Divergent topographic projection of cerebral cortical areas to overlapping cerebellar lobules through distinct regions of the pontine nuclei.

The massive axonal projection from the cerebrum to the cerebellum through the pontine nuclei supports the cerebrocerebellar coordination of motor and nonmotor functions. However, the cerebrum and cerebellum have distinct patterns of functional localization in their cortices. We addressed this issue by bidirectional neuronal tracing from 22 various locations of the pontine nuclei in the mouse in a comprehensive manner. Cluster analyses of the distribution patterns of labeled cortical pyramidal cells and cerebellar mossy fiber terminals classified all cases into six groups located in six different subareas of the pontine nuclei. The lateral (insular), mediorostral (cingulate and prefrontal), and caudal (visual and auditory) cortical areas of the cerebrum projected to the medial, rostral, and lateral subareas of the pontine nuclei, respectively. These pontine subareas then projected mainly to the crus I, central vermis, and paraflocculus divergently. The central (motor and somatosensory) cortical areas projected to the centrorostral, centrocaudal and caudal subareas of the pontine nuclei, which then projected mainly to the rostral and caudal lobules with a somatotopic arrangement. The results indicate a new pontine nuclei-centric view of the corticopontocerebellar projection: the generally parallel corticopontine projection to pontine nuclei subareas is relayed to the highly divergent pontocerebellar projection terminating in overlapping specific lobules of the cerebellum. Consequently, the mode of the pontine nuclei relay underlies the cerebellar functional organization.

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

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.