Learning by imitation is the foundation for verbal and musical expression, but its neural basis remains unclear. A juvenile male zebra finch imitates the multisyllabic song of an adult tutor in a process that depends on a song-specialized cortico-basal ganglia circuit1–4, affording a powerful system to identify the synaptic substrates of imitative motor learning. Plasticity at a particular set of cortico-basal ganglia synapses is hypothesized to drive rapid learning-related changes in song before these changes are subsequently consolidated in downstream circuits5. Nevertheless, this hypothesis is untested and the synaptic locus where learning initially occurs is unclear. Here, by combining a computational framework to quantify song learning with synapse-specific optogenetic and chemogenetic manipulations within and downstream of the cortico-basal ganglia circuit, we identified the specific cortico-basal ganglia synapses that drive the acquisition and expression of rapid vocal changes during juvenile song learning and characterized the hours-long timescale over which these changes consolidate. Furthermore, transiently augmenting postsynaptic activity in the basal ganglia briefly accelerates learning rates and persistently alters song, demonstrating a direct link between basal ganglia activity and rapid learning. These results localize the specific cortico-basal ganglia synapses that enable a juvenile songbird to learn to sing and reveal the circuit logic and behavioural timescales of this imitative learning paradigm.
