Songbird Ventral Basal Ganglia Sends Performance Error Signals to Dopaminergic Midbrain

Abstract

Ventral tegmental area (VTA) dopamine neurons signal prediction error, the difference between actual and predicted outcome, but it remains unclear how error is computed. Here we identify in songbirds a ventral basal ganglia (vBG) region that is required for song learning and that sends prediction error signals to VTA. During singing, vBG neurons heterogeneously encoded song timing, auditory error, predicted error, and the difference between the two (prediction error). Viral tracing revealed inputs to vBG from auditory and vocal motor thalamus, auditory and vocal motor cortex, and VTA. Our findings reveal a classic actor-critic circuit motif in which a ventral critic learns the ‘prediction’ component of a prediction error signal that is relayed by VTA to a dorsal actor (the vocal motor BG nucleus Area X). A circuit motif for computing reward prediction error can compute predicted performance quality during motor sequence learning.