Songbird subthalamic neurons signal song timing and error and project to dopaminergic midbrain

Abstract

Abstract Skill learning requires motor output to be evaluated against internal performance benchmarks. In songbirds, ventral tegmental area (VTA) dopamine neurons (DA) signal performance errors important for learning, but it remains unclear which brain regions project VTA and how these inputs may implement the sensorimotor comparisons necessary for error computation. Here we find that the songbird subthalamic nucleus (STN) projects to VTA and that STN microstimulation can excite VTA neurons. We also discover that STN receives inputs from auditory cortical and ventral pallidal brain regions previously implicated in song evaluation. In the first neural recordings from songbird STN, we discover that the activity of most STN neurons is associated with body movements and not singing, but a small fraction of neurons exhibits precise song timing and performance error signals consistent with performance evaluation. Together our results implicate the STN-VTA projection as an evolutionarily conserved pathway important for motor learning and expand the territories of songbird brain associated with song learning. New & Noteworthy Songbird subthalamic (STN) neurons exhibit song-timing and performance error signals and are interconnected with auditory pallium, ventral pallidum and ventral tegmental area, three areas important for song learning.