Responses to Tactile Stimulation in Deep Cerebellar Nucleus Neurons Result From Recurrent Activation in Multiple Pathways

In a previous study, we found that neurons in the deep cerebellar nuclei (DCN) respond to 5-ms brief facial tactile stimulation in rats anesthetized with ketamine-xylazine with multiphasic response patterns lasting over 200 ms. It remained unclear, however, to what extent these responses were shaped not only by ascending sensory input from the trigeminal nuclei but also by interactions with other major cerebellar afferent systems, in particular the inferior olive (IO) and cerebral cortex. In the present study, we recorded from the IO, cerebral cortex, cerebellar granule cell layer (GCL), and DCN during the presentation of 5-ms facial tactile stimuli to elucidate potential mechanisms of how extended DCN response patterns are generated. We found that tactile stimulation resulted in robust multiphasic local field potentials responses in the IO as well as in the activation of a wide region of the somatosensory cortex (SI) and the primary motor cortex (MI). DCN neurons responded to electrical stimulation of any of these structures (IO, SI, and MI) with complex temporal patterns strikingly similar to air-puff lip stimulation responses. Simultaneous recordings from multiple structures revealed that long-lasting activation patterns elicited in DCN neurons were based on recurrent network activation in particular between the IO and the DCN with a potential contribution of DCN rebound properties. These results are consistent with the hypothesis that sensory stimulation triggers a feedback network activation of cerebellum, IO, and cerebral cortex to generate temporal patterns of activity that may control the timing of behavior.