Dense projection of Stilling’s nucleus spinocerebellar axons that convey tail proprioception to the midline area in lobule VIII of the mouse cerebellum

Abstract

The cerebellar cortex has dual somatotopic representation, broadly in the anterior lobules and narrowly in the posterior lobules. However, the somatotopy has not been well understood in vermal lobule VIII, located in the center of the posterior representation. Here, we examined the axonal projections and somatosensory representation of the midline area of vermal lobule VIII in mice, using the striped zebrin expression pattern as a landmark of intra-lobular compartmentalization. Retrograde tracer injection into this area (zebrin stripes 1+ and 1− in lobule VIII) labeled neuronal clusters, bilaterally, in the pericanal gray matter (Stilling’s nucleus) in the sacral spinal cord. Spinocerebellar axons labeled by biotinylated dextran amine injection into the sacral pericanal gray matter terminated bilaterally in stripes 1+ and 1− in lobule VIII, with more than 70 terminals per axon, and the vermal stripes in lobules II–III. Dorsal flexion of the tail and electrical stimulation of the sacral spinal gray matter elicited the firing of mossy fiber terminals in stripes 1+ and 1− in lobule VIII. Anterograde labeling of Purkinje cell axons in this area showed terminals in the medial pole of the medial cerebellar nucleus. Lesioning of this area impaired locomotor performance in the rotarod test. These results demonstrated that stripes 1+ and 1− in lobule VIII receive tail proprioceptive sensation from the Stilling’s nucleus as their predominant mossy fiber input. The results also suggest that locomotion-related activity is represented not only in the anterior lobule, but also in lobule VIII in the cerebellar vermis.