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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BackgroundThe Role of Early Life Experience and Species Differences in Alcohol Intake in Microtine Rodents
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BackgroundOxytocin via oxytocin receptor excites neurons in the endopiriform nucleus of juvenile mice
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Oxytocin and cardiometabolic interoception: Knowing oneself affects ingestive and social behaviors
Smith, J. A., Eikenberry, S. A., Scott, K. A., Baumer-Harrison, C., de Lartigue, G., de Kloet, A. D., & Krause, E. G. (2022) · Appetite · doi:10.1016/j.appet.2022.106054 · Cited by 10
Yamasue, H. (2023) · Peptides · doi:10.1016/j.peptides.2023.171133 · Cited by 9
Social experiences shape song preference learning independently of developmental exposure to song
Wall, E. M., & Woolley, S. C. (2024) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2024.0358 · Cited by 13
“In a number of species, mating can lead to learning and plasticity, especially in species in which mating induces the formation of pair bonds: selective, enduring, and often monogamous relationships [8–11].”
BackgroundNeumann, I. D. (2008) · Springer eBooks · doi:10.1007/978-3-540-79288-8_7 · Cited by 8
“It has been reported in the monogamous prairie vole that establishing social bonds involves neural reward systems, including dopamine and opioid circuitry (Nelson and Panksepp 1998; Young and Wang 2004).”
BackgroundShirakawa, Y. (2013) · Journal of Clinical Toxicology · doi:10.4172/2161-0495.1000161 · Cited by 8
“Although we have much progress in the understanding of kinship interaction and pair bonding mechanisms [7,19], neurobiological mechanism of peer social interaction development is still uncertain.”
BackgroundPhylogenesis of mammal sexuality. Analysis of the evolution of proximal factors
Wunsch, S. (2017) · Sexologies · doi:10.1016/j.sexol.2016.12.001 · Cited by 8
Ménard, S., Gelez, H., Girard-Bériault, F., Coria‐Ávila, G. A., & Pfaus, J. G. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112577 · Cited by 8
Neural Contributions of the Hypothalamus to Parental Behaviour
Orikasa, C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136998 · Cited by 8
“OT receptor expression [71], coupled with MCHR in the NAc has a synergistic effect on inherent rewarding, contributing to the execution of parental behaviour [72].”
BackgroundBarriers and Breakthroughs in Targeting the Oxytocin System to Treat Alcohol Use Disorder
Ryabinin, A. E., & Zhang, Y. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.842609 · Cited by 8
Fine-scale spatial patterns of genetic relatedness among resident adult prairie voles
Keane, B., Ross, S., Crist, T. O., & Solomon, N. G. (2015) · Journal of Mammalogy · doi:10.1093/jmammal/gyv128 · Cited by 8
“Prairie voles (Microtus ochrogaster) are socially monogamous rodents that typically form pair bonds (Carter and Getz 1993; Getz et al. 1993; Young and Wang 2004) and sometimes breed cooperatively (Solomon and Getz 1997).”
BackgroundExtended epigenotype in aRattus novergicus–Toxoplasma gondiiassociation
Vyas, A. (2015) · Communicative & Integrative Biology · doi:10.4161/19420889.2014.992743 · Cited by 8
Kelton-Locke, S. (2016) · Journal of Infant Child and Adolescent Psychotherapy · doi:10.1080/15289168.2016.1257239 · Cited by 8
“Specifically, the neural circuits of reward and motivation, including the mesocorticolimbic dopaminergic reward circuit (Young & Wang, 2004), and the interaction of oxytocin, arginine vasopressin (AVP) and dopamine are thought to facilitate maternal pair-bond and adult pair-mating formation…”
BackgroundTomaszycki, M. L., & Atchley, D. (2017) · Integrative and Comparative Biology · doi:10.1093/icb/icx043 · Cited by 8
McNeal, N., Watanasriyakul, W. T., Normann, M. C., Akinbo, O. I., Dagner, A., Ihm, E., Wardwell, J., & Grippo, A. J. (2019) · Autonomic Neuroscience · doi:10.1016/j.autneu.2019.03.003 · Cited by 9
Creating a Community of Caring within a School
Keown, S., & Carroll, R. (2020) · lnternational Electronic Journal of Elementary Education · doi:10.26822/iejee.2020459469 · Cited by 8
“Young and Wang (2004) link oxytocin with neuroendocrine and psychosocial stress reduction.”
BackgroundRogers, S. M. (2013) · Research and perspectives in neurosciences · doi:10.1007/978-3-319-02904-7_2 · Cited by 8
Social relationships of female Guinea baboons (Papio papio) in Senegal
Goffe, A. S. (2017) · doi:10.53846/goediss-6391 · Cited by 7
Pair bonding slows epigenetic aging and alters methylation in brains of prairie volesPreprint
Sailer, L. L., Haghani, A., Zoller, J. A., Li, C. Z., Ophir, A. G., & Horvath, S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.25.313775 · Cited by 7
Neuroendocrine mechanisms of social bonds and separation stress in rodents, dogs, and other species
Nagasawa, M., & Kikusui, T. (2021) · Current topics in behavioral neurosciences · doi:10.1007/7854_2021_257 · Cited by 7
Borland, J. M. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105809 · Cited by 8
“Mating experience results in an increase in the expression of c-Fos in the nucleus accumbens (core and shell were analyzed together) in male Prairie voles (Lim and Young, 2004).”
Neuroendocrine mechanisms contributing to the coevolution of sociality and communication
Freiler, M. K., & Smith, G. T. (2023) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2023.101077 · Cited by 8
Oxytocin and Vasopressin Blood Levels in People with Post-Traumatic Stress Disorder
Zayman, E. P., Karabulut, A. B., Özdemir, S., & Kartalcı, Ş. (2023) · ALPHA PSYCHIATRY · doi:10.5152/alphapsychiatry.2023.21628 · Cited by 7
“25,26 .”
Conditioned preferences: Gated by experience, context, and endocrine systems
Monari, P. K., Hammond, E. R., Zhao, X., Maksimoski, A. N., Petric, R., Malone, C. L., Riters, L. V., & Marler, C. A. (2024) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105529 · Cited by 8
“…Zhao et al., 2020), social interactions such as play (C. Zhao et al., 2020), mating (Pitchers et al., 2014), communication (Riters, 2012), bonding (Young and Wang, 2004), parental care (Mulligan et al., 2021), and even aggression (Far-rell and Wilczynski, 2006; Legrand, 1970; Martínez et al.,…”
BackgroundMonogamous pair bonding in genetic algorithm
Lim, T. Y., Al‐Betar, M. A., & Khader, A. T. (2015) · IEEE Congress on Evolutionary Computation (CEC) · doi:10.1109/cec.2015.7256869 · Cited by 7
“In nature, extrapair copulations or infidelity are commonly found in the monogamous species [12], [13].”
BackgroundMating systems, social behaviour and hormones
Goymann, W., & Hofer, H. (2010) · Springer eBooks · doi:10.1007/978-3-642-02624-9_16 · Cited by 7
Rodriguez, N. A., Legzim, K. M., Aliou, F., Al-Naimi, O. A. S., & Bamshad, M. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.10.002 · Cited by 7
“Prairie voles are ideal models for investigating the regulatory mechanisms of monogamous tendencies because they are small rodents that exhibit a variety of mating strategies in nature, and they can be easily studied under laboratory conditions (Aragona and Wang, 2004; Carter et al., 1995; Young and Wang, 2004).”
BackgroundNeural networks of human nature and nurture
Levine, D. S. (2008) · Desafíos (Universidad del Rosario) · Cited by 7
Ramírez-Rodríguez, R., Tecamachaltzi-Silvarán, M. B., Díaz-Estrada, V. X., Chena-Becerra, F., Herrera‐Covarrubias, D., Paredes-Ramos, P., Manzo, J. G., García, L. I., & Coria‐Ávila, G. A. (2017) · Behavioural Processes · doi:10.1016/j.beproc.2017.01.010 · Cited by 7
Dell’Anna, F., Llorente, M., Weiß, B., von Fersen, L., & Amici, F. (2019) · American Journal of Primatology · doi:10.1002/ajp.23078 · Cited by 7
“…for instance, food sharing typically occurs among individuals frequently engaging in other cooperative behaviors, such as grooming and coalitionary support (Langergraber, 2012), and it plays a key role in social bonding under the influence of oxytocin (Wittig et al., 2014; Young & Wang, 2004).”
BackgroundRothman, J. M., Vogel, E. R., & Blumenthal, S. A. (2013) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199659449.003.0011 · Cited by 7
Ménard, S., Gelez, H., Coria‐Ávila, G. A., & Pfaus, J. G. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105900 · Cited by 7
Roh, H. W., Cho, E. J., Son, S. J., & Hong, C. H. (2022) · Journal of Affective Disorders · doi:10.1016/j.jad.2022.08.117 · Cited by 6
Feldman, R. (2023) · Acta Paediatrica · doi:10.1111/apa.16676 · Cited by 7
Thebrain and behavior in childhood and adolescent anxiety disorders
Pine, D. S. (2011) · Cambridge University Press eBooks · doi:10.1017/cbo9780511994920.010 · Cited by 7
Hobcraft, J. (2009) · Biodemography and Social Biology · doi:10.1080/19485560903382460 · Cited by 7
“Careful study has provided very strong evidence that specific markers on the oxytocin (for females) and vasopressin (for males) receptor genes are linked to these differences in behavior (eg, Young 2003 ; Young and Wang 2004 ).”
BackgroundMale and female brain evolution is subject to contrasting selection pressures in primates
Dunbar, R. (2007) · BMC Biology · doi:10.1186/1741-7007-5-21 · Cited by 7
Pan, Y., Liu, Y., Lieberwirth, C., Zhang, Z., & Wang, Z. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.12.026 · Cited by 7
“Microtine rodents display diverse social organizations and thus offer an excellent comparative model for studying the effects of the social environment on physiology and behavior (Young and Wang, 2004; Young et al., 2011).”
BackgroundInfluentialOxytocin drives prosocial biases in favor of attractive people
Hurlemann, R., Scheele, D., Maier, W., & Schultz, J. (2017) · Behavioral and Brain Sciences · doi:10.1017/s0140525x16000510 · Cited by 7
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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