Social experiences shape song preference learning independently of developmental exposure to song.

Communication governs the formation and maintenance of social relationships. The interpretation of communication signals depends not only on the signal's content but also on a receiver's individual experience. Experiences throughout life may interact to affect behavioural plasticity, such that a lack of developmental sensory exposure could constrain adult learning, while salient adult social experiences could remedy developmental deficits. We investigated how experiences impact the formation and direction of female auditory preferences in the zebra finch. Zebra finches form long-lasting pair bonds and females learn preferences for their mate's vocalizations. We found that after 2 weeks of cohabitation with a male, females formed pair bonds and learned to prefer their partner's song regardless of whether they were reared with ('normally reared') or without ('song-naive') developmental exposure to song. In contrast, females that heard but did not physically interact with a male did not prefer his song. In addition, previous work has found that song-naive females do not show species-typical preferences for courtship song. We found that cohabitation with a male ameliorated this difference in preference. Thus, courtship and pair bonding, but not acoustic-only interactions, strongly influence preference learning regardless of rearing experience, and may dynamically drive auditory plasticity for recognition and preference.

Dopamine in the songbird auditory cortex shapes auditory preference.

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 1 week 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.

Acetylcholine in action.

The neurotransmitter acetylcholine influences how male finches perform courtship songs by acting on a region of the premotor cortex called HVC.