Ultrastructural evidence for compensatory sprouting of climbing and mossy afferents to the cerebellar hemisphere after ipsilateral pedunculotomy in the newborn rat

Abstract

Unilateral section of the inferior and middle cerebellar peduncles was performed in rats at postnatal days 1 or 2. The ultrastructure of the cerebellar hemispheric cortex ipsilateral to the lesion was examined 3 months later. The absence of contralateral inferior olive and of ipsilateral middle peduncle, together with a marked regression of the contralateral pontine gray, were indicative of successful pedunculotomy. In spite of a relative atrophy of the hemisphere, its cytological structure was qualitatively normal. Mossy and climbing fibers were present and their terminal varicosities disclosed normal features. The density of climbing fiber terminals was reduced compared to control cerebellum, whereas the density of mossy terminals seemed unchanged. Subsequent to the reduction of climbing afferents two subclasses, or types, of Purkinje cells were present: A “normal” type characterized by its climbing fiber innervation and a “hyperspiny” type devoid of climbing fiber. In some of the adult rats pedunculotomized at birth, section of the contralateral peduncles was performed 24 hours before fixation. Terminal degeneration of climbing and mossy fibers was observed in the neonatally deprived hemisphere, providing the proof that these fibers result from a compensatory transcommissural sprouting of afferents destined to the contralateral hemicerebellum. These results demonstrate that the cerebellar cortex neonatally deprived of its main afferents can be innervated by climbing and mossy fibers through a process of transcommissural sprouting. Although the newly formed synapses maintain their target specificity, a functional reorganization must occur because of the altered distribution of both systems of afferents.