Neurobiological mechanisms of social attachment and pair bonding
Open accessAbstract
Species have evolved diverse social behavior and mating strategies in response to selective forces in their environments. While promiscuity is the predominant mating strategy across most vertebrate taxa, convergent evolution of monogamous mating systems has occurred multiple times across distant lineages. Monogamous behavior is thought to be facilitated by a neurobiological capacity to form and maintain selective social attachments, or pair bonds, with a mating partner. The neural mechanisms of pair bonding behavior have been investigated most rigorously in Microtine rodents, which exhibit diverse social organizations. These studies have highlighted mesolimbic dopamine pathways, social neuropeptides (oxytocin and vasopressin), and other neural systems as integral factors in the formation, maintenance, and expression of pair bonds.
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In monogamous prairie voles, oxytocin and vasopressin interact with the dopamine system to facilitate pair bond formation between mates.
“In monogamous prairie voles (Microtus ochrogaster), OT and AVP interact with the dopamine system to facilitate the formation of pair bonds between mates (2,6).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [6]
Oxytocin receptor signaling influences several social behaviors in animals, including maternal care and bonding, social reward and gregariousness, social recognition, and pair bonding in monogamous species.
“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 [8]
In prairie voles, OXTR is enriched in mesolimbic reward regions including the nucleus accumbens and prefrontal cortex, which are part of a neural network for pair bonding.
“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 [8]
Central OTRs exhibit extraordinarily diverse expression patterns that are associated with individual and species differences in social behavior.
“Central OTRs exhibit extraordinarily diverse expression patterns that are associated with individual and species differences in social behavior.”
From Oxytocin receptors modulate a social salience neural network in male prairie voles (2017) · cites this paper as Johnson and Young, 2015
Central distribution patterns and region-specific densities of OTRs have undergone rapid evolutionary divergence between closely related species of birds and mammals that exhibit divergent social behavior.
“Central distribution patterns and region-specific densities of OT receptors (OTRs) have undergone rapid evolutionary divergence between closely related species of birds and mammals that exhibit divergent social behavior”
From Oxytocin receptors modulate a social salience neural network in male prairie voles (2017) · cites this paper as Johnson and Young, 2015
In mammals, oxytocin modulates pair bonding behaviors in monogamous species.
“pair bonding behaviors in monogamous species (Hurlemann and Scheele, 2015; Johnson and Young, 2015; Ross and Young, 2009)”
From Central oxytocin receptors mediate mating-induced partner preferences and enhance correlated activation across forebrain nuclei in male prairie voles (2016) · cites this paper as Johnson and Young, 2015
Oxytocin facilitates social bonding behaviors by modulating neural transmission and encoding of social information across sensory and reward processing brain areas.
“It has been hypothesized that OT facilitates social bonding behaviors by modulating neural transmission and encoding of social information across sensory and reward processing brain areas (Johnson and Young, 2015; Numan and Young, 2015).”
From Central oxytocin receptors mediate mating-induced partner preferences and enhance correlated activation across forebrain nuclei in male prairie voles (2016) · cites this paper as Johnson and Young, 2015
Central oxytocin receptor signaling facilitates social bond formation by coordinating activity across a pair bonding neural network.
“These results are consistent with the hypothesis that central OTR signaling facilitates social bond formation by coordinating activity across a pair bonding neural network.”
From Central oxytocin receptors mediate mating-induced partner preferences and enhance correlated activation across forebrain nuclei in male prairie voles (2016) · cites this paper as Johnson and Young, 2015
The MeA, AON, PFC, NA, PVN and BLA are part of a hypothesized neural network underlying mating-induced pair bonds in prairie voles.
“The MeA, AON, PFC, NA, PVN and BLA are part of a hypothesized neural network underlying mating induced pair bonds in prairie voles (Johnson and Young, 2015; Numan and Young, 2015).”
From Central oxytocin receptors mediate mating-induced partner preferences and enhance correlated activation across forebrain nuclei in male prairie voles (2016) · cites this paper as Johnson and Young, 2015
Species differences in social relationships are not restricted to the oxytocin system per se but extend to other signaling pathways, including dopamine and arginine vasopressin, and their reciprocal interactions.
“However, accumulating evidence suggests that species differences in social relationships are not restricted to the OXT system per se but extend to other signaling pathways, including dopamine (DA) and argininevasopressin (AVP), and their reciprocal interactions (14,15).”
From Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships (2016) · cites this paper as [15]
The distribution of OT-ergic and AVP-ergic neurons and cellular receptors for OT and AVP have been well characterized in rodents and other vertebrates, with substantial overlap with the social behavior network.
“The distribution of OT-ergic and AVP-ergic neurons, and cellular receptors for OT (OTR) and AVP (V1aR, V1bR, V2R) have been well characterized in rodents (Albers, 2015; Johnson and Young, 2015) and other vertebrates (Goodson and Kabelik, 2009; O’Connell and Hofmann, 2012, 2011), and this distribution includes substantial overlap with the social behavior network (SBN; Newman, 1999).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Johnson and Young, 2015
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Specificity in Sociality: Mice and Prairie Voles Exhibit Different Patterns of Peer Affiliation
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Oxytocin and vasopressin: signalling, behavioural modulation and potential therapeutic effects
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Neuropeptide diversity and the regulation of social behavior in New World primates
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Thalamic integration of social stimuli regulating parental behavior and the oxytocin system
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Self-citationOxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys
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Modulation of social behavior by distinct vasopressin sources
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Sniff and mimic–Intranasal oxytocin increases facial mimicry in a sample of men
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We’re Not That Choosy: Emerging Evidence of a Progression Bias in Romantic Relationships
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Adult Attachment System Links With Brain Mu Opioid Receptor Availability In Vivo.
Turtonen, O., Saarinen, A., Nummenmaa, L., Tuominen, L., Tikka, M., Armio, R., Hautamäki, A., Laurikainen, H., Raitakari, O., Keltikangas-Järvinen, L., et al. (2020) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2020.10.013 · Cited by 81 · see citing works
Horie, K., Inoue, K., Nishimori, K., & Young, L. J. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.08.023 · Cited by 46 · see citing works
“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…”
BackgroundSelf-citationSeptal oxytocin administration impairs peer affiliation via V1a receptors in female meadow voles
Anacker, A. M. J., Christensen, J. D., LaFlamme, E. M., Grunberg, D. M., & Beery, A. K. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.02.025 · Cited by 44 · see citing works
Ludmer, J. A., González, A., Kennedy, J. L., Masellis, M., Meinz, P., & Atkinson, L. R. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.04.006 · Cited by 45 · see citing works
One cranium, two brains not yet introduced: Distinct but complementary views of the social brain
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Mustoe, A. C., Harnisch, A. M., Hochfelder, B., Cavanaugh, J., & French, J. A. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.01.025 · Cited by 40 · see citing works
Frank Beach award winner: Neuroendocrinology of group living
Beery, A. K. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.11.002 · Cited by 36 · see citing works
Oxytocin increases eye-gaze towards novel social and non-social stimuli
Eckstein, M., Bamert, V., Stephens, S. B. Z., Wallen, K., Young, L. J., Ehlert, U., & Ditzen, B. (2018) · Social Neuroscience · doi:10.1080/17470919.2018.1542341 · Cited by 36 · see citing works
Self-citationInterplay between the oxytocin and opioid systems in regulating social behaviour
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Endothelin neurotransmitter signalling controls zebrafish social behaviour
Gutiérrez, H. C., Colanesi, S., Cooper, B., Reichmann, F., Young, A. M. J., Kelsh, R. N., & Norton, W. (2019) · Scientific Reports · doi:10.1038/s41598-019-39907-7 · Cited by 34 · see citing works
Beyond romance: Neural and genetic correlates of altruism in pair-bonds.
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Rogers Flattery, C. N., Coppeto, D. J., Inoue, K., Rilling, J. K., Preuss, T. M., & Young, L. J. (2022) · Brain Structure and Function · doi:10.1007/s00429-021-02369-7 · Cited by 31 · see citing works
Self-citationUlloa, M., Portillo, W., Díaz, N. F., Young, L. J., Camacho, F. J., Rodríguez, V. M., & Paredes, R. G. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.10.015 · Cited by 31 · see citing works
Self-citationOxytocin, vasopressin and social behavior in the age of genome editing: a comparative perspective
Boender, A. J., & Young, L. J. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104780 · Cited by 30 · see citing works
Self-citationFish as a model in social neuroscience: conservation and diversity in the social brain network
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Partner Loss in Monogamous Rodents: Modulation of Pain and Emotional Behavior in Male Prairie Voles
Osako, Y., Nobuhara, R., Arai, Y.-C. P., Tanaka, K., Young, L. J., Nishihara, M., Mitsui, S., & Yuri, K. (2017) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000524 · Cited by 31 · see citing works
Self-citationBridging the gap between rodents and humans: The role of non‐human primates in oxytocin research
Putnam, P. T., Young, L. J., & Gothard, K. M. (2018) · American Journal of Primatology · doi:10.1002/ajp.22756 · Cited by 28 · see citing works
“Pair-bonding in these monogamous voles is critically dependent on the action of OT in specific brain circuits, including the nucleus accumbens and prefrontal cortex (Donaldson & Young,2008;Johnson&Young,2015,2017;Johnsonetal.,2016;Young & Wang, 2004).”
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Robinson, K. J., Twiss, S. D., Hazon, N., Moss, S. E. W., & Pomeroy, P. P. (2017) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.0554 · Cited by 27 · see citing works
Grabrucker, S., Pagano, J., Schweizer, J., Urrutia‐Ruiz, C., Schön, M., Thome, K., Ehret, G., Grabrucker, A. M., Zhang, R., Hengerer, B., et al. (2021) · The EMBO Journal · doi:10.15252/embj.2019104267 · Cited by 27 · see citing works
Evolutionary diversity as a catalyst for biological discovery
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Self-citationSocial zebrafish: Danio rerio as an emerging model in social neuroendocrinology
Kareklas, K., Teles, M. C., Nunes, A. R., & Oliveira, R. F. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13280 · Cited by 23 · see citing works
Oxytocin and positive couple interaction affect the perception of wound pain in everyday life
Pfeifer, A.-C., Schröder‐Pfeifer, P., Schneider, E., Schick, M., Heinrichs, M., Bodenmann, G., Ehlert, U., Herpertz, S. C., Läuchli, S., Eckstein, M., et al. (2020) · Molecular Pain · doi:10.1177/1744806920918692 · Cited by 23 · see citing works
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Neural and molecular mechanisms underlying female mate choice decisions in vertebrates
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Variation in social systems within Chaetodon butterflyfishes, with special reference to pair bonding
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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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Resting state brain networks in the prairie vole
Ortiz, J. J., Portillo, W., Paredes, R. G., Young, L. J., & Alcauter, S. (2018) · Scientific Reports · doi:10.1038/s41598-017-17610-9 · Cited by 18 · see citing works
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Chappell, A., Freeman, S. M., Lin, Y.-C., LaPrairie, J. L., Inoue, K., Young, L. J., & Hayes, L. D. (2016) · Journal of Zoology · doi:10.1111/jzo.12332 · Cited by 17 · see citing works
Self-citationEmerging Frontiers in Social Neuroendocrinology and the Study of Nonapeptides
Ondrasek, N. R. (2016) · Ethology · doi:10.1111/eth.12493 · Cited by 17 · see citing works
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A Role for Oxytocin-Like Receptor in Social Habituation in a Teleost
Weitekamp, C. A., Solomon‐Lane, T. K., Valle, P. D., Triki, Z., Nugent, B. M., & Hofmann, H. A. (2017) · Brain Behavior and Evolution · doi:10.1159/000464098 · Cited by 15 · see citing works
The Prairie Vole Model of Pair-Bonding and Its Sensitivity to Addictive Substances
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Blurring the Lines: Exploring the Work Spouse Phenomenon
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The Neurobiology and Genetics of Affiliation and Social Bonding in Animal Models
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An evolutionary case for polygyny to counter demographic collapse
Larsen, M. (2023) · Frontiers in Psychology · doi:10.3389/fpsyg.2023.1062950 · Cited by 10 · see citing works
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Smith, A. L., Walum, H., Connor‐Stroud, F., Freeman, S. M., Inoue, K., Parr, L. A., Goodman, M. M., & Young, L. J. (2016) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2016.10.035 · Cited by 9 · see citing works
Self-citationGenetic ancestry predicts male-female affiliation in a natural baboon hybrid zone
Fogel, A. S., McLean, E. M., Gordon, J. B., Archie, E. A., Tung, J., & Alberts, S. C. (2020) · Animal Behaviour · doi:10.1016/j.anbehav.2021.07.009 · Cited by 9 · see citing works
Social experiences shape song preference learning independently of developmental exposure to song
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Chova, P. E., Ferrer, E. E., Goetze, L. R., Dufek, M. E., Freeman, S. M., & Bales, K. L. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114334 · Cited by 7 · see citing works
- Authors
- Johnson, Z. V., & Young, L. J.
- Affiliations
- Emory University (US)
- Corresponding author
- Johnson, Zachary V
- Young, Larry J
- Venue
- Current Opinion in Behavioral Sciences
- Publisher
- Elsevier BV
- Published
- 2015-06
- Volume
- 3
- Pages
- 38-44
- ISSN
- 2352-1546 (ISSN-L)
- PMC
- PMC4486624
- OpenAlex
- W1963831028
- Cited by
- 169
- References
- 59
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 11 · 2023: 18 · 2022: 8 · 2021: 17 · 2020: 14 · 2019: 15 · 2018: 23 · 2017: 17 · 2016: 20 · 2015: 13
- FWCI
- 3.79
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Current Opinion in Behavioral Sciences (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (R01MH096983, 1P50MH100023, OD P51OD11132)
- 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 › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- pair bonding, social attachment, monogamy, monogamous mating system, mesolimbic dopamine system, oxytocin, vasopressin, microtine rodents, mating strategies, convergent evolution
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