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The basal ganglia (BG) participate in aspects of reinforcement learning that require evaluation and selection of motor programs associated with improved performance. However, whether the BG additionally contribute to behavioral variation ("motor exploration") that forms the substrate for such learning remains unclear. In songbirds, a tractable system for studying BG-dependent skill learning, a role for the BG in generating exploratory variability, has been challenged by the finding that lesions of Area X, the song-specific component of the BG, have no lasting effects on several forms of vocal variability that have been studied.

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Discrimination between spoken words composed of overlapping elements, such as "captain" and "captive," relies on sensitivity to unique combinations of prefix and suffix elements that span a "uniqueness point" where the word candidates diverge. To model such combinatorial processing, adult female zebra finches were trained to discriminate between target and distractor syllable sequences that shared overlapping "contextual" prefixes and differed only in their "informative" suffixes. The transition from contextual to informative syllables thus created a uniqueness point analogous to that present between overlapping word candidates, where targets and distractors diverged.

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Naturalistic stimulation drives opposing heterosynaptic plasticity at two inputs to songbird cortex.

Nat Neurosci

September 2015

Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, California, USA.

Songbirds learn precisely sequenced motor skills (songs) subserved by distinct brain areas, including the premotor cortical analog HVC, which is essential for producing learned song, and a 'cortical'-basal ganglia loop required for song plasticity. Inputs from these nuclei converge in RA (robust nucleus of the arcopallium), making it a likely locus for song learning. However, activity-dependent synaptic plasticity has never been described in either input.

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Accumulating evidence suggests that dopamine (DA) is involved in altering neural activity and gene expression in a zebra finch cortical-basal ganglia circuit specialized for singing, upon the shift between solitary singing and singing as a part of courtship. Our objective here was to sample changes in the extracellular concentrations of DA in Area X of adult and juvenile birds, to test the hypothesis that DA levels would change similarly during presentation of a socially salient stimulus in both age groups. We used microdialysis to sample the extracellular milieu of Area X in awake, behaving adult and juvenile male zebra finches, and analysed the dialysate using high-performance liquid chromatography coupled with electrochemical detection.

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Emergence of context-dependent variability across a basal ganglia network.

Neuron

April 2014

Department of Psychiatry, University of California, San Francisco, San Francisco, CA 94158, USA; Department of Physiology, University of California, San Francisco, San Francisco, CA 94158, USA.

Context dependence is a key feature of cortical-basal ganglia circuit activity, and in songbirds the cortical outflow of a basal ganglia circuit specialized for song, LMAN, shows striking increases in trial-by-trial variability and bursting when birds sing alone rather than to females. To reveal where this variability and its social regulation emerge, we recorded stepwise from corticostriatal (HVC) neurons and their target spiny and pallidal neurons in Area X. We find that corticostriatal and spiny neurons both show precise singing-related firing across both social settings.

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