A cortically gated sensory reference to the basal ganglia guides vocal reinforcement learning in songbirds

Abstract

Songbirds learn to sing by copying a memorized tutor song. Reinforcement learning models of vocal imitation propose that a dopaminergic signal strengthens the cortico basal ganglia synapses whose activity coincides with similarity to the tutor like song. To do so, the circuit must access a representation of the tutor song. Whether such a reference is available within the songbird basal ganglia nucleus Area X, and how it arrives, is unknown. In juvenile male zebra finches that learn to imitate adult courtship songs, we found that lesions of Area X impaired imitation more severely the earlier they were made. Intracellular recordings from Area X in awake juvenile zebra finches showed that the tutor song evokes precise subthreshold depolarizations that inversely scaled with imitation proficiency throughout song learning. Silencing the upstream nucleus HVC reduced these tutor-evoked responses, whereas disinhibiting HVC enhanced them. An inhibitory gate in HVC thus supplies Area X with the temporally aligned tutor reference that reinforcement driven vocal learning requires. These findings uncover a critical missing link in biological reinforcement learning, revealing how the brain structurally routes sensory templates to the basal ganglia to guide the acquisition of complex motor skills.