Neural activity in cortico-basal ganglia circuits of juvenile songbirds encodes performance during goal-directed learning

Abstract

Cortico-basal ganglia circuits are thought to mediate goal-directed learning by a process of outcome evaluation to gradually select appropriate motor actions. We investigated spiking activity in CORE and SHELL subregions of the cortical nucleus LMAN during development as juvenile zebra finches are actively engaged in evaluating feedback of self-generated behavior in relation to their memorized tutor song (the goal). Spiking patterns of single neurons in both CORE and SHELL subregions during singing correlated with acoustic similarity to tutor syllables, suggesting a process of outcome evaluation. Both CORE and SHELL neurons encoded tutor similarity via either increases or decreases in firing rate, although only SHELL neurons showed a significant association at the population level. Tutor similarity predicted firing rates most strongly during early stages of learning, and SHELL but not CORE neurons showed decreases in response variability across development, suggesting that the activity of SHELL neurons reflects the progression of learning.