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Dopamine neurons encode performance error in singing birds

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Science  09 Dec 2016:
Vol. 354, Issue 6317, pp. 1278-1282
DOI: 10.1126/science.aah6837

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Birds of a feather sing together

How do birds know that a song that they hear is from a member of their own species, and how do they learn their songs in the first place? Araki et al. identified two types of brain cells involved in how finches learn their songs (see the Perspective by Tchernichovski and Lipkind). When zebra finches were raised by Bengalese finch foster parents, they learned a song whose morphology resembled that of their foster father. However, the temporal structure remained zebra finch–specific, suggesting that it is innate. Gadagkar et al. recorded activity in specific dopamine neurons in singing zebra finches while controlling perceived song quality with distorted auditory feedback. This distorted feedback represented worse performance than predicted and resulted in negative prediction errors. These findings suggest again that finches have an innate internal goal for their learned songs.

Science, this issue p. 1282, p. 1234; see also p. 1278

Abstract

Many behaviors are learned through trial and error by matching performance to internal goals. Yet neural mechanisms of performance evaluation remain poorly understood. We recorded basal ganglia–projecting dopamine neurons in singing zebra finches as we controlled perceived song quality with distorted auditory feedback. Dopamine activity was phasically suppressed after distorted syllables, consistent with a worse-than-predicted outcome, and was phasically activated at the precise moment of the song when a predicted distortion did not occur, consistent with a better-than-predicted outcome. Error response magnitude depended on distortion probability. Thus, dopaminergic error signals can evaluate behaviors that are not learned for reward and are instead learned by matching performance outcomes to internal goals.

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