Performance-Dependent Consolidation of Learned Vocal Changes in Adult Songbirds

Abstract

Motor skills learned through practice are consolidated at later time, which can include nighttime, but the time course of motor memory consolidation and its underlying mechanisms remain poorly understood. We investigated neural substrates underlying motor memory consolidation of learned changes in birdsong, a tractable model system for studying neural basis of motor skill learning. Previous studies in male zebra finches and Bengalese finches have demonstrated that adaptive changes in adult song structure learned through a reinforcement paradigm are initially driven by a cortical-basal ganglia circuit, and subsequently consolidated into downstream cortical motor circuitry. However, the time course of the consolidation process, including whether it occurs offline during nighttime or online during daytime, remains unclear and even controversial. Here, we provide in both species experimental evidence of virtually no consolidation of learned vocal changes during nighttime. We demonstrate instead that the consolidation occurs during daytime and the amount of consolidation is strongly correlated with the amount of learning, suggesting online, performance-dependent mechanisms of consolidation of learned vocal changes. Moreover, by using computer simulations based on our experimental results, we demonstrate that such online, performance-dependent consolidation can account for the contradicting conclusions concerning the time course of consolidation process reached by previous studies. These results thus reconcile a controversy in the study of vocal motor consolidation in songbirds, and illustrate the neural substrates through which newly learned motor skills initially implemented by corticalbasal ganglia circuits become encoded in the cortical motor circuitry.