A hypothesis for basal ganglia-dependent reinforcement learning in the songbird

Most of our motor skills are not innately programmed, but are learned by a combination of motor exploration and performance evaluation, suggesting that they proceed through a reinforcement learning (RL) mechanism. Songbirds have emerged as a model system to study how a complex behavioral sequence can be learned through an RL-like strategy. Interestingly, like motor sequence learning in mammals, song learning in birds requires a basal ganglia (BG)-thalamocortical loop, suggesting common neural mechanisms. Here, we outline a specific working hypothesis for how BG-forebrain circuits could utilize an internally computed reinforcement signal to direct song learning. Our model includes a number of general concepts borrowed from the mammalian BG literature, including a dopaminergic reward prediction error and dopamine-mediated plasticity at corticostriatal synapses. We also invoke a number of conceptual advances arising from recent observations in the songbird. Specifically, there is evidence for a specialized cortical circuit that adds trial-to-trial variability to stereotyped cortical motor programs, and a role for the BG in “biasing” this variability to improve behavioral performance. This BG-dependent “premotor bias” may in turn guide plasticity in downstream cortical synapses to consolidate recently learned song changes. Given the similarity between mammalian and songbird BG-thalamocortical circuits, our model for the role of the BG in this process may have broader relevance to mammalian BG function.This article is part of a Special Issue entitled: Function and Dysfunction of the Basal Ganglia.

▶The songbird has emerged as a model system to study learning of complex behaviors. ▶We present a specific hypothesis for how BG-forebrain circuits direct song learning. ▶The output of specialized variability-generating circuits is evaluated by MSNs. ▶A dopaminergic reward drives plasticity at corticostriatal synapses. ▶MSNs then “bias” variability in favor of improved song performance.