A common neural circuit mechanism for internally guided and externally reinforced forms of motor learning

The complex skills underlying verbal and musical expression can be learned without external punishment or reward, indicating their learning is internally guided. The neural mechanisms that mediate internally guided learning are poorly understood, but a circuit comprising dopamine-releasing neurons in the midbrain ventral tegmental area (VTA) and their targets in the basal ganglia are important to externally reinforced learning. Juvenile zebra finches copy a tutor song in a process that is internally guided and, in adulthood, can learn to modify the fundamental frequency (pitch) of a target syllable in response to external reinforcement with white noise. Here we combined intersectional genetic ablation of VTA neurons, reversible blockade of dopamine receptors in the basal ganglia, and singing-triggered optogenetic stimulation of VTA terminals to establish that a common VTA–basal ganglia circuit enables internally guided song copying and externally reinforced syllable pitch learning. Intersectional gene ablation, pharmacology & song-triggered optogenetic stimulation of VTA terminals together show a common VTA–basal ganglia circuit enabling internally and externally guided juvenile song-copying and adult pitch learning in finches.