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Friendships, or selective peer relationships, are a vital component of healthy social functioning in humans, and deficits in these relationships are associated with negative physical and mental health consequences. Like humans, prairie voles are among the few mammalian species that form selective social bonds with both peers and mates, making them an excellent model for the mechanistic investigation of selective social attachment. Here, we explored the role of oxytocin receptors in selective peer attachment using female prairie voles lacking a functional oxytocin receptor gene (Oxtr1−/−). We found that Oxtr1−/− animals exhibited significant delays in peer relationship formation compared with wild-type animals. Oxytocin receptor function also contributed to the maintenance of peer bonds, as Oxtr1−/− voles displayed reduced relationship stability and lost selective attachments rapidly in a multi-chamber, group-living habitat. Oxtr1−/− voles also showed deficits in general social reward as well as selective social reward for a peer partner over an unfamiliar conspecific. Evoked oxytocin release in the nucleus accumbens was reduced in male and female Oxtr1−/− animals compared with their wild-type counterparts, indicating that these voles do not have a compensatory increase in oxytocinergic signaling. Together, these data indicate that oxytocin receptors influence the formation, persistence, and reward value of peer relationships.
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Reunion with a peer partner reduces PVN oxytocin neuron immunoreactivity in socially selective voles
Friendships—i.e. selective peer relationships—are an important aspect of human behavior, but are rare in rodent species. Meadow voles are seasonally social rodents that form non-reproductive social groups in winter/short day lengths that are selective in nature. Across rodents, oxytocin neurons in the paraventricular nucleus (PVN) of the hypothalamus are typically active during socially salient events, including interaction with novel individuals as well as social separation. To assess whether familiar and novel peer interactions produce different patterns of immunolabeling in a species that forms bonds with familiar individuals, we measured oxytocin neuron immunoreactivity and colabeling with the immediate early gene product cFos. Oxytocin labeling and oxytocin/cFos colabeling were higher after interaction with a novel same-sex conspecific than after reunion with a peer partner. Colabeling was also high after 24 h separation without reunion. Circulating corticosterone concentrations paralleled PVN oxytocin neuron activity. We also investigated whether oxytocin signaling was photoperiod dependent and could contribute to seasonal differences in meadow vole social behavior. Oxytocin receptor densities are known to be higher in multiple brain regions in short day lengths in meadow voles, but we found no concomitant change in PVN oxytocin positive cell count. Together these studies indicate that seasonal changes in behavior correlate with oxytocin signaling at the receptor level, while short term experiences modulated oxytocin neuron activity differentially by social context.
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- PAR ID:
- 10665040
- Publisher / Repository:
- Nature Portfolio
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 15
- Issue:
- 1
- ISSN:
- 2045-2322
- Subject(s) / Keyword(s):
- reunion, social behavior, oxytocin, cFos, corticosterone, meadow vole
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1038/s41598-025-17920-3
