Reward mechanisms and the neurobiology of affiliation in the monogamous prairie vole (Microtus ochrogaster)

The prairie vole (Microtus ochrogaster) displays a number of characteristic behaviors of social monogamy, including pair-bonding, biparental care, and cooperative breeding. Previous research has found a remarkable amount of developmental plasticity in adult prairie vole behavior following neonatal manipulation. Additionally, pair-bond formation among adults is followed by a number of behavioral and neurophysiological adaptations, suggesting clear plasticity in species-typical behavior during adulthood. Social behavior has been proposed to function as an ethologically relevant natural reward, and the highly social prairie vole is an ideal animal model for exploring 'social reward.' The following studies broadly aimed to explore the role of reward on both developmental and adult plasticity. Dopamine is a key neurotransmitter in reward processing, with distinct actions via two major classes of receptors, the D1-like (D1) and D2-like (D2). First, we aimed to expand our understanding of dopamine's role in social behavior by looking at the effect of receptor specific agonists and antagonists on alloparental behavior and response to a juvenile conspecific. In the second set of experiments, we gave a single neonatal treatment of each D1 or D2 agonist or antagonist to 8-day- old pups, and then measured adult behavior. Although we did not see any clear, receptor-specific effects on pup- or juvenile-directed behavior in subjects treated as adults, early manipulation of this system did have sex- and receptor-specific effects on adult prairie vole behavior. As adults, females treated neonatally with a D2 antagonist exhibited reduced anxiety-like behavior in an elevated plus maze and a reduction in infanticidal behavior. Neonatal treatment with a D1 agonist inhibited partner preference formation in both males and females. In the final study, we looked at the activity of the transcription factor DeltaFosB in response to a number of social conditions. This protein has been implicated in brain plasticity following exposure to other chronic stimuli, including drugs of abuse and repeated stress. Specifically, we looked at DeltaFosB expression following prolonged exposure to a novel same-sex or novel heterosexual partner, as well as social isolation. None of the conditions led to changes in DeltaFosB expression. We therefore conclude that this protein is not involved in the long-term changes in brain and behavior following social cohabitation or isolation. Overall, the present research suggests that dopaminergic modulation of prairie vole social behavior is highly stimulus- and receptor-subtype specific, and may be altered by a single early pharmacological treatment. We have also shown that pair-bonding does not activate the same neural mechanisms as drugs of abuse, as measured by DeltaFosB. These findings suggest that neural mechanisms of attachment formation in this species differ from those of long-term maintenance.