How brain circuits are organized to skillfully produce learned sequences of behaviours is still poorly understood. Here we functionally examined how the cortical song premotor region HVC, which is necessary for zebra finch song1, controls the sequential production of learned song syllables. We found that HVC could generate the complete sequence of learned song syllables independently of its main synaptic input pathways. Thalamic input to HVC was needed for song initiation, but it was not required for transitions between syllables or for song completion. We showed that excitation of HVC neurons during song reliably caused vocalizations to skip back to the beginning of the song, in a manner reminiscent of a skipping record. This restarting of syllable sequences could be induced at any moment of the song and relied on local circuits within HVC. We identified and computationally modelled a synaptic network, including intratelencephalic premotor and corticostriatal neurons within HVC that are essential for completing song syllable sequences. Together, our results show that the learned zebra finch song is controlled by a cortical sequence-generating network in HVC that, once started, can sustain production of all song syllables independent of major extrinsic input pathways. Thus, sequential neuronal activity can be organized to fuse well-learned vocal motor sequences, ultimately achieving holistic control of this naturally learned behaviour.
