Long-term social bonds are critical for survival and reproductive success in many species. Although courtship and pair-bond formation are relatively well studied, much less is known about the neural regulation of behaviors that occur after pair bonding that reinforce the bond and contribute to reproductive success. Dopamine and opioids in the nucleus accumbens (NAc) alter motivational state and reward by binding to receptor subtypes that engage distinct and opposing second messenger systems, and there is evidence that receptor ratios may influence social behavior. We used quantitative real-time PCR to explore relationships between messenger RNA ratios for dopamine D1 and D2 receptors (D1:D2) and mu and kappa opioid receptors (MOR:KOR) in NAc and behaviors implicated in reproductive investment and pair-bond maintenance in established male-female zebra finch pairs. In males, D1:D2 expression in NAc related negatively, whereas MOR:KOR related positively, to undirected song production. D1:D2 receptors also related positively to physical contact with a female. For females, D1:D2 expression was lower in females exposed to high compared to low rates of the partner's undirected song, and MOR:KOR expression in females related positively to undirected song exposure and allopreening. Analyses of single genes did not yield the same results. These findings suggest that the ratio of D1 to D2 and MOR to KOR receptor signaling in NAc causes differences in behavior or that behavior (or the partner's behavior) causes receptor ratio changes to modulate behaviors that maintain pair bonds and promote reproductive investment.
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