Holistic Motor Control of Zebra Finch Song Syllable Sequences

How brain circuits are organized to skillfully produce learned sequences of behaviors is still poorly understood. Here, we functionally examine how the 'cortical' song premotor region HVC, which is necessary for zebra finch song, controls the sequential production of learned song syllables. We find that HVC can generate the complete sequence of learned song syllables independently of its main synaptic input pathways. Thalamic input to HVC is permissive for song initiation but it is not required for transitions between syllables or completing song. We show that excitation of HVC neurons during song reliably causes vocalizations to skip back to the beginning of song, reminiscent of a skipping record. This restarting of syllable sequences can be induced at any moment in song and depends on local circuits within HVC. We identify and computationally model 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 behavior.