Developmentally regulated pathways for motor skill learning in songbirds

Vocal learning in songbirds is mediated by cortico-basal ganglia circuits that govern diverse functions during different stages of development. We investigated developmental changes in axonal projections to and from motor cortical regions that underlie learned vocal behavior in juvenile zebra finches (Taeniopygia guttata). Neurons in LMAN-core project to RA, a motor cortical region that drives vocal output; these RA-projecting neurons send a transient collateral projection to AId, a region adjacent to RA, during early vocal development. Both RA and AId project to a region of dorsal thalamus (DLM), which forms a feedback pathway to cortico-basal ganglia circuitry. These projections provide pathways conveying efference copy and a means by which information about vocal motor output could be reintegrated into cortico-basal ganglia circuitry, potentially aiding in the refinement of juvenile vocalizations during learning. We used tract-tracing techniques to label the projections of LMAN-core to AId and of RA to DLM in juvenile songbirds. The volume and density of terminal label in the LMAN-core→AId projection declined substantially during early stages of sensorimotor learning. In contrast, the RA→DLM projection showed no developmental change. The retraction of LMAN-core→AId axon collaterals indicates a loss of efference copy to AId and suggests that projections that are present only during early stages of sensorimotor learning mediate unique, temporally restricted processes of goal-directed learning. Conversely, the persistence of the RA→DLM projection may serve to convey motor information forward to the thalamus to facilitate song production during both learning and maintenance of vocalizations.

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