Neuron‐glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electonmicroscopic study in Macacus rhesus

Abstract

The cytology of the postmitotic migratory granule cell and its relationship to Bergmann glial processes was examined with Golgi staining and electron microscopy in the three cardinal planes in the developing cerebellar cortex of Macacus rhesus at various late fetal and early postnatal ages. After final mitosis the granule cell body transforms from a nearly round shape in the superficial zone of the external granular layer to a horizontal bipolar form with elongated processes oriented longitudinally to the folium, at the outer border of the molecular layer. Another descending process develops, and the cell soma becomes a pyramid flattened in the plane longitudinal to the folium. The nucleus moves into the descending process and the cell soma assumes a vertically oriented spindle shape while migrating among previously formed parallel fibers deeper in the molecular layer, and finally attains a round shape again when it lies deep to the Purkinje cell layer. During these transformations, the cell cytoplasm becomes more voluminous and contains a prominent Golgi apparatus, numerous free ribosomes, mitochondria, multivesicular and dense bodies, and fascicles of microtubules Longitudinally oriented microtubules concentrated in the vertical leading process disappear by the time the cell soma enters the granular layer. The slender trailing process loss most of its cytoplasmic organelles, acquires microtubules and together with the horizontal processes forms the characteristic T‐shaped axon. The axon forms synapses with Purkinje and stellate cell dendrites at a time when other granule cells are still migrating among them. During the entire course of their migration across the molecular layer, granule cells are directly apposed to vertically oriented Bergmann fibers belonging to the Golgi epithelial cells. The sequence of developmental stages indicates that Golgi epithelial cells are a type of protoplasmic astrocyte. The Bergmann fibers were present at all stages examined, and their constant apposition to granule cells suggests a role in the lartter's migration. Numerous electronluscent beady enlargements are seen along the fiber except at sites were the surface is in contact with migrating cells; probably these enlargements change position as the granule cells pass along the Bergmann fiber. Lamellate expansions also project from the main shaft of the glial fiber and envelop the synaptic sites on spines of Purkinje cell dendrites. These expansions seem more durable, and the young neuron appears to avoid collision with them by sprialling around the glial shaft during its descent to the granular layer. The neuron‐glia relationship apparently provides the necessary conditions for the migration of the young granule cell. Especially at late developmental stages when the molecular layer is more than 250 μ wide and is densely packed with highly oriented cell processes that have already established synaptic connections.