The songbird lateral habenula projects to dopaminergic midbrain and is important for normal vocal development

Mistakes in performance feel disappointing, suggesting that brain pathways for aversive feedback may play a role in motor learning. Here we tested if the lateral habenula (LHb), an evolutionarily conserved part of the limbic system known in mammals to relay aversive feedback from ventral pallidum (VP) to ventral tegmental area (VTA) dopamine neurons, is involved in birdsong learning and production. By combining viral tract tracing and functional circuit mapping, we discovered that songbird LHb links VP and an auditory cortical area to singing-related DA neurons that signal song errors. As in mammals, VP stimulation activated LHb activity and LHb stimulation suppressed DA firing. To test this pathway’s role in learning we lesioned the LHb in juvenile zebra finches and recorded their songs in adulthood. Birds with the LHb lesioned as juveniles produced highly unusual vocalizations as adults, including prolonged high-pitch notes and species-atypical trills. These findings identify a songbird VP-LHb-VTA pathway with similar functional connectivity as mammals, expand the known territories of vocal learning circuits, and demonstrate that limbic circuits associated with disappointing outcomes are important for motor performance learning.