Emergence of social recognition in auditory and integrative circuits during pair bonding

Social relationships profoundly shape the perception of communication signals. In animals that form long-term social bonds, sensory cues such as vocalizations, scent, or physical appearance, and rewarding mating experiences can become associated with a bonded mate. While this natural process has hallmarks of some forms of associative learning, little is known about where or how these experiences shape neural circuits over the course of pair bonding. We used whole-brain BOLD fMRI in female songbirds to explore experience-dependent changes in neural activity in response to male songs. Pair bonding experiences drove changes in activation in response to the partner's song within secondary auditory areas as well as two regulatory hubs that receive sensory input and connect to circuits that generate behavioral responses. In contrast, mere exposure to the vocal interactions of a neighboring pair did not result in changes in response to the neighbor's song within the same areas, suggesting that pair bonding uniquely impacts auditory responses to familiar songs in select sensory and integrative circuits. Moreover, within the areas that showed increased activation for the partner's song over the course of pair bonding, we observed diminished activation in response to the partner's song after blocking D1 dopamine receptors, indicating a potential role for dopamine in the expression or maintenance of preference for the partner's song. Eavesdropping females had changes in neural activation in response to the familiar song in a different suite of brain regions that were not affected by dopamine manipulation. Our data identify a potential circuit in which concurrent activation of sensory, reward, and regulatory hubs integrates multisensory information from social interactions and leads to the emergence of acoustic preferences and formation of long-lasting social bonds.