Neuron
Volume 98, Issue 1, 4 April 2018, Pages 208-221.e5
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Article
A Basal Ganglia Circuit Sufficient to Guide Birdsong Learning

https://doi.org/10.1016/j.neuron.2018.02.020Get rights and content
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Highlights

  • Optogenetic excitation and inhibition of dopaminergic axon terminals in songbirds

  • Ventral tegmental area to basal ganglia pathway is sufficient to guide song learning

  • Activation and inhibition have opposing effects on song learning

  • Optogenetically learned changes in song are temporally and spectrally precise

Summary

Learning vocal behaviors, like speech and birdsong, is thought to rely on continued performance evaluation. Whether candidate performance evaluation circuits in the brain are sufficient to guide vocal learning is not known. Here, we test the sufficiency of VTA projections to the vocal basal ganglia in singing zebra finches, a songbird species that learns to produce a complex and stereotyped multi-syllabic courtship song during development. We optogenetically manipulate VTA axon terminals in singing birds contingent on how the pitch of an individual song syllable is naturally performed. We find that optical inhibition and excitation of VTA terminals are each sufficient to reliably guide learned changes in song. Inhibition and excitation have opponent effects on future performances of targeted song syllables, consistent with positive and negative reinforcement of performance outcomes. These findings define a central role for reinforcement mechanisms in learning vocalizations and demonstrate minimal circuit elements for learning vocal behaviors.

Keywords

vocal learning
reinforcement learning
songbird
birdsong
optogenetics
basal ganglia
dopamine
skill learning
ventral tegmental area
zebra finch

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