Tendril and glomerular collaterals of climbing fibers in the granular layer of the rat's cerebellar cortex.

Abstract

Rapid Golgi preparations show that two kinds of collaterals issue from the climbing fiber in its course through the granular layer. The first resembles the tendrils found in the molecular layer and consists of globose varcosities connected by a very fine thread. In electron micrographs these varicosities in the granular layer contain dense aggregates of round synaptic vesicles at least 520 A in diameter and the connecting threads contain numerous microtubules. The varicosities synapse on the somata of Golgi II cells and on the shafts of dendrites belonging to both Golgi II and granule cells. The second type of collateral emerges from the main stem of the climbing fiber as a stout branch that sprays out abruptly into a large efflorescence. In electron micrographs this terminal appears as the central stellate structure in a glomerulus and is packed with round synaptic vesicles like those in the tendril varicosities. Granule cell dendrites encircle the terminal and occasionally synapse with it. Often the terminal in the glomerulus also forms an extensive junction—a synapse en marron—with the some of Golgi II cell. In this region the surface of the cell is wrinkled like a Spanish chestnut and the glomerular terminal is reciprocally ridged and furrowed to match. Synaptic complexes occur only in the furrows of the cell surface. A broad subsynaptic zone is filled with a fine filamentous matrix. This study provides the first morphological identification and description of climbing fiber terminations in the granular layer, the existence of which has been suggested by earlier Golgi studies and postulated by neurophysiologists. The fact that climbing fibers synapse on both granule cells and Golgi II cells complicates the analysis of the way in which the cerebellar cortex operates, because these two cells have postsynaptic effects of opposite sign. The climbing fiber is known to evoke a complex discharge from the Purkinje cell, consisting of a large primary spike and smaller secondary potentials. It is suggested that when a climbing fiber volley traverses the granular layer, the granule cells on which it synapses are induced to excite stellate and basket cells in the molecular layer which in their turn inhibit the secondary spikes of the climbing fiber response in the Purkinje cell. Meanwhile the Golgi II cells, stimulated by the same climbing fiber volley, suppress the granule cells and thus transsynaptically limit the duration of the inhibitory effects exerted by the interneurons in the molecular layer.