The DOI matches its Crossref record; 36 of the 36 references it cites were found in a registry or an index.
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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In the citing paper
“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]
In the citing paper
“The relationship between maternal affiliative touch and maternal oxytocin levels has been observed in other mammals (monogamous and polygamous volves; Insel and Shapiro, 1992).”
From The evolved nest, oxytocin functioning, and prosocial development (2023) · cites this paper as Insel and Shapiro (1992)
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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 the citing paper
“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]
In the citing paper
“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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“The relationship between maternal affiliative touch and maternal oxytocin levels has been observed in other mammals (monogamous and polygamous volves; Insel and Shapiro, 1992).”
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Metadata
- 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
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › 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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