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Interruption of a basal ganglia–forebrain circuit prevents plasticity of learned vocalizations

Abstract

Birdsong, like speech, is a learned vocal behaviour that relies greatly on hearing; in both songbirds1 and humans2 the removal of auditory feedback by deafening leads to a gradual deterioration of adult vocal production. Here we investigate the neural mechanisms that contribute to the processing of auditory feedback during the maintenance of song in adult zebra finches. We show that the deleterious effects on song production that normally follow deafening can be prevented by a second insult to the nervous system—the lesion of a basal ganglia–forebrain circuit. The results suggest that the removal of auditory feedback leads to the generation of an instructive signal that actively drives non-adaptive changes in song; they also suggest that this instructive signal is generated within (or conveyed through) the basal ganglia–forebrain pathway. Our findings provide evidence that cortical-basal ganglia circuits may participate in the evaluation of sensory feedback during calibration of motor performance, and demonstrate that damage to such circuits can have little effect on previously learned behaviour while conspicuously disrupting the capacity to adaptively modify that behaviour.

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Figure 1: Hypothetical flow of auditory feedback through the song system.
Figure 2: Song system nuclei in intact and lesioned birds.
Figure 3: Changes to song following deafening in intact and lesioned birds.
Figure 4: Summary of song stability following deafening of intact or LMAN lesioned birds.

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Acknowledgements

We thank M. Stryker, M. Churchland, T. Troyer and K. T. Moortgat for comments on the manuscript, and A. Arteseros, G. Carrillo and A. Tam for technical assistance. This work was supported by a Burroughs Wellcome Fund fellowship of the Life Sciences Research Foundation (M.S.B.), and by the John Merck Fund, the EJLB Foundation and the National Institutes of Health (A.J.D.).

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Correspondence to Michael S. Brainard.

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Brainard, M., Doupe, A. Interruption of a basal ganglia–forebrain circuit prevents plasticity of learned vocalizations. Nature 404, 762–766 (2000). https://doi.org/10.1038/35008083

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