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Cited by 162Neuroendocrine regulation and behaviorStress Responses and CortisolAttachment and Relationship Dynamics

Oxytocin and Social Relationships: From Attachment to Bond Disruption

Open access
Bosch, Oliver J., Young, Larry J.·2017·Current Topics in Behavioral Neurosciences
DOI 10.1007/7854_2017_10PMC PMC5815947
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Abstract

Social relationships throughout life are vital for well-being and physical and mental health. A significant amount of research in animal models as well as in humans suggests that oxytocin (OT) plays an important role in the development of the capacity to form social bonds, the mediation of the positive aspects of early-life nurturing on adult bonding capacity, and the maintenance of social bonding. Here, we focus on the extensive research on a socially monogamous rodent model organism, the prairie vole (Microtus ochrogaster). OT facilitates mating-induced pair bonds in adults through interaction with the mesolimbic dopamine system. Variation in striatal OT receptor density predicts resilience and susceptibility to neonatal social neglect in female prairie voles. Finally, in adults, loss of a partner results in multiple disruptions in OT signaling, including decreased OT release in the striatum, which is caused by an activation of the brain corticotropin releasing factor (CRF) system. The dramatic behavioral consequence of partner loss is increased depressive-like behavior reminiscent of bereavement. Importantly, infusions of OT into the striatum of adults prevents the onset of depressive-like behavior following partner loss, and evoking endogenous OT release using melanocortin agonists during neonatal social isolation rescues impairments in social bonding in adulthood. This work has important translational implications relevant to the disruptions of social bonds in childhood and in adults.

AI snapshot

Written from the paper’s full text.

TL;DR

This review synthesizes prairie vole research showing that oxytocin interacts with mesolimbic dopamine and CRF systems to facilitate pair bonds, shape resilience to early social neglect, and mediate the consequences of partner loss. It argues that oxytocin signaling in the nucleus accumbens is central to social attachment and has translational implications for bereavement and early-life social disruption.

Key findings

  • Oxytocin facilitates mating-induced pair bonds in adult prairie voles through interaction with the mesolimbic dopamine system; striatal oxytocin receptor density predicts resilience versus susceptibility to neonatal social neglect in female prairie voles. Females with naturally high nucleus accumbens OTR binding were resilient and formed partner preferences normally, whereas low-OTR females that experienced neglect failed to form partner preferences.
  • Neonatal social isolation (3 h daily from days 1–14 of life) impaired pair bond formation in adult female, but not male, prairie voles at ~90 days of age, even after 48 h of cohabitation with a male partner; treatment with the oxytocin system-stimulant Melanotan II rescued normal social attachments.
  • Partner loss in male prairie voles increased anxiety-related behavior for up to 4 weeks, increased passive stress-coping/depressive-like behavior, higher basal plasma corticosterone, adrenal hypertrophy, and autonomic changes. Separation decreased OT mRNA in the hypothalamic paraventricular nucleus at 5 days, reduced OTR binding in the NAc shell, and CRF-R2 activation reduced local OT release; chronic intra-NAc OT normalized passive stress-coping, while OTR antagonist or shRNA knockdown increased it.
  • The brain CRF system mediates partner-loss effects: CRF mRNA increased in the medial bed nucleus of the stria terminalis at 5 days and CRF immunoreactivity increased in the PVN at 4 weeks; CRF-R1 or CRF-R2 antagonists normalized passive stress-coping, whereas a CRF-R2 agonist increased it and reduced OT release in the NAc shell.

Methods

  • Narrative review of prairie vole (*Microtus ochrogaster*) literature, with comparisons to human studies; no new primary data are reported.
  • Describes the partner preference test: a three-chamber apparatus in which a pair bond is typically inferred when the experimental subject spends more than twice as much time in the chamber of, or huddling with, the familiar partner than with an unfamiliar stranger.
  • Synthesizes cited experimental paradigms including neonatal social isolation (3 h daily, days 1–14), adult pair-bond separation after 5 days of cohousing with testing 3–5 days or 2–4 weeks later, central/local infusions, viral vector OTR silencing, and melanocortin agonist treatment.

Limitations

  • The paper states no formal limitations section.
  • Evident from the text: it is a review relying heavily on an animal model, so translational implications for humans are inferential; human evidence for OT in pair bond formation is described as less consistent, with stronger evidence for maintenance.
  • Evident from the text: many findings are sex-specific or from male prairie voles, and the neonatal isolation effects on adult pair bonding were observed in females but not males, so generalization across sexes and species is uncertain.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1007/7854_2017_10

Cites

141 of 141 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 72 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    In prairie voles, partner loss increases CRF signaling in the brain.

    “Our research has shown that partner loss increases CRF signaling in the brain”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Prairie voles are the first model organisms to provide insights into the neural mechanisms associated with psychiatric phenotypes based on loss of a partner.
  • Findingown data

    In prairie voles, OTR in the NAc are reduced after partner loss.

    “OTR in the NAc are reduced”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Prairie voles are the first model organisms to provide insights into the neural mechanisms associated with psychiatric phenotypes based on loss of a partner.
  • Findingreasoning

    In prairie voles, partner loss leads to an impoverished OT environment, especially in the NAc.

    “which leads to an impoverished OT environment especially in the NAc”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Prairie voles are the first model organisms to provide insights into the neural mechanisms associated with psychiatric phenotypes based on loss of a partner.
  • Findingown data

    In prairie voles, the excitatory drive onto OT neurons is reduced after partner loss.

    “as is the excitatory drive onto OT neurons”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Prairie voles are the first model organisms to provide insights into the neural mechanisms associated with psychiatric phenotypes based on loss of a partner.
  • Premisenone given

    Partner loss increases depressive-like behavior reminiscent of bereavement.

    “The dramatic behavioral consequence of partner loss is increased depressive-like behavior reminiscent of bereavement.”
    Quote in the paperSubstantial claim
  • May combine two claims. 20

  • May combine two claims.

    Premisecitation

    In both sexually naïve male and female prairie voles, mating facilitates partner preferences; longer durations of cohabitation without mating can also result in a pair bond.

    “In both sexually naïve male and female prairie voles, mating facilitates partner preferences; however, longer durations of cohabitation without mating can also result in a pair bond”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Williams et al. 1992 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    OT has been implicated in the onset of parental nurturing and maternal bonds, the consequences of parenting on the developing brain, pair bonding, empathy-based consoling behavior, and the consequences of social loss in animal models.

    “Specifically, the neuropeptide oxytocin (OT) has been implicated in the onset of parental nurturing and maternal bonds (Bosch and Neumann 2012; Numan and Young 2016; Rilling and Young 2014), the consequences of parenting on the developing brain (Champagne et al. 2001; Barrett et al. 2015), pair bonding (Johnson et al. 2016; Johnson and Young 2015), empathy-based consoling behavior (Burkett et al.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Bosch and Neumann 2012 source

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    • cites Burkett et al. 2016 source

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  • May combine two claims.

    Study design and conductcitation

    Prairie voles are amenable to laboratory experimentation, and pair bond assessment is made possible by a highly reliable, automatable partner preference test.

    “The prairie voles are amenable to laboratory experimentation, and the assessment of a pair bond is made possible by a highly reliable, automatable partner preference test”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Williams et al. 1992 source

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    • cites Ahern et al. 2009

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  • May combine two claims.

    Premisecitation

    The prairie vole is a socially monogamous mammal that has provided remarkable insights into the neural and neurogenetic mechanisms of social attachments.

    “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)”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Young and Wang 2004 source

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    • cites Ross and Young 2009

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  • May combine two claims.

    Premisecitation

    Single mother-reared animals, particularly females, have increased OT content in the hypothalamus and greater dorsal raphe CRF-R2 densities, and both measures correlated with licking and grooming experienced during the first 10 days of life.

    “single mother-reared animals, particularly females, have increased OT content in the hypothalamus and greater dorsal raphe CRF-R2 densities, and both measures correlated with licking and grooming experienced during the first 10 days of life”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ahern and Young 2009

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    CRF-R2 are abundantly expressed on OT neurons in the PVN and on OT fibers projecting to the NAc shell.

    “Importantly, CRF-R2 are abundantly expressed on OT neurons in the PVN as well as on its OT fibers projecting to the NAc shell”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Bosch et al. 2016 source

      Not checked in the free run.

    • cites Dabrowska et al. 2011 source

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  • May combine two claims.

    Premisecitation

    In humans there is less evidence that the OT system plays a role in pair bond formation, but the brain OT system seems important for its maintenance.

    “In contrast, in humans there is less evidence that the OT system plays a role in pair bond formation (e.g., Schneiderman et al. 2012), but the brain OT system does seem to be important for its maintenance (Hurlemann and Scheele 2016).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Schneiderman et al. 2012 source

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    • cites Hurlemann and Scheele 2016 source

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  • May combine two claims.

    Premisecitation

    Female prairie voles with naturally high densities of OTR binding in the NAc were resilient to disruptions in early-life attachment behaviors and formed partner preferences as adults normally.

    “those females with naturally high densities of OTR binding in the NAc were resilient to disruptions in early-life attachment behaviors and formed partner preferences as adults normally”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Barrett et al. 2015 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The depressive-like state after breaking the pair bond is accompanied by decreased parasympathetic and increased sympathetic drive to the heart, increased heart rate, adrenal hypertrophy, and higher basal plasma corticosterone concentration.

    “The depressive-like state after breaking the pair bond is accompanied by decreased parasympathetic and increased sympathetic drive to the heart in conjunction with increased heart rate (McNeal et al. 2014), adrenal hypertrophy (Bosch et al. 2009), and higher basal plasma corticosterone concentration”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites McNeal et al. 2014 source

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    • cites Bosch et al. 2009 source

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  • May combine two claims.

    Premisecitation

    Intranasal OT administration in men caused increased rating of their partners' attractiveness in pictures and heightened NAc activation.

    “intranasal OT administration in men caused them to increase the rating of their partners’ attractiveness in pictures as well as heightened NAc activation”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Scheele et al. 2013 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The brain OT system significantly contributes to pair bond formation, initially demonstrated in females.

    “The brain OT system is significantly contributing to pair bond formation as has been demonstrated initially in females by Sue Carter’s group”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Williams et al. 1994 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Compared to pups that experienced biparental care, those raised only by their mother display lower levels of alloparental behavior and impairments in partner preference formation as adults.

    “compared to pups that experienced biparental care, those raised only by their mother display lower levels of alloparental behavior and impairments in partner preference formation as adults”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ahern and Young 2009

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The OT/CRF system may play an adaptive role in the wild by serving to maintain pair bonds over a lifetime, but become maladaptive if reunion with the partner is not achievable.

    “This system may play an adaptive role in the wild by serving to maintain pair bonds over a lifetime, but become maladaptive if reunion with the partner is not achievable.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Prairie voles are the first model organisms to provide insights into the neural mechanisms associated with psychiatric phenotypes based on loss of a partner.

  • May combine two claims.

    Interpretationreasoning

    Reduced OT tone leads to an aversive state and eventually to passive coping behaviors reminiscent of bereavement.

    “leading to an aversive state and eventually to passive coping behaviors reminiscent of bereavement”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Prairie voles are the first model organisms to provide insights into the neural mechanisms associated with psychiatric phenotypes based on loss of a partner.

  • May combine two claims.

    Interpretationcitation

    An activated brain CRF system following partner loss negatively impacts striatal OT signaling, causing increased passive stress-coping behavior indicative of depressive-like behavior.

    “Taken together, these data provide striking evidence for the significant negative impact of an activated brain CRF system following partner loss on striatal OT signaling, thereby causing the increased passive stress-coping behavior indicative of depressive-like behavior”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Cryan and Mombereau 2004 source

      Not checked in the free run.

    • cites Cryan et al. 2005

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  • May combine two claims.

    Interpretationreasoning

    Each of these processes (increased CRF signaling, impoverished OT environment, reduced OTR in NAc, reduced excitatory drive onto OT neurons) reduces OT tone.

    “Each of these processes reduces OT tone”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Prairie voles are the first model organisms to provide insights into the neural mechanisms associated with psychiatric phenotypes based on loss of a partner.

  • May combine two claims.

    Interpretationreasoning

    Results in prairie voles parallel many studies in humans, suggesting that findings from vole studies may have important translational implications for psychiatry.

    “The results in prairie voles parallel many studies in humans, suggesting that the findings from vole studies may have important translational implications for psychiatry.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    The negative emotional state during short separation encourages reunion with the partner and may have evolved to maintain long-term partnerships.

    “Hence, this negative emotional state during short separation, i.e., 5 days, encourages reunion with the partner and may have evolved to maintain long-term partnerships”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Bosch et al. 2009 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In humans, the NAc becomes activated in men viewing the face of their female partner, but not other women, a physiological effect that can be enhanced by intranasal OT.

    “In humans, the NAc becomes activated in men viewing the face of their female partner, but not other women, a physiological effect that can be enhanced by intranasal OT”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Scheele et al. 2013 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Polymorphisms in the human OTR predict social behavioral phenotypes, including those associated with autism, and how early-life experiences shape later psychiatric outcomes.

    “Several psychiatric genetic studies have suggested that polymorphisms in the human OTR predict not only social behavioral phenotypes, including those associated with autism (Skuse et al. 2014; Parker et al. 2014; LoParo and Waldman 2015), but also how early-life experiences shape later psychiatric outcomes”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Skuse et al. 2014 source

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    • cites Schneider-Hassloff et al. 2016 source

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20 of 20

  • The paper relies on this without support.

    Prairie voles are the first model organisms to provide insights into the neural mechanisms associated with psychiatric phenotypes based on loss of a partner.

    “Prairie voles have been the first model organisms to provide insights into the neural mechanism associated with psychiatric phenotypes based on the loss of a partner.”
1 of 1

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?

  • Pair bonding primes the CRF system and, upon partner separation, activity at CRF2s leads to diminished OT signaling in the NAc and subsequent passive stress-coping behaviors, which may reflect negative affect.

    “Together, these findings suggest that pair bonding primes the CRF system and, upon partner separation, activity at CRF2s leads to diminished OT signaling in the NAc and subsequent passive stress-coping behaviors, which may reflect negative affect [2].”

    From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [2]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Separation group changes from female partners to female siblings

    Minor

    The described separation experiment compares males housed with female partners against males housed with male siblings. The later sentence instead identifies the group with heightened passive stress-coping as males separated from female siblings.

1 of 1

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. Zisook S, Shuchter SR, Sledge PA, Paulus M, Judd LL (1994) The spectrum of depressive phenomena after spousal bereavement. J Clin Psychiatry 55(Suppl):29–36

Cited by

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Related

Authors
Bosch, O. J., & Young, L. J.
Affiliations
  • University of Regensburg (DE)
  • Emory University (US)
Corresponding author
  • Bosch, Oliver J.
  • Young, Larry J.
ORCID
Venue
Current Topics in Behavioral Neurosciences
Publisher
Springer International Publishing
Published
2017
Volume
35
Pages
97-117
ISSN
  • 1866-3370 (ISSN-L)
  • 1866-3389
DOI
10.1007/7854_2017_10
PMC
PMC5815947
OpenAlex
W2746848384
Cited by
162
References
140
Citations by year
2026: 13 · 2025: 21 · 2024: 22 · 2023: 19 · 2022: 18 · 2021: 25 · 2020: 22 · 2019: 8 · 2018: 12 · 2017: 2
FWCI
46.41
Type
book chapter
Language
en
Open access
Licence
www.springer.com/tdm (unspecified)
Locations
  • Current topics in behavioral neurosciences (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Deutsche Forschungsgemeinschaft
  • National Institutes of Health (P51OD011132)
  • National Institute of Mental Health (R01MH096983, P50MH100023, R01MH077776)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Social Sciences › Psychology › Social Psychology › Attachment and Relationship Dynamics
Keywords
oxytocin, social bonding, Microtus ochrogaster, pair bonding, mesolimbic dopamine system, loss of a partner, depression-like behavior, bereavement, corticotropin-releasing factor, striatum, melanocortin agonists, social isolation, attachment, interpersonal relationships
MeSH terms
Animals, Brain, Arvicolinae, Female, Male, Object Attachment, Oxytocin, Pair Bond, Social Behavior, Receptors, Oxytocin

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