Postnatal development of the inferior olivary complex in the rat. II. Topographic organization of the immature olivocerebellar projection

Abstract

The state of organization of the olivocerebellar projection in newborn and 5-day-old rats has been analyzed by autoradiography of anterogradely transported ³H-leucine, as well as by retrograde transport of horseradish peroxidase. The efferent axons of the inferior olivary neurons are already present and already highly organized in the cerebellum of newborn rats. Most of the autoradiographic labelling subsequent to the injection of ³H-leucine into the inferior olive is seen in the subcortical medullary zone. Labelled axons only partially invade the gray matter, where they reach the zone occupied by randomly distributed Purkinje cells. At this immature stage, olivocerebellar projections are already entirely crossed and distributed according to a pattern which is similar to the adult. At the fifth postnatal day olivocerebellar projections have moved from the medullary zone toward the interface between the molecular and the granular layers where Purkinje cells have arranged in a monolayer. Evidence for translocation of climbing fibers from their perisomatic to their peridendritic position is already distinct in these young cerebella. Combination of anterograde and retrograde fiber system tracing experiments discloses the following crossed topography of olivocerebellar projections: The caudal half of the medial accessory olive projects mainly to the vermis of the posterior lobe, whereas its rostral half projects to the flocculus, paraflocculus, and the intermediate cortex. The principal olive, ventral and dorsal lamellae, supplies climbing fiber inputs to the hemispheric cortex. The caudal half of the dorsal accessory olive projects to the lateral portion of the vermis of the anterior lobe, whereas neurons in its rostral half send their axons toward the intermediate cortex. This topographic arrangement is, therefore, similar to that reported for adult mammals. The present results, alone or when compared with those obtained during other studies on the synaptogenesis between climbing fibers and Purkinje cells, allow the following conclusions: (1) The climbing fibers enter the cerebellar cortex before Purkinje cells have reached the developmental phase compatible with synaptogenesis. They wait in the medullary white matter until appropriate maturation of their cellular targets. (2) Olivocerebellar topography is roughly similar in newborn, 5-day-old, and adult rats. (3) Synaptogenesis between climbing fibers and Purkinje cells, which is known not to start before the second postnatal day, is not necessary for the establishment of the topographic organization of the olivocerebellar projection. (4) Similarities between the topography of olivocerebellar projections in 5-day-old rats, the phase of highest level of poly-innervation of Purkinje cells by climbing fibers, and in adult animals also indicate that most of the acquisition of this topography depends on factors other than the regressive process of synapse elimination, which takes place during the second postnatal week.