A lobule-specific neuronal representation of song temporal structure in the songbird cerebellum

Abstract

The cerebellum is involved in the acquisition and production of speech as revealed by clinical evidence and imaging studies, but its specific role however remains unclear. Songbirds provide a unique model to study the neural mechanisms of speech learning and production. Recent evidence highlights a contribution of the cerebellum to syllable duration in songbirds. Here, we aim at better understanding how and which cerebellar circuits may contribute to the tight control of syllable duration in zebra finches. We first confirmed that lesions in the lateral cerebellum affect syllable duration. We then recorded neuronal activity in the various cerebellar lobules in response to song playback and during singing with or without auditory feedback perturbation. We found that many cerebellar lobules receive non-selective auditory information locked to syllable boundaries during song playback, both in anaesthetized and awake behaving birds. During singing, cerebellar neurons in several lobules display song-locked responses with varying degrees of alignment to their playback responses and no alteration during auditory feedback perturbation. Singing-related activity tends to correlate with the fluctuations in syllable duration rather than any acoustic song feature. Importantly, neurons in lobule IV of the cerebellum are largely unaffected by auditory stimulation but display syllable-locked firing rate modulations during singing that precisely encode syllable boundaries with a sharp and tight increase in firing at syllable onsets and offsets. Altogether, our findings reveal cerebellar signals that may contribute to the control of the duration of vocal elements during singing, possibly serving as a forward model of song temporal features.