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Sensorimotor Processing and Control of Whisker Movements by Principal Neurons of the Cerebellum in Mice

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The cerebellum is involved in sensorimotor processing and motor control in the brain. What has been found across many species for many behaviors is cerebellar Purkinje (Pkj) cells and cerebellar nuclear (CbN) cells show activity that is related to and predictive of movements. Less is known about how patterns of activity arising in Pkj cells and CbN cells are transformed into motor behavior. Here, we make use of the mouse whisker system to explore sensorimotor processing within the principal cells of the cerebellar cortex and cerebellar nuclei and how it contributes to the production of whisker movements. We find that both cell types show whisking-modulated activity that is correlated with sensory-evoked and spontaneous whisker movements. With air puffs to the whisker pad, Pkj cells show early cycles of suppression that correspond with elevations of CbN cell firing. Using optogenetic suppression of CbN cells, we demonstrate that CbN cell responses associated with air puffs contribute to ~30% of the amplitude of sensory-evoked movements. Similar to responses to air puffs, we find that contacting the whiskers with a metal bar elicits a brief suppression followed by a prolonged increase in firing of Pkj cells along with a robust complex spike response. As with air puffs, CbN cells fired maximally during the Pkj cell suppression. In contrast, when mice actively protracted their whiskers into the bar, we found increases in firing rate in Pkj cells and CbN cells associated with the whisker movements, but no change in complex spike firing nor suppression in Pkj cells. Together, these data demonstrate that crus I, crus II, and the lateral nucleus of the cerebellum make up a central hub for whisker-related sensorimotor processing and likely contributes to the control of reflexive and volitional whisker movements.

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