Early auditory and adult mating experiences interact with singer identity to shape neural responses to song in female zebra finches

Abstract

Social and sensory experiences across the lifespan can shape social interactions; however, experience-dependent plasticity is widely studied within discrete life stages. In the socially monogamous zebra finch, in which females use learned vocal signals to identify individuals and form long-lasting pair bonds, developmental exposure to song is key for females to show species-typical song perception and preferences. Although adult mating experience can still lead to pair-bonding and song preference learning even in birds with limited previous song exposure ("song-naive"), whether similarities in adult behavioral plasticity between normally reared and song-naive females reflect convergent patterns of neural activity is unknown. We investigated this using expression of a marker of neural activity and plasticity [phosphorylated S6 (pS6)] in mated normally reared and song-naive females in response to song from either their mate, a neighbor, or an unfamiliar male. We found that, in portions of a secondary auditory region (the caudomedial nidopallium, NCM) and in dopaminergic neurons of the caudal ventral tegmental area, hearing the mate's song significantly increased pS6 expression in females from both rearing conditions. In contrast, within other NCM subregions, song identity drove different patterns of pS6 expression depending on the rearing condition. These data suggest that developmental experiences can have long-lasting impacts on the neural signatures of behaviors acquired in adulthood and that socially driven behavioral plasticity in adults may arise through both shared and divergent neural circuits depending on an individual's developmental experiences.NEW & NOTEWORTHY Social and sensory experiences across the lifespan can shape social interactions. Female zebra finches form long-lasting social bonds with a male mate and preferences for his song; however, few studies have investigated how neural responses to the mate's song compare to responses to familiar or unfamiliar songs. We found multiple regions that differentially respond to the song of the mate, and, in some of these regions, responses were modulated by the female's previous auditory experience.

Keywords: auditory learning; female zebra finch; individual recognition; learning and memory; mate song learning.