Songbird subthalamic neurons project to dopaminergic midbrain and exhibit singing-related activity

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 to VTA and how these inputs may contribute to DA error signaling. 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 motor cortical, 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. Our results place the STN in a pathway important for song learning, but not song production, and expand the territories of songbird brain potentially associated with song learning.NEW & NOTEWORTHY Songbird subthalamic (STN) neurons exhibit singing-related signals and are interconnected with the motor cortical nucleus, auditory pallium, ventral pallidum, and ventral tegmental area, areas important for song generation and learning.