Differential Maturation of Climbing Fiber Innervation in Cerebellar Vermis

Folding of the brain surface is a general morphological adaptation to maximize surface area in a limited cranial volume. Surface folding is present not only in the neocortex but also in the cerebellar cortex. This folding creates subdivisions of the cortical surface: the sulci, the gyri, and the straight bank region, which is interposed. Is cortical folding only the solution to a surface-volume problem or does it also confer functional differences on the subdivisions that are created by this geometry? Here we have used the innervation of Purkinje cells by climbing fibers as a model system to explore potential functional differences. Purkinje cells are innervated by multiple climbing fibers at birth but undergo an activity-dependent refinement, such that by postnatal day (P) 21, most are contacted by a single climbing fiber. Using whole-cell recording from slices of cerebellar vermis derived from juvenile (P18-25) or adult (P60-83) mice, we found that significantly more Purkinje cells in the sulcus were innervated by multiple climbing fibers than in the gyrus or bank subdivisions; however, the basic properties of climbing fiber-Purkinje cell EPSCs such as kinetics, amplitude, and paired-pulse ratio were similar across cortical subdivisions. To search for a morphological correlate of differential multiple climbing fiber innervation, we labeled climbing fibers and performed reconstructions of immunofluorescent images. These revealed that, unlike the bank-gyrus subdivisions, most of the climbing fibers in the sulcus do not innervate the superficial molecular layer. These findings suggest that the subdivisions of the cerebellar cortex produced by folding may create functionally distinct entities.