Peer Social Environment Impacts Behavior and Dopamine D1 Receptor Density in Prairie Voles (Microtus ochrogaster)

Abstract

Prairie voles (Microtus ochrogaster) are socially monogamous rodents that form selective, long-lasting relationships with mates and with same-sex peers. It is unknown to what extent mechanisms supporting ‘peer relationships’ are similar to those involved in mate relationships. The formation of pair bonds is dependent on dopamine neurotransmission, whereas the formation of peer relationships is not, providing evidence of relationship type-specificity. The current study assessed endogenous structural changes in dopamine D1 receptor density in male and female voles across different social environments, including long-term same-sex partnerships, new same-sex partnerships, social isolation, and group housing. We also related dopamine D1 receptor density and social environment to behavior in social interaction and partner preference tests. Unlike prior findings in mate pairs, voles paired with new same-sex partners did not exhibit upregulated D1 binding in the nucleus accumbens (NAcc) relative to controls paired from weaning. This is consistent with differences in relationship type: D1 upregulation in pair bonds aids in maintaining exclusive relationships through selective aggression, and we found that formation of new peer relationships did not enhance aggression. Isolation led to increases in NAcc D1 binding, and even across socially housed voles, individuals with higher D1 binding exhibited increased social avoidance. These findings suggest that elevated D1 binding may be both a cause and a consequence of reduced prosociality. These results highlight the neural and behavioral consequences of different non-reproductive social environments and contribute to growing evidence that the mechanisms underlying reproductive and non-reproductive relationship formation are distinct. Elucidation of the latter is necessary to understand mechanisms underlying social behavior beyond a mating context.