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bioRxiv · 10.1101/2024.09.26.615128

Cerebellar control of targeted tongue movements

Bina, L.·Ciapponi, C.·Ju, S.-y.·Wang, X.·Bosman, L. W. J.·De Zeeuw, C. I.
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Abstract

The cerebellum is critical for coordinating movements related to eating, drinking and swallowing. Cerebellar Purkinje cell activity has been shown to encode ongoing tongue movements, but it is unclear how this activity can alter the trajectory of the tongue. To elucidate the impact of Purkinje cells on goal-directed tongue movements, we recorded their activity in the vermis and hemispheres during spontaneous licking from a stationary or moving water spout. Some Purkinje cells encode rhythmic tongue movements with their complex spikes, others with their simple spikes or a combination of both. Complex spikes predominantly marked the start and end of a licking bout, and thus encoded behavioural state changes, while simple spike firing was more related to individual licks. In addition, complex spikes reported unexpected changes in the position of the water spout and subsequent modulation of simple spike firing caused bending of the tongue, reaching out for the new target position. Using machine learning, we demonstrated that it is possible to predict licking activity based on the spiking patterns of individual Purkinje cells. Using optogenetic stimulation of Purkinje cells, we could experimentally replicate the impact of modulated simple spike firing, suggesting that increased simple spike activity indeed causes ipsilateral bending of the tongue during goal-directed movements. Our data highlight that directional control of movements is paramount in cerebellar function and that complex spike and simple spike modulation complement each other during sensorimotor coordination. These results bring us closer to understanding clinical implications of cerebellar disorders during eating, drinking and swallowing. Key pointsO_LIWhen drinking, mice make rhythmic tongue movements directed towards the water source. C_LIO_LICerebellar Purkinje cells can fire rhythmically in tune with the tongue movements. C_LIO_LIPurkinje cells encode changes in the position of the water source with complex spikes. C_LIO_LIPurkinje cell simple spike firing affects the direction of tongue movements. C_LIO_LIPurkinje cells that report changes in the position of the target can also adjust movements in the right direction. C_LI

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Bina, L., Ciapponi, C., Ju, S.-y., Wang, X., Bosman, L. W. J., De Zeeuw, C. I.. 2024-09-26. Cerebellar control of targeted tongue movements. https://doi.org/10.1101/2024.09.26.615128

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