Dual phases of migration of cerebellar granule cells guided by axonal and dendritic leading processes

During lamination of the cerebellar cortex, granule cells initially migrate tangentially along the external granule layer, and then make a vertical turn and migrate radially to the internal granule layer. We comparatively analyzed the properties of biphasic migration of granule cells in a microexplant culture in which quantitation of morphology and subcellular localization of molecules were readily accomplished. Tangential migration was guided by a leading process that later formed a parallel fiber axon. Translocation of the soma within the axonal process occurred independently of the rapid displacement of the large growth cone. On the other hand, radial migration was guided by a leading process that differentiated into a dendrite after completion of migration. Displacement of the soma and the tiny growth cone were linked so that the radial leading process adopted locomotion and kept a constant length. We propose that the dual phases of granule cell migration are achieved by distinct cellular mechanisms guided by the leading processes forming an axon and a dendrite, respectively.