Discrete Evaluative and Premotor Circuits Enable Vocal Learning in Songbirds

Virtuosic motor performance requires the ability to evaluate and modify individual gestures within a complex motor sequence. Where and how the evaluative and premotor circuits operate within the brain to enable such temporally precise learning is poorly understood. Songbirds can learn to modify individual syllables within their complex vocal sequences, providing a system for elucidating the underlying evaluative and premotor circuits. We combined behavioral and optogenetic methods to identify 2 afferents to the ventral tegmental area (VTA) that serve evaluative roles in syllable-specific learning and to establish that downstream cortico-basal ganglia circuits serve a learning role that is only premotor. Furthermore, song performance-contingent optogenetic stimulation of either VTA afferent was sufficient to drive syllable-specific learning, and these learning effects were of opposite valence. Finally, functional, anatomical, and molecular studies support the idea that these evaluative afferents bidirectionally modulate VTA dopamine neurons to enable temporally precise vocal learning. •Two inputs onto songbird midbrain dopamine neurons evaluate song performance•Activating these evaluative inputs drives song learning effects of opposite valence•Physiology and anatomy reveal midbrain circuitry mediating these opposing effects•Downstream cortical neurons serve a premotor role to enable song learning Kearney et al. used behavioral and optogenetic methods in singing birds to distinguish neural pathways that evaluate song performance from downstream premotor circuits that are guided by these evaluations to learn new vocal behaviors.