Tendril and glomerular collaterals of climbing fibers in the granular layer of the rat's cerebellar cortex (original) (raw)
Summary
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 Å 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.
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References
- Cajal, S. R.: Histologie du Système Nerveux de l'Homme et des Vertébrés, vols. I and II. Paris: Maloine 1909–1911. Reprinted Madrid: Consejo Superior de Investigaciones Cientificas 1952.
Google Scholar - Chan-Palay, V., Palay, S. L.: Interrelations of basket cell axons and climbing fibers in the cerebellar cortex of the rat. Z. Anat. Entwickl.-Gesch. 132, 191–227 (1970).
Google Scholar - ——: The synapse en marron between Golgi II neurons and mossy fibers in the rat's cerebellar cortex. Z. Anat. Entwickl.-Gesch. 133, 274–287 (1971).
Google Scholar - Eccles, J. C., Ito, M., Szentágothai, J.: The cerebellum as a neuronal machine. New York: Springer 1967.
Google Scholar - —, Llinás, R., Sasaki, K.: The inhibitory interneurones within the cerebellar cortex. Exp. Brain Res. 1, 1–16 (1966a).
Google Scholar - ———: The mossy fibre-granule cell relay of the cerebellum and its inhibitory control by Golgi cells. Exp. Brain Res. 1, 82–101 (1966b).
Google Scholar - ———: The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J. Physiol. (Lond.) 182, 268–296 (1966c).
Google Scholar - Fox, C. A., Andrade, A., Schwyn, R. C.: Climbing fiber branching in the granular layer. In: Neurobiology of cerebellar evolution and development (R. Llinás, ed.), p. 603–611. Chicago: AMA-ERF Institute for Biomedical Research 1969.
Google Scholar - Gray, E. G.: Axo-somatic and axo-dendrite synapses of the cerebral cortex: An electron microscope study. J. Anat. (Lond.) 93, 420–433 (1959).
Google Scholar - —: The granule cells, mossy synapses and Purkinje spine synapses of the cerebellum: light and electron microscope observations. J. Anat. (Lond.) 95, 345–356 (1961).
Google Scholar - Hámori, J., Szentágothai, J.: Identification under the electron microscope of climbing fibers and their synaptic contacts. Exp. Brain Res. 1, 65–81 (1966a).
Google Scholar - ——: Participation of Golgi neuron processes in the cerebellar glomeruli: An electron microscopic study. Exp. Brain Res. 2, 35–48 (1966b).
Google Scholar - Larramendi, L. M. H., Lemkey-Johnston, N. J.: The distribution of recurrent Purkinje collateral synapses in the mouse cerebellar cortex: An electron microscopic study. J. comp. Neurol. 138, 451–482 (1970).
Google Scholar - Larsell, O.: The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat. J. comp. Neurol. 97, 281–358 (1952).
Google Scholar - Mugnaini, E.: Neurones as synaptic targets. In: Excitatory synaptic mechanisms (P. Andersen and J. K. S. Jansen, Jr., eds.). Oslo: Universitets Forlaget 1970.
Google Scholar - Palay, S. L.: Principles of cellular organization in the nervous system. In: The neurosciences (G. C. Quarton, T. Melnechuk, and F. O. Schmitt, eds.), p. 24–31. New York: Rockefeller University Press 1967.
Google Scholar - Richardson, K. C., Jarett, L., Finke, E. H.: Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960).
Google Scholar - Scheibel, M. E., Scheibel, A. B.: Observations on the intracortical relations of the climbing fibers of the cerebellum. J. comp. Neurol. 101, 733–763 (1954).
Google Scholar - Szentágothai, J.: The use of degeneration methods in the investigation of short neuronal connexions. In: Progress in brain research, vol. 14: Degeneration patterns in the nervous system (M. Singer and J. P. Schadé, eds.), p. 1–32. Amsterdam: Elsevier 1965.
Google Scholar - —, Rajkovits, U.: Über den Ursprung der Kletterfasern des Kleinhirns. Z. Anat. Entwickl.-Gesch. 121, 130–141 (1959).
Google Scholar
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Authors and Affiliations
- Department of Neurobiology, Harvard Medical School, Boston, Massachusetts
Victoria Chan-Palay & Sanford L. Palay - Department of Anatomy, Harvard Medical School, Boston, Massachusetts
Victoria Chan-Palay & Sanford L. Palay
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- Victoria Chan-Palay
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Supported by U. S. Public Health Service Research Grant NS 03659 and Training Grant NS 05591 from the National Institute of Neurological Diseases and Stroke.
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Chan-Palay, V., Palay, S.L. Tendril and glomerular collaterals of climbing fibers in the granular layer of the rat's cerebellar cortex.Z. Anat. Entwickl. Gesch. 133, 247–273 (1971). https://doi.org/10.1007/BF00519302
- Received: 21 January 1971
- Issue Date: January 1971
- DOI: https://doi.org/10.1007/BF00519302