Hidden neural states underlie canary song syntax.

Coordinated skills such as speech or dance involve sequences of actions that follow syntactic rules in which transitions between elements depend on the identity and order of past actions. Canary songs are comprised of repeated syllables, called phrases, and the ordering of these phrases follows long-range rules(1), where the choice of what to sing depends on song structure many seconds prior. The neural substrates that support these long-range correlations are unknown. Using miniature head-mounted microscopes and cell-type-specific genetic tools, we observed neural activity in the premotor nucleus HVC(2–4) as canaries explore various phrase sequences in their repertoire. We find neurons that encode past transitions, extending over 4 phrases and spanning up to 4 seconds and 40 syllables. These neurons preferentially encode past actions rather than future actions, can reflect more than a single song history, and occur mostly during the rare phrases that involve history-dependent transitions in song. These findings demonstrate that HVC dynamics includes “hidden states” not reflected in ongoing behavior – states that carry information about prior actions. These states provide a possible substrate to control syntax transitions governed by long-range rules.