Social selectivity and social motivation in voles

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.

Selectivity and Sociality: Aggression and Affiliation Shape Vole Social Relationships

“…Female prairie voles treated with oxytocin shortly after birth exhibited more aggression toward a same-sex stranger in a neutral arena after brief exposure to a male, compared to control or oxytocin antagonist-treated females ( Bales and Carter, 2003 ). Oxytocin receptor density in the BNST of female prairie voles was associated with increased aggression toward unfamiliar voles ( Beery et al, 2021 ), and in males, an Oxtr genotype that is associated with striatal oxytocin receptor expression and bond formation ( King et al, 2016 ; Ahern et al, 2021 ) is also strongly associated with aggression toward strangers ( Vahaba et al, 2021 ). Oxytocin also mediates aggression and social anxiety in many other rodent species, including rats, mice, naked mole rats, California mice, hamsters, and Mongolian gerbils (reviewed in Campbell, 2008 ; de Jong and Neumann, 2018 ; Steinman et al, 2019 ).…”

“…Although aggression mediates selectivity in prairie vole mate and peer relationships, the relative importance of prosocial motivation varies across relationship type. Prairie vole mate relationships rely on dopamine and opioid signaling ( Aragona et al, 2003 , 2006 ; Resendez et al, 2012 , 2016 ), and are associated with behavioral reward in socially conditioned place preference (sCPP) tests and operant studies using a social reward ( Ulloa et al, 2018 ; Goodwin et al, 2019 ; Beery et al, 2021 ). While dopamine signaling is not essential for the formation of peer relationships in prairie voles ( Lee and Beery, 2021 ), female prairie voles find familiar peers more motivating than strangers or an empty chamber, and condition toward socially associated cues in the sCPP test ( Beery et al, 2021 ; Lee and Beery, 2021 ).…”

“…Prairie vole mate relationships rely on dopamine and opioid signaling ( Aragona et al, 2003 , 2006 ; Resendez et al, 2012 , 2016 ), and are associated with behavioral reward in socially conditioned place preference (sCPP) tests and operant studies using a social reward ( Ulloa et al, 2018 ; Goodwin et al, 2019 ; Beery et al, 2021 ). While dopamine signaling is not essential for the formation of peer relationships in prairie voles ( Lee and Beery, 2021 ), female prairie voles find familiar peers more motivating than strangers or an empty chamber, and condition toward socially associated cues in the sCPP test ( Beery et al, 2021 ; Lee and Beery, 2021 ). Because prairie voles direct their affiliation and aggression at specific targets, both aspects of behavior likely contribute to their highly selective social groups.…”

“…Meadow voles are not socially monogamous, and because they are closely related to, yet behaviorally distinct from prairie voles, they provide an opportunity to assess similarities and differences in behavior and mechanism across species and mating systems (e.g., Wang et al, 1994 ; Kingsbury et al, 2012 ; Inoue et al, 2013 ; Lee et al, 2019 ; Beery et al, 2021 ). Meadow voles also provide a within-species opportunity to examine mechanisms underlying variation in social grouping, as they exhibit seasonal shifts in social behavior.…”

“…While meadow voles naturally cohabit in winter social groups, social reward does not appear to play an important role in group formation. Meadow voles housed in SDs in the lab show no sign of social reinforcement in either sCPP tests ( Goodwin et al, 2019 ) or in operant conditioning tests with social rewards ( Beery et al, 2021 ). Partner preferences for same-sex peers are also dopamine-independent in this species ( Beery and Zucker, 2010 ).…”