Dopamine in the songbird auditory cortex shapes auditory preference

Abstract

Vocal communication signals can provide listeners with information about the signaler and elicit motivated responses. Auditory cortical and mesolimbic reward circuits are often considered to have distinct roles in these processes, with auditory cortical circuits responsible for detecting and discriminating sounds and mesolimbic circuits responsible for ascribing salience and modulating preference for those sounds. Here, we investigated whether dopamine within auditory cortical circuits themselves can shape the incentive salience of a vocal signal. Female zebra finches demonstrate natural preferences for vocal signals produced by males ("songs"), and we found that brief pairing of passive song playback with pharmacological dopamine manipulations in the secondary auditory cortex significantly altered song preferences. In particular, pairing passive song playback with retrodialysis of dopamine agonists into the auditory cortex enhanced preferences for less-preferred songs. Plasticity of song preferences by dopamine persisted for at least 1week and was mediated by D1 receptors. In contrast, song preferences were not shaped by norepinephrine. In line with this, while we found that the ventral tegmental area, substantia nigra pars compacta, and locus coeruleus all project to the secondary auditory cortex, only dopamine-producing neurons in the ventral tegmental area differentially responded to preferred versus less-preferred songs. In contrast, norepinephrine neurons in the locus coeruleus increased expression of activity-dependent neural markers for both preferred and less-preferred songs. These data suggest that dopamine acting directly in sensory-processing areas can shape the incentive salience of communication signals.