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Cited by 276Neuroendocrine regulation and behaviorPrimate Behavior and EcologyAnimal Behavior and Reproduction

The prairie vole: An emerging model organism for understanding the social brain

Open access
McGraw, Lisa A., Young, Larry J.·2010·Trends in Neurosciences
DOI 10.1016/j.tins.2009.11.006PMC PMC2822034
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Abstract

Unlike most mammalian species, the prairie vole is highly affiliative, forms enduring social bonds between mates and displays biparental behavior. Over two decades of research on this species has enhanced our understanding of the neurobiological basis not only of monogamy, social attachment and nurturing behaviors but also other aspects of social cognition. Because social cognitive deficits are hallmarks of many psychiatric disorders, discoveries made in prairie voles can direct novel treatment strategies for disorders such as autism spectrum disorder and schizophrenia. With the ongoing development of molecular, genetic and genomic tools for this species, prairie voles will likely maintain their current trajectory becoming an unprecedented model organism for basic and translational research focusing on the biology of the social brain.

AI snapshot

Written from the paper’s full text.

TL;DR

The prairie vole is a socially monogamous, biparental rodent that has become a leading model for the neurobiology and genetics of social bonding, parental care, social loss, and social cognition. The review argues that its natural social diversity and emerging genomic tools make it exceptionally useful for translational research on psychiatric disorders involving social deficits.

Key findings

  • Prairie voles form enduring pair bonds and show biparental care, but genetic monogamy is not the norm: 23–56% of litters are sired by multiple males, and ~35–45% of males adopt a “wandering” tactic rather than a “resident” pair-bonding tactic.
  • Oxytocin, vasopressin, and dopamine act in reward-related circuitry to regulate pair bonding: OT receptors in the nucleus accumbens facilitate female partner preferences, AVPR1A in the ventral pallidum/lateral septum is critical in males, and D2-type dopamine receptor activation facilitates while D1-type activation prevents partner preference formation.
  • About 60% of adult virgin female prairie voles spontaneously display alloparental nurturing toward novel pups, while 40% ignore or attack pups; this variation is associated with oxytocin receptor density in the nucleus accumbens.
  • Early-life family structure and adult social loss have lasting effects: single-mother rearing reduced alloparental behavior and lengthened cohabitation needed for partner preferences, while social isolation or pair-bond disruption produced depression-like behaviors and cardiac changes.

Methods

  • Narrative review synthesizing over two decades of prairie vole research, including comparative, pharmacological, neuroanatomical, genetic, and genomic studies.
  • Draws on laboratory, semi-natural, and field studies of prairie voles and related vole species, with the partner preference test described as the prototypical assay for social attachment.
  • Main analysis is qualitative thematic synthesis of findings on social bonding, parental care, early life experience, social loss, human social behavior, and sociogenomic tools.

Limitations

  • The paper states that prairie voles cannot model disrupted aspects of social cognition characteristic of ASD, such as facial processing, empathy, or theory of mind, and are unlikely to identify exact etiologies of human psychiatric disorders.
  • The paper notes that the precise mechanisms by which the Avpr1a microsatellite contributes to receptor distribution and behavior remain poorly understood, and that much more research is needed on oxytocin in ASD.
  • Evident from the text: this is a narrative review without a systematic search or quantitative synthesis, so its conclusions depend on the selected cited literature rather than a formal meta-analytic design.

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

Integrity signals

Registry

Crossref · 10.1016/j.tins.2009.11.006

Cites

Statistics

Nothing to recompute.

Claims the paper makes

0 of 123 cited sources checked · 0 supported · 0 flagged

  • Premisecitation

    Infusion of OT into the brain during cohabitation with a male accelerates the development of a partner preference.

    “Infusion of OT into the brain during cohabitation with a male accelerates the development of a partner preference, while blocking OTR in the NAcc during mating prevents this behavior [14, 15].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [14] Young, 2001, Cellular mechanisms of social attachment, Horm. Behav. source

      Not checked in the free run.

    • cites [15] Williams, 1994, Oxytocin administered centrally facilitates formation of a partner preference in prairie voles (Microtus ochrogaster), J. Neuroendocrinol. source

      Not checked in the free run.

  • Premisecitation

    Sociosexual interactions trigger the release of OT into the NAcc from neuronal fibers that likely originate from magnocellular neurons in the hypothalamus that also project to the pituitary.

    “Sociosexual interactions trigger the release of OT into the NAcc from neuronal fibers that likely originate from magnocellular neurons in the hypothalamus that also project to the pituitary [10].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [10] Ross, 2009, Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior, Front. Neuroendocrinol. source

      Not checked in the free run.

  • Premisecitation

    When female prairie voles lose a mate, they often fail to take on a new partner.

    “Initial observations of the socially monogamous mating system of prairie voles stemmed from field observations in which male-female pairs were repeatedly captured together within the same home ranges [52–55] and subsequent laboratory studies determined that when female prairie voles lose a mate, they often fail to take on a new partner [56].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [56] Pizzuto, 1998, Female prairie voles (Microtus ochrogaster) fail to form a new pair after loss of mate, Behav. Processes source

      Not checked in the free run.

  • Premisecitation

    V1aR density in the posterior cingulated/retrosplenial cortex predicted reproductive success in "wanderers".

    “Instead, V1aR density in the posterior cingulated/retrosplenial cortex, a region of the brain involved in spatial learning and memory predicted reproductive success in “wanderers”.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [3] Ophir, 2008, Field tests of cis-regulatory variation at the prairie vole avpr1a locus: association with V1aR abundance but not sexual or social fidelity, Horm. Behav. source

      Not checked in the free run.

  • Premisecitation

    Meadow voles and montane voles are relatively asocial.

    “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].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [2] Young, 2004, The neurobiology of pair bonding, Nat. Neurosci. source

      Not checked in the free run.

  • May combine two claims. 12
  • Classified as probably not a substantial claim. 1

  • May combine two claims.

    Premisecitation

    Prairie voles from Kansas are less social and display lower levels of physical contact between adult males and females, less spontaneous alloparental and parental behavior, and are more aggressive than Illinois prairie voles.

    “For example, prairie voles from Kansas are less social and display lower levels of physical contact between adult males and females, less spontaneous alloparental and parental behavior, and are more aggressive than Illinois prairie voles [61, 62].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [61] Roberts, 1998, Role of social and endocrine factors in alloparental behavior of prairie voles (Microtus ochrogaster), Can. J. Zool. source

      Not checked in the free run.

    • cites [62] Cushing, 2001, The effects of peptides on partner preference formation are predicted by habitat in prairie voles, Horm. Behav. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    "Wanderer" male prairie voles typically only sire offspring via extra-pair fertilizations and provide no care for their young.

    ““Wanderer” males typically only sire offspring via extra-pair fertilizations and provide no care for their young.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [57] Getz, 1993, Social organization of the prairie vole (Microtus ochrogaster), J. Mammal. source

      Not checked in the free run.

    • cites [58] Thomas, 1979, Parental care and mating system of the prairie vole, Microtus ochrogaster, Behav. Ecol. Sociobiol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Levels of V1aR in the ventral pallidum and lateral septum did not correspond to male mating tactic, male mating success, nor the male's propensity to engage in extra-pair copulations.

    “Surprisingly, although AVPR1A in the ventral pallidum and lateral septum have been shown to be involved in the regulation of partner preference formation and paternal care, levels of V1aR in these regions did not correspond to male mating tactic, male mating success, nor the male’s propensity to engage in extra-pair copulations.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [3] Ophir, 2008, Field tests of cis-regulatory variation at the prairie vole avpr1a locus: association with V1aR abundance but not sexual or social fidelity, Horm. Behav. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Ophir et al. (2008), most male prairie voles (74%) were classified as a member of a bonded pair, while the remaining males assumed the "wandering" tactic.

    “Most males (74%) were classified as a member of a bonded pair, while the remaining males assumed the “wandering” tactic.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] Ophir, 2008, Field tests of cis-regulatory variation at the prairie vole avpr1a locus: association with V1aR abundance but not sexual or social fidelity, Horm. Behav. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Prairie voles are routinely studied in their natural and semi-natural habitats.

    “Prairie voles and related vole species are easily maintained and housed in standard rodent vivariums and are also routinely studied in their natural and semi-natural habitats [3, 4] (Box 1).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [3] Ophir, 2008, Field tests of cis-regulatory variation at the prairie vole avpr1a locus: association with V1aR abundance but not sexual or social fidelity, Horm. Behav. source

      Not checked in the free run.

    • cites [4] Solomon, 2008, Estimates of reproductive success for group-living prairie voles, Microtus ochrogaster, in high-density populations, Anim. Behav. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In prairie voles, cohabitation with a female resulted in a decrease in AVP content in the lateral septum, coincident with an increase in paternal responsiveness.

    “Early comparative studies discovered that in prairie voles, cohabitation with a female resulted in a decrease in AVP content in the lateral septum (likely reflecting a release of AVP from neuronal fibers in the region), which was coincident with an increase in paternal responsiveness.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [36] Bamshad, 1994, Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster), Physiol. Behav. source

      Not checked in the free run.

    • cites [37] Bamshad, 1993, Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster and meadow voles, M. pennsylvanicus, J. Neuroendocrinol. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Variation in OTR density during development, or perhaps OTR in additional brain regions, are contributing to the diversity in alloparental behavior.

    “These results suggest that variation in OTR density during development, or perhaps OTR in additional brain regions are contributing to the diversity in alloparental behavior.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Socially monogamous male prairie voles have high densities of AVPR1A binding in the ventral pallidum, while non-monogamous vole species do not.

    “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].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [2] Young, 2004, The neurobiology of pair bonding, Nat. Neurosci. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    While D1 and D2 receptors are associated with species differences in social behaviors, they are not solely responsible.

    “These data suggest that while these receptors are associated with species differences in social behaviors, they are not solely responsible.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Viral vector-mediated over-expression of OTR within the NAcc of adult female prairie voles does not result in enhanced alloparental behavior, even though partner preference formation is accelerated in those same animals.

    “Although high densities of OTR within the NAcc are correlated with high levels of alloparental care in females, viral vector-mediated over-expression of OTR within the NAcc of adult female prairie voles does not result in enhanced alloparental behavior, even though partner preference formation is accelerated in those same animals [35].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [35] Ross, 2009, Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles, J. Neurosci. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    When antagonists are used to block D1 receptors in meadow voles, males show greater affiliate behavior towards a female after a short cohabitation period, but do not form a partner preference.

    “When antagonists are used to block these receptors, males show greater affiliate behavior towards a female after a short cohabitation period, but do not form a partner preference [26].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] Aragona, 2006, Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds, Nat. Neurosci. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Approximately 60% of adult female prairie voles display spontaneous maternal nurturing toward novel pups, while 40% either ignore or attack pups.

    “Approximately 60% of adult females display spontaneous maternal nurturing toward novel pups, while 40% either ignore or attack pups [33–35].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [33] Olazábal, 2006, Oxytocin receptors in the nucleus accumbens facilitate “spontaneous” maternal behavior in adult female prairie voles, Neuroscience source

      Not checked in the free run.

    • cites [34] Olazábal, 2006, Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum, Horm. Behev. source

      Not checked in the free run.

    • cites [35] Ross, 2009, Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles, J. Neurosci. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Male prairie voles with relatively short microsatellites had lower levels of AVPR1A binding in the olfactory bulb and lateral septum, and were less likely to display a partner preference than males with longer microsatellites.

    “For example, montane and meadow voles have considerably shorter microsatellite elements than prairie voles [30], and male prairie voles with relatively short microsatellites had lower levels of AVPR1A binding in the olfactory bulb and lateral septum, and were less likely to display a partner preference than males with longer microsatellites [31].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [31] Hammock, 2005, Microsatellite instability generates diversity in brain and sociobehavioral traits, Science source

      Not checked in the free run.

13 of 13

  • The paper relies on this without support.

    Impairments in the ability to engage in healthy social interactions and to form stable social attachments are common characteristics of several mental health disorders, including depression, addiction, schizophrenia and autism spectrum disorders.

    “Impairments in the ability to engage in healthy social interactions and to form stable social attachments are common characteristics of several mental health disorders, including depression, addiction, schizophrenia and autism spectrum disorders (ASD).”

  • The paper relies on this without support.

    The ability to form stable social attachments is rare in animals, particularly among those species typically studied in the laboratory.

    “Because the ability to form stable social attachments is rare in animals, particularly among those species typically studied in the laboratory, studies of the biological bases of complex social behaviors that recapitulate the richness of human social relationships have been limited.”

  • The paper relies on this without support.

    Few eukaryotic animal models recapitulate the richness of human social behavior, including the capacity to form lasting social attachments.

    “However, the translational utility of a model organism is only as valuable as the traits it expresses, and though almost all eukaryotic animal models exhibit some form of social behavior, few recapitulate the richness of social behavior of humans, including our capacity to form lasting social attachments.”

  • The paper relies on this without support.

    Laboratory-reared prairie vole colonies are systematically outbred, often only a few generations from the field.

    “In addition, laboratory-reared prairie vole colonies are systematically outbred, often only a few generations from the field, allowing for the study of individual variation in neurochemistry and sociobehavioral traits (Figure 1B).”

  • The paper relies on this without support.

    Both laboratory-reared and recently captured wild voles are amenable to pharmacological and genetic manipulations and classic behavioral paradigms used in mice and rats.

    “Both laboratory-reared and recently captured wild voles are amenable to pharmacological and genetic manipulations and classic behavioral paradigms used in mice and rats.”

  • The paper relies on this without support.

    Little is known of the genetic regulation of the neural components underlying social bonding.

    “Although many of the neural components underlying social bonding are beginning to be identified, little is known of the genetic regulation of these systems.”
6 of 6

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 prairie vole is the premier animal model for the neurobiology of social bonding and is increasingly used to screen drugs with therapeutic potential for social disorders such as autism.

    “The prairie vole (Microtus ochrogaster), a socially monogamous rodent native to the American Midwest (24), is the premier animal model for the neurobiology of social bonding (25) and increasingly used to screen drugs that have therapeutic potential for social disorders such as autism (26,27).”

    From Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles (2013) · cites this paper as [25]

  • Prairie voles form a lifelong pair bond upon social interaction and mating, resulting in a dramatic change in the way they interact with other individuals.

    “Upon social interaction and mating, prairie voles (Microtus ochrogaster) form a lifelong pair bond resulting in a dramatic change in the way they interact with other individuals 22.”

    From Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles (2022) · cites this paper as [22]

The citation lists haven’t been fetched yet

References 68 · Cited by 276

Research works printed but not linked: 2

  1. Ross, 2009, Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles, J. Neurosci., 29, 1312, 10.1523/JNEUROSCI.5039-08.2009 · DOI · Paper page
  2. Ahern, 2009, Evaluation of two automated metrics for analyzing partner preference tests, J. Neurosci. Methods, 182, 180, 10.1016/j.jneumeth.2009.06.010 · DOI

Authors
McGraw, L. A., & Young, L. J.
Affiliations
Emory University (US)
Corresponding author
McGraw, Lisa A.
ORCID
Venue
Trends in Neurosciences
Publisher
Elsevier BV
Published
2010-02
Volume
33
Issue
2
Pages
103-109
ISSN
0166-2236 (ISSN-L)
DOI
10.1016/j.tins.2009.11.006
PMC
PMC2822034
OpenAlex
W2106302542
Cited by
276
References
68
Citations by year
2026: 13 · 2025: 19 · 2024: 19 · 2023: 17 · 2022: 16 · 2021: 17 · 2020: 12 · 2019: 10 · 2018: 21 · 2017: 20 · 2016: 20 · 2015: 25 · 2014: 15 · 2013: 16 · 2012: 15
FWCI
1.66
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Trends in Neurosciences (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (5r21mh082225-02)
  • National Institute of Mental Health (R21 MH082225, F32MH079561, R01MH056538, R01MH077776, R01MH056897)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords
Microtus ochrogaster, social brain, social attachment, monogamy, biparental care, social cognition, social behavior, autism spectrum disorder, schizophrenia, mental illness, model organisms
MeSH terms
Animals, Behavior, Animal, Brain, Arvicolinae, Depression, Heart Diseases, Neural Pathways, Social Behavior, Models, Animal, Neurogenesis, Metagenomics

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