Coding of tactile response properties in the rat deep cerebellar nuclei

Abstract

In the lateral hemispheres of the cerebellar cortex, somatosensory responses are represented in a finely grained fractured somatotopy. It is unclear, however, how these responses contribute to the ultimate output of the cerebellum from the deep cerebellar nuclei (DCN). Robust responses of DCN neurons to somatosensory stimuli have been described, but a detailed examination of their somatotopic arrangement and stimulus coding properties is lacking. To address these questions, we recorded extracellular, single-unit activity in the DCN of ketamine-anesthetized rats in response to air-puff stimuli aimed at six different orofacial and forelimb locations. In additional experiments, the duration and intensity of air-puff stimuli to the ipsilateral upper lip were systematically varied. Overall, we found that DCN neuron responses to air puff stimuli showed combinations of three distinct response components: a short-latency spike response, a pronounced inhibition, and a long-latency increase in firing. Individual neurons responsive to air-puff stimulation exhibited any combination of just one, two, or all three of these response components. The inhibitory response was most common and frequently consisted of a complete cessation of spiking despite a high spontaneous rate of baseline firing. In contrast to published findings from cerebellar cortical recordings, the receptive fields of all responsive neurons in the DCN were large. In fact, the receptive field of most neurons covered the ipsi- and contralateral face as well as forepaws. Response properties of individual neurons did not reliably indicate stimulus intensity or duration, although as a population DCN neurons showed significantly increasing response amplitudes as air-puff intensity or duration increased. Overall, the responses were characterized by a distinct temporal profile in each neuron, which remained unchanged with changes in stimulus condition. We conclude that the responses in the DCN of rats to air-puff stimuli differ substantially from cerebellar cortical responses in their receptive field properties and do not provide a robust code of tactile stimulus properties. Rather, the characteristic temporal response profile of each neuron may be tuned to control the timing of a specific task to which its output is linked.