Compensatory climbing fiber innervation after unilateral pedunculotomy in the newborn rat: origin and topographic organization.

In neonatal rats the unilateral transection of the cerebellar peduncles causes a fast and complete degeneration of the contralateral inferior olive. Axons from the remaining olive recross the cerebellar midline and partially innervate the deprived hemicortex. Analysis of the topographic organization of this compensatory projection studied with the axonal tracing method provided the following results: Retrograde tracing experiments revealed that the bulk of compensatory afferents originates from neurons in the ipsilateral medial accessory olive, especially from its medial region, whereas afferents from the principal olive and the dorsal accessory olive contribute to a much lesser degree. In case of incomplete neonatal pedunculotomy, neurons with a similar location in the ipsilateral intact olive still contribute to the innervation of the partially deprived hemicortex, along with the atrophic contralateral olive. Moreover, these experiments revealed important information about the organization of the compensation. Although its specificity was not totally maintained, the mediolateral distribution of sprouted afferents in the cerebellum matched the caudorostral disposition of parent neurons in the olive, as in the case in normal olivocerebellar projection. Anterograde studies showed that compensatory fibers recrossing the cerebellar midline spread throughout the whole extent of the deprived cortex and terminate solely in the molecular layer as typical climbing fibers. The latter were not homogeneously distributed, their density being markedly reduced according to a mediolateral gradient. Compensatory projection followed a sagittal striped pattern, as does the normal climbing fiber projection. Moreover, if the cortex is divided broadly into vermal, intermediate, and hemispheral regions, an apparent reciprocity seems to exist concerning the relative involvement of the various cortical subdivision in both hemicerebella. Our present results indicate that the immature olivocerebellar system is capable of anatomical plasticity, although to a limited extent. More important, they suggest that a certain degree of specificity is maintained during the process of sprouting, resulting in a topographical arrangement of the transcommissural climbing fiber projection. This indicates, in turn, that cues which guide the growth of olivocerebellar fibers during normal development could also direct the compensatory innervation.