The compartmentalization of the monkey and rat cerebellar cortex: zebrin I and cytochrome oxidase

Abstract

The cerebellar cortex of mammals is composed of parasagittal zones that encompass the afferent inputs, the efferent corticonuclear and corticovestibular projections, and a number of intrinsic molecular markers. One such marker is the polypeptide antigen zebrin I that is recognized by monoclonal antibody (mab) Q113. In rodents, zebrin I immunocytochemistry reveals an array of parasagittal Purkinje cell compartments. In the present study, zebrin I has been used to reveal the molecular heterogeneity of the cerebellar cortex in the squirrel monkey ( Saimiri sciureus). As in rodents, zebrin I is Purkinje cell specific in the primate cerebellum and not all Purkinje cells are immunoreactive. Immunocytochemistry on frontal or horizontal sections reveals a system of bands of zebrin I + cells extending through the vermis of both anterior and posterior lobes. A midline (P1 +) band and two more lateral bands (P2 + and P3 +) are found in all lobules. The situation in the paravermis and hemispheres is similar, with alternating zebrin I + and zebrin I − compartments, but the complex lobulation obscures the precise band pattern: it seems probable that 4 additional bands are present in the hemispheres, as in rodents. Comparison of rat and monkey cerebellums suggests that the cortex has expanded in primates by the growth of the same individual bands found in rats rather than by the addition of supplementary compartments. The zebrin I compartmentalization revealed by using mab Q113 is reproducible from individual and thus provides a stable frame of reference that has been used to compare the different chemoarchitectonic patterns found in the cerebellar cortex. In the present study, the histochemical zonation of cytochrome oxidase (CO) is compared with the Purkinje cell compartmentalization revealed by zebrin I immunoreactivity in the rat and monkey cerebellar cortex. In the adult rat, the CO zonation is present in the molecular and granular layers and respects the same architectonic boundaries as zebrin I. The high CO-activity bands coincide with the zebrin I − and the CO-weak bands with the zebrin I + compartments. In contrast, in the cerebellar cortex of the squirrel monkey, the CO band pattern occurs predominantly in the granular layer. Nevertheless, there is still a precise correspondence to the zebrin I zonation. However, in the monkey the CO-rich bands coincide with the zebrin I + compartments and CO-weak bands with zebrin I − zones. The differential CO expression between Purkinje cell compartments is present in rat from birth, suggesting that it is a fundamental characteristic of the zebrin I phenotype and not a secondary response to patterns of use.