Dataset Information

A Basal Ganglia Circuit Sufficient to Guide Birdsong Learning.

ABSTRACT: 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. VIDEO ABSTRACT.

SUBMITTER: Xiao L

PROVIDER: S-EPMC5918681 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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A Basal Ganglia Circuit Sufficient to Guide Birdsong Learning.

Xiao Lei L Chattree Gaurav G Oscos Francisco Garcia FG Cao Mou M Wanat Matthew J MJ Roberts Todd F TF

Neuron 20180315 1

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 sing ...[more]

PMID: 29551492

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Project description:We learn complex skills such as speech and dance through a gradual process of trial and error. Cortical-basal ganglia circuits have an important yet unresolved function in this trial-and-error skill learning; influential 'actor-critic' models propose that basal ganglia circuits generate a variety of behaviours during training and learn to implement the successful behaviours in their repertoire. Here we show that the anterior forebrain pathway (AFP), a cortical-basal ganglia circuit, contributes to skill learning even when it does not contribute to such 'exploratory' variation in behavioural performance during training. Blocking the output of the AFP while training Bengalese finches to modify their songs prevented the gradual improvement that normally occurs in this complex skill during training. However, unblocking the output of the AFP after training caused an immediate transition from naive performance to excellent performance, indicating that the AFP covertly gained the ability to implement learned skill performance without contributing to skill practice. In contrast, inactivating the output nucleus of the AFP during training completely prevented learning, indicating that learning requires activity within the AFP during training. Our results suggest a revised model of skill learning: basal ganglia circuits can monitor the consequences of behavioural variation produced by other brain regions and then direct those brain regions to implement more successful behaviours. The ability of the AFP to identify successful performances generated by other brain regions indicates that basal ganglia circuits receive a detailed efference copy of premotor activity in those regions. The capacity of the AFP to implement successful performances that were initially produced by other brain regions indicates precise functional connections between basal ganglia circuits and the motor regions that directly control performance.

Dataset Information

A Basal Ganglia Circuit Sufficient to Guide Birdsong Learning.

Publications

A Basal Ganglia Circuit Sufficient to Guide Birdsong Learning.

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