Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles
Open accessAbstract
The neuropeptide oxytocin has been implicated in the mediation of several forms of affiliative behavior including parental care, grooming, and sex behavior. Here we demonstrate that species from the genus Microtus (voles) selected for differences in social affiliation show contrasting patterns of oxytocin receptor expression in brain. By in vitro receptor autoradiography with an iodinated oxytocin analogue, specific binding to brain oxytocin receptors was observed in both the monogamous prairie vole (Microtus ochrogaster) and the polygamous montane vole (Microtus montanus). In the prairie vole, oxytocin receptor density was highest in the prelimbic cortex, bed nucleus of the stria terminalis, nucleus accumbens, midline nuclei of the thalamus, and the lateral aspects of the amygdala. These brain areas showed little binding in the montane vole, in which oxytocin receptors were localized to the lateral septum, ventromedial nucleus of the hypothalamus, and cortical nucleus of the amygdala. Similar differences in brain oxytocin receptor distribution were observed in two additional species, the monogamous pine vole (Microtus pinetorum) and the polygamous meadow vole (Microtus pennsylvanicus). Receptor distributions for two other neurotransmitter systems implicated in the mediation of social behavior, benzodiazepines, and mu opioids did not show comparable species differences. Furthermore, in the montane vole, which shows little affiliative behavior except during the postpartum period, brain oxytocin receptor distribution changed within 24 hr of parturition, concurrent with the onset of maternal behavior. We suggest that variable expression of the oxytocin receptor in brain may be an important mechanism in evolution of species-typical differences in social bonding and affiliative behavior.
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Activation of D1-like dopamine receptors inhibits partner preference formation induced by either mating or by D2 activation.
“Activation of D1-like DA receptors inhibits partner preference formation induced by either mating or by D2 activation [63, 64].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [64]
The striatum and regions within the midbrain are highly populated with oxytocin receptors in non-human animals.
“it is well known from non-human animal work that the striatum and regions within the midbrain are highly populated with oxytocin receptors.44, 45”
From Intranasal oxytocin enhances intrinsic corticostriatal functional connectivity in women (2017) · cites this paper as [44]
Oxytocin receptor binding in the nucleus accumbens is dense in monogamous prairie voles and low to absent in non-monogamous meadow and montane voles.
“Interestingly, OXTR binding in the NAcc, which is dense in monogamous prairie voles, is low to absent in the non-monogamous but closely-related meadow and montane voles (19)”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [19]
Monogamous prairie voles have significantly greater OTR density in prefrontal cortex, caudate-putamen, and nucleus accumbens shell than non-monogamous vole species.
“Monogamous prairie voles have significantly greater OTR density in the prefrontal cortex (the cortical component of the mesolimbic DA pathway), as CP, and NAS than do non-monogamous vole species (Insel and Shapiro 1992).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Insel and Shapiro 1992
There are striking species differences in the location and density of AVP and OT receptors.
“Although there are few species differences in the distribution of AVP and OT in the brain [10, 11], there are striking species differences in the location and density of their respective receptors [7, 8].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [7]
Monogamous prairie voles have a significantly higher density of oxytocin receptors in the nucleus accumbens compared to non-monogamous montane voles.
“Monogamous prairie voles, who maintain a pair bond for life, were found to have a significantly higher density of OXT receptors in the nucleus accumbens (NAc), a critical node in the brain's reward circuitry [11,12], when compared to non-monogamous montane voles [13].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [13]
Oxytocin, released by the hypothalamic paraventricular nucleus (PVN), is a critical maternal hormone.
“Oxytocin1,2,9–15, which is released by the hypothalamic paraventricular nucleus (PVN), is a critical maternal hormone.”
From Oxytocin neurons enable social transmission of maternal behaviour (2021) · cites this paper as [9]
Oxytocin acts in the brain to increase the salience of social information and enable alloparenting in mice.
“Oxytocin also acts in the brain to increase the salience of social information and enable alloparenting in mice1,9,12–14.”
From Oxytocin neurons enable social transmission of maternal behaviour (2021) · cites this paper as [9]
OXTR mRNA localization in the rodent brain is well-described, but its anatomical distribution across the human brain is poorly understood because investigations have historically sampled very few brain regions.
“While OXTR mRNA localization in the rodent brain is well-described11, its anatomical distribution across the human brain is poorly understood, as investigations have historically tended to sample very few brain regions12.”
From Oxytocin pathway gene networks in the human brain (2019) · cites this paper as [11]
In rodents, oxytocin receptors are located in regions that are crucial for social behavior and the processing of social cues.
“In these animals, oxytocin receptors are located in regions that are crucial for social behavior and the processing of social cues11.”
From Oxytocin pathway gene networks in the human brain (2019) · cites this paper as [11]
Yatawara and colleagues reported positive effects of oxytocin on social communication in young children with ASD aged 3 to 8 years, with significant improvements in positive social behaviours as measured by caregiver ratings on the Social Responsiveness Scale, and significant order effects.
“Very recently, Yatawara and colleagues reported positive effects of oxytocin administration on social communication in the first study of very young children with ASD, aged between 3 to 8 years.57 Similar to Watanabe et al., these authors employed a crossover trial, with a five week administration period of either oxytocin or placebo, switched to the alternate drug after a one month washout period”
From Beyond the hype and hope: critical considerations for intranasal oxytocin research in autism spectrum disorder (2017) · cites this paper as [57]
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- Authors
- Insel, T. R., & Shapiro, L. E.
- Affiliations
- National Institute of Mental Health (US)
- ORCID
- Insel, T R
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1992-07
- Volume
- 89
- Issue
- 13
- Pages
- 5981-5985
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC402122
- OpenAlex
- W1998107589
- Cited by
- 833
- References
- 36
- Citations by year
- 2026: 21 · 2025: 18 · 2024: 28 · 2023: 25 · 2022: 26 · 2021: 38 · 2020: 39 · 2019: 27 · 2018: 43 · 2017: 52 · 2016: 45 · 2015: 37 · 2014: 41 · 2013: 41 · 2012: 37
- FWCI
- 15.12
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- oxytocin receptor, social organization, monogamy, polygamy, voles, Microtus ochrogaster, montane vole, pine vole, Microtus pennsylvanicus, affiliative behavior, social bonding, maternal behavior, childbirth, brain receptor distribution, prelimbic cortex, bed nucleus of the stria terminalis, nucleus accumbens, amygdala, lateral septum, benzodiazepine receptor, mu-opioid receptor, Microtus
- MeSH terms
- Animals, Behavior, Animal, Brain, Brain Mapping, Arvicolinae, Enkephalins, Flunitrazepam, Lactation, Oxytocin, Receptors, Angiotensin, Receptors, Opioid, Receptors, GABA-A, Social Behavior, Species Specificity, Receptors, Opioid, mu, Receptors, Oxytocin, Enkephalin, Ala(2)-MePhe(4)-Gly(5)-
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