Zebrin-Immunopositive and -Immunonegative Stripe Pairs Represent Functional Units in the Pigeon Vestibulocerebellum

The cerebellum is a site of complex sensorimotor integration and contains up to 80% of the neurons in the brain, yet comparatively little is known about the organization of sensorimotor systems within the cerebellum. It is known that afferent projections and Purkinje cell (PC) response properties are organized into sagittal "zones" in the cerebellum. Moreover, the isoenzyme aldolase C [also known as zebrin II (ZII)] is heterogeneously expressed in cerebellar PCs such that there are sagittal stripes of PCs with high expression (ZII+) interdigitated with stripes of little or no expression (ZII-). In the present study, we show how the ZII stripes in folium IXcd of the vestibulocerebellum in pigeons are related to response properties of PCs. IXcd consists of seven pairs of ZII+/- stripes denoted P1+/- (medial) to P7+/- (lateral). Electrophysiological studies have shown that vestibulocerebellar PCs respond to particular patterns of optic flow resulting from self-motion in three-dimensional space. In our study, we recorded optic flow preferences from PCs in IXcd, marked recording locations with injections of fluorescent tracer, and subsequently immunoreacted coronal sections for ZII. We found that the PCs within a ZII+/- stripe pair all responded best to the same pattern of optic flow. That is, a ZII+/- stripe pair forms a functional unit in the cerebellum. This is the first demonstration that the function of PCs is associated with ZII stripes across the mediolateral extent of an entire folium.