Extrinsic cytological determinants of basket and stellate cell dendritic pattern in the cerebellar molecular layer.

Abstract

AbstractGolgi and ultrastructural features of mature and developing dendrites of cerebellar stellate and basket neurons were analyzed in relation to the genesis of parallel fibers in a timed series of rhesus monkeys. Three‐dimensional reconstruction of the mature molecular layer demonstrates differences in dendritic patterns and systematic decreases in the volume of dendritic distribution from deep to superficially situated interneurons.Developmental analysis revealed that the earliest‐forming interneurons (basket cells) assume a horizontal bipolar shape below the inner margin of the external granular layer. From their initial formation the bipolar processes lie in the sagittal plane (transverse to the folium) at a right angle to an earlier‐formed bed of underlying parallel fibers. As more parallel fibers are laid down external to their predecessors during further development, the dendrites of basket cells expand mainly upwards among them and thereby acquire a final dendritic distribution within the space of a sagittally‐flattened hemiellipsoid, its base facing the Purkinje layer and containing the basket cell soma. The interneurons destined to reside eventually in the middle of the molecular layer (stellate cells) similarly differentiate initially as sagittally‐oriented bipolar cells at the inner edge of the external granular layer, but do so at stages when the molecular layer below has become thickened by the further accretion of parallel fibers; their dendrites grow both downward to contact earlier‐formed parallel fibers and upward as new parallel fiber axons are being generated above. Hence their final dendritic distribution lies within a space shaped as a full ellipsoid flattened in the sagittal plane and with the stellate cell soma situated centrally. The more superficial stellate cells differentiate last from similar immature bipolar forms, but the direction of their dendritic growth is mainly downward, hence the space occupied by these dendrites takes the shape of an inverted, sagittally flattened hemiellipsoid, its base facing the pia and containing the stellate cell soma.A specific affinity of basket and stellate dendrites for parallel fibers was inferred from their exclusive growth within the axonal milieu of the molecular layer in the direction which allows the maximum number of interactions with individual parallel fibers, the contact points between them potentially developing as synaptic junctions. Such an hypothesis also explains the systematic variation of dendritic pattern and the relative flatness of their arborization in the plane transverse to the folium. The progressively decreased volumes of these dendritic spheres from deep to superficial cells presumably relates to the time‐ and space‐dependent progressively decreasing synaptogenic activity of the parallel fibers. The present analysis, therefore, supports the idea that a changing local milieu rather than genetic specialization may be responsible for development of morphological diversity among neurons of essentially identical origin.