What Is the Role of Thalamostriatal Circuits in Learning Vocal Sequences?

Abstract

Basal ganglia (BG) circuits integrate sensory and motor-related information from the cortex, thalamus, and midbrain to guide learning and production of motor sequences. Birdsong, like speech, is comprised of precisely sequenced vocal elements. Learning song sequences during development relies on Area X, a vocalization related region in the medial striatum of the songbird BG. Area X receives inputs from cortical-like pallial song circuits and midbrain dopaminergic circuits and sends projections to the thalamus. It has recently been shown that thalamic circuits also send substantial projections back to Area X. Here, we outline a gated-reinforcement learning model for how Area X may use signals conveyed by thalamostriatal inputs to direct song learning. Integrating conceptual advances from recent mammalian and songbird literature, we hypothesize that thalamostriatal pathways convey signals linked to song syllable onsets and offsets and influence striatal circuit plasticity via regulation of cholinergic interneurons (ChIs). We suggest that syllable sequence associated vocal-motor information from the thalamus drive precisely timed pauses in ChIs activity in Area X. When integrated with concurrent corticostriatal and dopaminergic input, this circuit helps regulate plasticity on medium spiny neurons (MSNs) and the learning of syllable sequences. We discuss new approaches that can be applied to test core ideas of this model and how associated insights may provide a framework for understanding the function of BG circuits in learning motor sequences.