Cerebellar control of targeted tongue movements

The cerebellum is critical for coordinating movements related to eating, drinking and swallowing, all of which require proper control of the tongue. Cerebellar Purkinje cells can encode tongue movements, but it is unclear how their simple spikes and complex spikes induce changes in the shape of the tongue that contribute to goal-directed movements. To study these relations, we recorded and stimulated Purkinje cells in the vermis and hemispheres of mice during spontaneous licking from a stationary or moving water spout. We found that Purkinje cells can encode rhythmic licking with both their simple spikes and complex spikes. Increased simple spike firing during tongue protrusion induces ipsiversive bending of the tongue. Unexpected changes in the target location trigger complex spikes that alter simple spike firing during subsequent licks, adjusting the tongue trajectory. Furthermore, we observed increased complex spike firing during behavioural state changes at both the start and the end of licking bouts. Using machine learning, we confirmed that alterations in Purkinje cell activity accompany licking, with different Purkinje cells often exerting heterogeneous encoding schemes. Our data highlight that directional movement control is paramount in cerebellar function and that modulation of the complex spikes and that of the simple spikes are complementary during acquisition and execution of sensorimotor coordination. These results bring us closer to understanding the clinical implications of cerebellar disorders during eating, drinking and swallowing. KEY POINTS: When drinking, mice make rhythmic tongue movements directed towards the water source. Cerebellar Purkinje cells can fire rhythmically in tune with the tongue movements. Purkinje cells encode changes in the position of the water source with complex spikes. Purkinje cell simple spike firing affects the direction of tongue movements. Purkinje cells that report changes in the position of the target can also adjust movements in the right direction.