The Entire Trajectories of Single Olivocerebellar Axons in the Cerebellar Cortex and their Contribution to Cerebellar Compartmentalization

Abstract

The functional partitioning of the cerebellar cortex depends on the projection patterns of its afferent and efferent neurons. However, the entire morphology of individual projection neurons has been demonstrated in only a few classes of neurons in the vertebrate CNS. To investigate the contribution of the projection pattern of individual olivocerebellar axons to the cerebellar functional compartmentalization, we labeled individual olivocerebellar axons, which terminate in the cerebellar cortex as climbing fibers, with biotinylated dextran amine injected into the inferior olive in the rat, and completely reconstructed the entire trajectories of 34 olivocerebellar axons from serial sections of the cerebellum and medulla. Single axons had seven climbing fibers on average, which terminated at similar distances from the midline in a single or in multiple lobules. Cortical projection areas of adjacent olivary neurons were clustered as narrow but separate longitudinal segments and often innervated by collaterals of single neurons. Comparison of the cerebellar distribution of olivocerebellar axons arising from different sites within a single olivary subnucleus indicated that slightly distant neurons projected to complementary sets of such segments in a single longitudinal band. Several of these longitudinal bands formed a so-called parasagittal zone innervated by a subnucleus of the inferior olive. Single olivocerebellar axons projected rostrocaudally to segments within a single band but did not project mediolaterally to multiple bands. These results suggest fine substructural organization in the cerebellar compartmentalization that may represent functional units.

Molecular, Topographic, and Functional Organization of the Cerebellar Cortex: A Study with Combined Aldolase C and Olivocerebellar Labeling

“…3D-G), as reported previously (Sugihara et al, 2001). Figure 3 shows typical examples of individual longitudinal bands extending in both the rostral and caudal cerebellar cortex.…”

“…The longitudinal organization has been further elaborated by the demonstration of zones A-D (Voogd, 1967;Groenewegen and Voogd, 1977; and even much narrower "microzones" (Andersson and Oscarsson, 1978), which are based on topographic corticonuclear Purkinje cell projection and olivocortical climbing fiber projection. Recent analyses have shown that the axon of an inferior olivary neuron provides multiple climbing fibers to a single narrow longitudinal band-shaped area comparable in size to a cortical microzone and sends collaterals to a small area in the cerebellar nucleus (Sugihara et al, , 2001. In contrast, a single lateral reticular nucleus neuron branches to form multiple mossy fibers that project to several longitudinal band-shaped areas .…”

“…Ipsilateral projections, encountered infrequently, were ignored. A previous standardized unfolded representation of the Purkinje cell layer of the whole cerebellar cortex (Sugihara et al, 2001) was modified by incorporating the aldolase C labeling pattern. The mediolateral distance for a given compartment was measured at the apex of each folium from the midline along the cerebellar surface.…”

“…The procedure for mapping injection sites in the horizontal representation of the inferior olive from brains cut coronally has been described previously (Sugihara et al, 2001). In brains cut horizontally, the contour of the inferior olive, the cut end of the medulla, the midline, and the injection spots were drawn using a camera lucida apparatus from each of the serial sections.…”

Isolation of glutamate transport-coupled charge flux and estimation of glutamate uptake at the climbing fiber–Purkinje cell synapse

“…In mature rats, each CF provides an exceptionally strong synaptic input onto a few PCs in the cerebellum (34,35). Glutamate released at this synapse rapidly elicits a large non-N-methyl-Daspartic acid (NMDA) receptor-mediated EPSC that is strongly inhibited by ionotropic GluR antagonists.…”