Control of tongue movements by the Purkinje cells of the cerebellum

Abstract

AbstractTo quantify the cerebellum’s contributions to control of the tongue, we trained head-fixed marmosets to make dexterous movements, harvesting food from small tubes that were placed orthogonal to the mouth. We identified the lingual regions in lobule VI of the vermis and recorded from hundreds of Purkinje cells (P-cells), each in sessions where the subject produced thousands of licks. Most movements aimed for one of the small tubes, while other movements groomed the mouth area. To quantify contributions of a P-cell to control of the tongue, we relied on the fact that in a small fraction of the licks, the input from the inferior olive produced a complex spike (CS), which then briefly but completely silenced the P-cell. When the movements were targeting a tube, the CS rates increased during protraction for both ipsilateral and contralateral targets, thus identifying the preferred axis of motion in the olivary input, termed CS-on. However, for grooming movements this modulation was absent. We compared the tongue’s trajectory in the targeted movement that had experienced the CS with temporally adjacent targeted licks that had not. When the SS suppression occurred during protraction, the tongue exhibited hypermetria, and when the suppression took place during retraction, the tongue exhibited slowing. These effects amplified when two P-cells were simultaneously suppressed. Therefore, CS-induced suppression of P-cells in the lingual vermis disrupted the forces that would normally decelerate the tongue as it approached the target, demonstrating a specialization in stopping the movement. Because the CS-on direction tended to align with the direction of downstream forces produced during P-cell suppression, this suggests that for targeted licks, the olivary input defined an axis of control for the P-cells.Significance statementDuring dexterous licking, a CS-induced suppression of P-cells in the lingual vermis inhibited the forces that would otherwise retract the tongue, resulting in hypermetria during protraction and slowing during retraction. Because the direction of these forces aligned with the direction of motion specified by the olivary input, a pattern that is also present for P-cells in the oculomotor region of the cerebellum, the results imply a general computation for P-cells during control of targeted movements.