Social selectivity and social motivation in voles.

Annaliese K Beery,Nicole S Lee,Katrina L Blandino,Natalie S Bourdon,Sarah A Lopez

doi:10.7554/elife.72684

Abstract

Selective relationships are fundamental to humans and many other animals, but relationships between mates, family members, or peers may be mediated differently. We examined connections between social reward and social selectivity, aggression, and oxytocin receptor signaling pathways in rodents that naturally form enduring, selective relationships with mates and peers (monogamous prairie voles) or peers (group-living meadow voles). Female prairie and meadow voles worked harder to access familiar versus unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles displayed strongly selective huddling preferences for familiar animals, but only worked harder to repeatedly access females versus males, with no difference in effort by familiarity. This reveals a striking sex difference in pathways underlying social monogamy and demonstrates a fundamental disconnect between motivation and social selectivity in males-a distinction not detected by the partner preference test. Meadow voles exhibited social preferences but low social motivation, consistent with tolerance rather than reward supporting social groups in this species. Natural variation in oxytocin receptor binding predicted individual variation in prosocial and aggressive behaviors. These results provide a basis for understanding species, sex, and individual differences in the mechanisms underlying the role of social reward in social preference.

Highlights

The brain regions and neurochemicals involved in social behaviors show remarkable conservation across species (O’Connell and Hofmann, 2011)
Female prairie voles pressed more for familiar partners than unfamiliar strangers, with no effect of opposite-sex vs. same-sex pairings (Figure 2A, effect of stimulus familiarity: F(1, 14) = 15.17, p =
Because male meadow voles do not undergo this transition (Madison and McShea, 1987; Beery et al, 2009), we focused on comparison of social motivation in female meadow voles relative to female prairie voles

Summary

Introduction

The brain regions and neurochemicals involved in social behaviors show remarkable conservation across species (O’Connell and Hofmann, 2011). The formation of selective social relationships is a particular hallmark of both human and prairie vole societies. Such relationships are difficult to study in traditional lab rodents because mice, rats, and other rodents typically don’t form preferences for known peers or mates (Triana-Del Rio et al, 2015; Schweinfurth et al, 2017; Beery et al, 2018; CymerblitSabba et al, 2020; Insel et al, 2020; Beery and Shambaugh, 2021). The role of social motivation and tolerance may differ by familiarity, sex, and type of relationship (e.g., samesex peer versus opposite-sex mate). Voles provide an opportunity to probe the role of selectivity and social reward across relationship types and social organization

Results

Discussion

Conclusion