In social species, relationships may form between mates, parents and their offspring, and/or social peers. Prairie voles and meadow voles both form selective relationships for familiar same-sex peers, but differ in mating system, allowing comparison of the properties of peer and mate relationships. Prairie vole mate bonds are dopamine-dependent, unlike meadow vole peer relationships, indicating potential differences in the mechanisms and motivation supporting these relationships within and/or across species. We review the role of dopamine signaling in affiliative behavior, and assess the role of behavioral reward across relationship types. We compared the reinforcing properties of mate versus peer relationships within a species (prairie voles), and peer relationships across species (meadow and prairie voles). Social reinforcement was assessed using the socially conditioned place preference test. Animals were conditioned using randomly assigned, equally preferred beddings associated with social (CS+) and solitary (CS-) housing. Prairie vole mates, but not prairie or meadow vole peers, conditioned toward the social cue. A second study in peers used counter-conditioning to enhance the capacity to detect low-level conditioning. Time spent on CS+ bedding significantly decreased in meadow voles, and showed a non-significant increase in prairie voles. These data support the conclusion that mate relationships are rewarding for prairie voles. Despite selectivity of preferences for familiar individuals in partner preference tests, peer relationships in both species appear only weakly reinforcing or non-reinforcing. This suggests important differences in the pathways underlying these relationship types, even within species.

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.

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 (prairie voles) or peers (meadow voles). Female prairie and meadow voles worked harder to access familiar vs. unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles also displayed strongly selective huddling preferences for familiar animals, but worked hardest to repeatedly access females vs. males, with no difference in effort by familiarity. This demonstrates a fundamental disconnect between motivation and social selectivity in males, and reveals a striking sex difference in pathways underlying social monogamy. 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 genotype was associated with oxytocin receptor density, and both genotype and 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.

No abstract