The recurrent collaterals of Purkinje cell axons: A correlated study of the rat's cerebellar cortex with electron microscopy and the Golgi method

Summary Each Purkinje cell axon with its recurrent collaterals occupies a roughly triangular space in the folium, apex pointed towards the white matter and base against the Purkinje cell layer. The axon is smooth initially but develops distensions that become more obvious at twists and turns and at points where collaterals originate. These thin, finely beaded collaterals make characteristic acute angles with the axon from which they issue. The collaterals bifurcate further, their terminal branches becoming more varicose, intertwining with each other to form plexuses in the molecular and granular layers. These fiber plexuses are found in three locations: (1) the recurrent collateral plexus in the granular layer which synapses with dendrites and somata of deep Golgi II neurons; (2) the profuse infraganglionic plexus, boutons of which terminate in relation with the somata and dendrites of Purkinje cells and Lugaro cells, in addition to participating in other complex synaptic arrangements in the neuropil; (3) the sparse supraganglionic plexus which forms synapses with dendrites of Purkinje cells and occasionally with basket cells.In electron micrographs, terminals belonging to recurrent collaterals contain a mixture of neurofilaments, microtubules, and slender mitochondria with a loose array of flat, elliptical, and round synaptic vesicles embedded in a dark filamentous matrix. It is usual to find a cluster of boutons on the postsynaptic surface. Each synapse consists of several separate macular junctional complexes. The synaptic cleft is widened and contains a dense fibrous material while both pre- and postsynaptic components have very shallow, symmetrical filamentous densities adherent to the cytoplasmic surfaces of the membranes.It is suggested that recurrent collaterals from axons of Purkinje cells may provide a rapid monosynaptic feed-back mechanism for inhibitory control of Purkinje cell responses. These collaterals may also participate in a slower positive feed-forward circuit or resetting mechanism involving at least two synapses. The existence of this circuit is indicated by synapses on deep Golgi II neurons. The inhibition of Golgi II cells may depress their inhibitory activity on surrounding granule cells, thus resetting the mechanism for the subsequent responses to excitatory afferent input. Recurrent collateral inhibition also may aid in the disinhibition of Purkinje cells through the depression of basket cell activity.Supported by U.S. Public Health Service Research Grant NS03659 and Training Grant NS05591 from the National Institute of Neurological Diseases and Stroke.