract
A neurobiological model for pair-bond formation has emerged from studies in monogamous rodents. The neuropeptides oxytocin and vasopressin contribute to the processing of social cues necessary for individual recognition. Mesolimbic dopamine is involved in reinforcement and reward learning. Concurrent activation of neuropeptide and dopamine receptors in the reward centers of the brain during mating results in a conditioned partner preference, observed as a pair bond. Differential regulation of neuropeptide receptor expression may explain species differences in the ability to form pair bonds. These and other studies discussed here have intriguing implications for the neurobiology of social attachment in our own species.
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In the citing paper
“Meta-analyses and systematic reviews indicate that a range of common therapies can indeed be effective in relieving couple distress in many situations [26, 27].”
From Could intranasal oxytocin be used to enhance relationships? Research imperatives, clinical policy, and ethical considerations (2013) · cites this paper as [26]
In the citing paper
“The hypothalamic peptide oxytocin (OXT) has been identified as a key modulator of pair-bonding in men, but its effects in women are still elusive.”
From Hormonal contraceptives suppress oxytocin-induced brain reward responses to the partner’s face (2016) · cites this paper as Young and Wang, 2004
In the citing paper
“A study injecting 3H-leucine into the SON found multiple extrahypothalamic projections, including olfactory bulb, amygdala, cingulum, and locus coeruleus [140].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [140]
In the citing paper
“which suggests that species-specific differences in neural distributions of OXTR can reflect the social organisation of the species (20,21).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [20]
In the citing paper
“OXTR signaling in the NAcc is required for mating-induced partner preference formation, a laboratory proxy of pair bonding (6).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [6]
In the citing paper
“OXTR affects a range of social behaviors in animals including maternal nurturing and bonding (1, 2), social reward and gregariousness (3, 4), social recognition (5), and pair bonding in monogamous species (6–8).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [6]
In the citing paper
“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 [6]
In the citing paper
“OXTR density is much higher in the NAcc of prairie voles than promiscuous vole species”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [6]
In the citing paper
“It is thought that the interface between oxytocin and the dopaminergic reward system may contribute to the success of mother-infant and pair-bonding processes [18,[75][76][77].”
From Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees (2014) · cites this paper as [76]
In the citing paper
“Our first studies of the role of the AVPR1a gene in social cognition exemplified by a simple laboratory paradigm converges with a wide range of both animal and human experimentation showing that arginine vasopressin (AVP) and the closely related oxytocin (OT) are key neuropeptides that facilitate social communication, affiliative behaviors and social cognition across mammals [6], [7] .”
From The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the dictator game and the social value orientations task (2009) · cites this paper as [7]
In the citing paper
“By contrast, other related vole species such as the meadow vole (M. pennsylvanicus) and the montane vole (M. montanus) are relatively asocial and do not readily form social bonds, providing a useful point of comparison for identifying neurobiological and genetic systems leading to diversity in social behaviors [2].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [2]
In the citing paper
“By contrast, other related vole species such as the meadow vole (M. pennsylvanicus) and the montane vole (M. montanus) are relatively asocial and do not readily form social bonds, providing a useful point of comparison for identifying neurobiological and genetic systems leading to diversity in social behaviors [2].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [2]
In the citing paper
“For example, socially monogamous male prairie voles have high densities of AVPR1A binding in the ventral pallidum, a major output of the NAcc, while non-mongamous vole species do not [2].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [2]
In the citing paper
“One of these socially monogamous mammals that has provided remarkable insights into the neural and neurogenetic mechanisms of social attachments is the prairie vole (Microtus ochrogaster)”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Young and Wang 2004
In the citing paper
“V1aR signaling in the ventral pallidum and LS promote partner preferences (149), while pair bond-induced aggression is mediated by V1aR in the lateral hypothalamus (43,150).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [149]
In the citing paper
“Because animal research has documented that OT is primarily a social bonding hormone that activates socio-emotional neural pathways in the brain 22,23 , we would also expect the effect of OT in humans to be limited to social situations where initiating or establishing partnership is important to realize synergy.”
From A registered replication study on oxytocin and trust (2020) · cites this paper as [23]
In the citing paper
“this finding fits with the crucial function of OT as a female hormone in labor, bonding and parenting both in human- [54], [4] and non-human mammals [55]”
From A direct examination of the effect of intranasal administration of oxytocin on approach-avoidance motor responses to emotional stimuli (2013) · cites this paper as [55]
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“Because mating and pregnancy strengthens pair bonds in prairie voles (Insel 6 et al., 1995; Williams et al., 1992; Winslow et al., 1993; Young and Wang, 2004), we 7 confirmed that females were pregnant.”
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“The NAcc is central to the social brain, especially through its contribution to the (social) reward 41 and bonding circuits 42 .”
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“Accumulating evidence from sophisticated animal models suggests that some of the complex regulatory effects of OXT are critically mediated by interactions with other neurotransmitter systems such that animal models demonstrated that dopamine partly mediated OXT’s effects on pair bonding (Young and Wang, 2004) while th…”
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“difference in the distribution of these receptors between sexes, pharmacological and transgenic manipulations have demonstrated that OXTR within the nucleus accumbens plays an important role in pair bonding in females, while AVPR1A within the ventral pallidum and lateral septum contributes to pair bond formation in ma…”
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“Prairie voles are rodents that form monogamous social bonds similar to humans (Carter, DeVries, & Getz, 1995; Carter & Getz, 1993; Young & Wang, 2004), display depression- and anxiety-relevant behaviors, and several physiological alterations following long-term social isolation (Grippo, Cushing, &…”
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“Formation and maintenance of pair bonds involve oxytocin and arginine vasopressin and their receptors as well as the dopaminergic system (Young and Wang, 2004).”
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“The Journal of Comparative Neurology | Research in Systems Neuroscience 523:335–358 (2015) 335 Additionally, the V1aR has attracted considerable interest because of its effects on mammalian social behavior (Young et al., 1999a,b; Young and Wang, 2004; Lim et al., 2004; Donaldson and Young, 2008).”
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“Several studies indicate that OXT is more important than AVP for female pair bonding [169].”
BackgroundPedersen, C. A., Chang, S. W. C., & Williams, C. L. (2014) · Brain Research · doi:10.1016/j.brainres.2014.07.033 · Cited by 17
“Supporting this contention are the OT and AVP dependence of pairbond formation in the monogamous prairie vole (Young and Wang, 2004) and marmosets (Smith et al., 2010), studies indicating OT regulation of social interactions in rhesus macaques (Chang et al., 2012; Parr et al., 2013; Ebitz et al.,…”
BackgroundKATAYAMA, M., Hirayama, T., Kiyono, T., Onuma, M., Tani, T., Takeda, S., Nishimori, K., & Fukuda, T. (2017) · Journal of Reproduction and Development · doi:10.1262/jrd.2016-164 · Cited by 15
“The prairie vole is a useful animal model with which to analyze social behaviors such as pair bonding [17, 18].”
BackgroundDhungel, S., Rai, D., Terada, M., Orikasa, C., Nishimori, K., Sakuma, Y., & Kondo, Y. (2018) · Neuroscience Research · doi:10.1016/j.neures.2018.11.008 · Cited by 15
Welling, L. L. M. (2014) · Evolutionary psychology · doi:10.1007/978-1-4939-0314-6_12 · Cited by 14
Birnbaum, G. E. (2015) · European Psychologist · doi:10.1027/1016-9040/a000237 · Cited by 18
Social modulation of learned behavior by dopamine in the basal ganglia: Insights from songbirds
Leblois, A. (2012) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2012.09.002 · Cited by 15
“As DA has been involved in the control of both complex motor (Wickens et al., 2003; Joshua et al., 2009) and social behaviors (Young and Wang, 2004; Skuse and Gallagher, 2009), songbirds offer a unique opportunity as a model system to study the role of DA signaling in the social modulation of a…”
BackgroundClock Gene Modulates Roles of OXTR and AVPR1b Genes in Prosociality
Ci, H., Wu, N., & Su, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109086 · Cited by 14
Reply: Does imitation act as an oxytocin nebulizer in autism spectrum disorder?
Aoki, Y. Y., & Yamasue, H. (2015) · Brain · doi:10.1093/brain/awv061 · Cited by 15
Sauer, C., Montag, C., Reuter, M., & Kirsch, P. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2018.06.005 · Cited by 13
Diabetes insipidus: vasopressin deficiency
Chasseloup, F., Tabarin, A., & Chanson, P. (2024) · Annales d'Endocrinologie · doi:10.1016/j.ando.2023.11.006 · Cited by 12
Form and function in systems neuroscience
Kristan, W. B., & Katz, P. (2006) · Current Biology · doi:10.1016/j.cub.2006.08.079 · Cited by 13
Vitale, E. M., Kirckof, A., & Smith, A. S. (2023) · Genes Brain & Behavior · doi:10.1111/gbb.12861 · Cited by 13
“13 Pair bonding in males and females is behaviorally documented by a selective affiliation for a social partner over other conspecifics, intruder-directed aggression, and social proximity-seeking following partner separation.”
BackgroundPfaus, J. G., Safron, A., & Zakreski, E. (2023) · Sexual Medicine Reviews · doi:10.1093/sxmrev/qead034 · Cited by 14
Evolution of the arginine vasopressin 1a receptor and implications for mammalian social behaviour
Heckel, G., & FINK, S. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00426-3 · Cited by 13
Does maternal oxytocin protect the fetal brain?
Brown, C. H., & Grattan, D. R. (2007) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2007.04.003 · Cited by 13
Powell, J. M., Inoue, K., Wallace, K. J., Seifert, A. W., Young, L. J., & Kelly, A. M. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02581-z · Cited by 13
“Comparative and experimental studies have revealed that differences in OXTR and AVPR1A neuroanatomical distributions reflect differences in social phenotype observed both across and within species (Caldwell 2017; Goodson et al. 2009; Young and Wang 2004; Campbell et al. 2009).”
Sexual coordination in a whole-brain map of prairie vole pair bonding
Gustison, M. L., Muñoz-Castañeda, R., Osten, P., & Phelps, S. M. (2023) · eLife · doi:10.7554/elife.87029 · Cited by 16
“The neurobiology of bonding is most studied in the prairie vole, a socially monogamous rodent in which females and males form bonds, share a nest, and raise young together ( Lieberwirth and Wang, 2014 ; Young and Wang, 2004 ).”
BackgroundResultSex Differences in Jealousy: A Population-Based Twin Study in Sweden
Walum, H., Larsson, H., Westberg, L., Lichtenstein, P., & Magnusson, P. K. E. (2013) · Twin Research and Human Genetics · doi:10.1017/thg.2013.57 · Cited by 13
“Studies in voles have shown neuropeptides vasopressin (AVP) and oxytocin (OT) to be key molecules in the facilitation of pair-bond formation in males and females respectively (Young & Wang, 2004).”
BackgroundMolecular characterization and brain distribution of the progesterone receptor in whiptail lizards
O’Connell, L. A., Matthews, B. J., Patel, S. B., O’Connell, J. D., & Crews, D. P. (2010) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2010.12.010 · Cited by 13
“Secondly, many studies indicate that the mesolimbic ‘‘reward’’ system (including the mid-brain dopaminergic system) is the neural network where the evaluation of stimulus salience takes place [14,69,75].”
The social neuroscience and the theory of integrative levels
Bello‐Morales, R., & Delgado-Garcia, J. M. (2015) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2015.00054 · Cited by 14
“Oxytocin has been involved in the modulation of a wide variety of behaviors in mammals, and humans in particular, such as aggression, affiliation or social memory (Young and Wang, 2004; Lee et al., 2009; Ross and Young, 2009), and its role in social cognition in humans has been the focus of extensive research in recen…”
BackgroundDarting, anesthesia, and handling
Glander, K. E. (2013) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199659449.003.0003 · Cited by 13
Yohn, C. N., Leithead, A. B., & Becker, E. A. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.03.008 · Cited by 12
“…distribution of AVP immunoreactive (AVP-ir) cells in the BNST, paraventricular nucleus (PVN), and supraoptic nucleus (SON), regions associatedwith aggression (Engelmann et al., 2000; Frazier et al., 2006; Young and Wang, 2004) and hypothalamuspituitary-adrenal (HPA) function, (Merali et al., 2006).”
BackgroundMethodDai, J., Chen, Y., & Sakata, J. T. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.03.032 · Cited by 13
Bozdoğan, S. T., Kütük, M. Ö., Tufan, A. E., Altıntaş, Z. M., Temel, G. Ö., & Toros, F. (2018) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2018.16.1.415 · Cited by 13
The 4 D’s of Pellagra and Progress
Williams, A. C., & Hill, L. J. (2020) · International Journal of Tryptophan Research · doi:10.1177/1178646920910159 · Cited by 13
Martin, T. J., Sexton, T., Kim, S. A., Severino, A. L., Peters, C. M., Young, L. J., & Childers, S. R. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.10.047 · Cited by 13
“Prairie voles also, like humans, engage in alloparental behavior with both male and female involved in rearing of the young (Young et al., 2001, Young and Wang, 2004, Ahern and Young, 2009, Ahern et al., 2011).”
Awake Canine fMRI Predicts Dogs’ Preference for Praise Versus FoodPreprint
Cook, P. F., Prichard, A., Spivak, M., & Berns, G. S. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/062703 · Cited by 14
Murta, V., Seiffe, A., & Depino, A. M. (2023) · Sexes · doi:10.3390/sexes4030024 · Cited by 13
“While both neuropeptides are pro-social in both sexes [245], AVP is more involved in the expression of male social behaviors, such as scent marking, aggression, parental behavior, pair bonding, and social recognition (reviewed in [246]), while OT is essential for the manifestation of many female…”
Borland, J. M. (2025) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2025.101175 · Cited by 13
Black, A. M., Komatsu, N., Zhao, J., Taskey, S. R., Serrano, N. S., Sharma, R., Manoli, D. S., Landry, M. P., & Beery, A. K. (2025) · Current Biology · doi:10.1016/j.cub.2025.07.042 · Cited by 14
Learning through the ages: How the brain adapts to the social world across development
Nelson, E. E. (2017) · Cognitive Development · doi:10.1016/j.cogdev.2017.02.013 · Cited by 13
Latzman, R. D., Schapiro, S. J., & Hopkins, W. D. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00407 · Cited by 14
“For example, AVPR1A, the vasopressin V1A receptor gene, has been shown to be related to several social behaviors including pair bonding, territoriality, and aggression among voles, particularly males (e.g., Young and Wang, 2004; Hammock and Young, 2005, 2006).”
BackgroundTeed, A. R., Han, K., Rakic, J., Mark, D. B., & Krawczyk, D. C. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.04.014 · Cited by 13
Asadi, E., Khodagholi, F., Asadi, S., Kamsorkh, H. M., Kaveh, N., & Maleki, A. (2021) · Brain Research · doi:10.1016/j.brainres.2021.147568 · Cited by 13
Individual differences in social attachment: A multi‐disciplinary perspective
Gustison, M. L., & Phelps, S. M. (2022) · Genes Brain & Behavior · doi:10.1111/gbb.12792 · Cited by 15
“In the NAMA model, for example, the affective networks derived from human studies map well onto networks implicated in animal bonding.(31,189) For example, the “approach module” outlined by the NAMA model includes the ventral striatum, prefrontal cortex, orbitofrontal cortex and the ventral tegmental area/substantia n…”
MethodPutnam, P. T., & Chang, S. W. C. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0047 · Cited by 13
“The classic prairie vole (Microtus ochrogaster) model of pair-bonding has been demonstrated to be mediated not just by oxytocin receptors in the nucleus accumbens [37–39,41], but also by mesolimbic dopamine circuits in the reward centres of the brain to create a conditioned partner preference [39,65].”
BackgroundMate Selection, Sexual Orientation, and Pair Bonding
Balthazart, J., & Young, L. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00048-x · Cited by 12
Iwata, E., Nagai, Y., & Sasaki, H. (2010) · The Open Fish Science Journal · doi:10.2174/1874401x01003010147 · Cited by 12
“Both AVP and OT are important for social recognition in rats and mice [15], and one study has shown that these peptides are involved in pair-bond formation in monogamous prairie voles [16].”
BackgroundSobrian, S., & Holson, R. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00066 · Cited by 14
“Moreover, AVP V1a receptor antagonist selectively blocks aggressive behavior in hamsters (Ferris et al., 2006), and there appears to be an association between Avpr-1a receptor gene and partner preference in the male prairie vole (Young and Wang, 2004).”
BackgroundL'attachement. De Konrad Lorenz à Larry Young : de l'éthologie à la neurobiologie
Lambert, N., & Lotstra, F. (2005) · Cahiers critiques de thérapie familiale et de pratiques de réseaux · doi:10.3917/ctf.035.0083 · Cited by 14
Metadata
- Authors
- Young, L. J., & Wang, Z.
- Affiliations
- Emory University (US)
- Florida State University (US)
- Corresponding author
- Young, Larry J
- Venue
- Nature Neuroscience
- Published
- 2004-09-26
- Volume
- 7
- Issue
- 10
- Pages
- 1048-1054
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2055445652
- Cited by
- 1,523
- References
- 76
- Citations by year
- 2026: 42 · 2025: 63 · 2024: 54 · 2023: 64 · 2022: 62 · 2021: 65 · 2020: 73 · 2019: 60 · 2018: 83 · 2017: 85 · 2016: 99 · 2015: 96 · 2014: 86 · 2013: 106 · 2012: 85
- FWCI
- 6.10
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- pair bonding, monogamy, oxytocin, vasopressin, mesolimbic dopamine system, reward learning, social attachment, individual recognition, social behavior
- MeSH terms
- Animals, Brain, Dopamine, Humans, Neural Pathways, Neuropeptides, Pair Bond, Reward, Receptors, Neuropeptide, Models, Animal
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