Summary
An analytical study was undertaken with both electron microscopy and the rapid Golgi method in order to clarify the interrelations of climbing fibers, basket cell axons, and Purkinje cell dendrites. The two fibers are readily distinguished in electron micrographs by means of their differing content of microtubules and neurofilaments, the packing density of synaptic vesicles, and the disposition of their synaptic junctions on the Purkinje cell dendrite. Climbing fibers are generally thin and contain many microtubules. They give off attenuated collaterals, whose rounded varicosities are densely packed with vesicles and which form en passant synapses with clusters of thorns projecting from the major Purkinje dendrites. In contrast, basket axons are relatively thick and contain many neurofilaments. By means of slight dilatations containing loosely aggregated vesicles, the axon and its collaterals form numerous synapses en passant with the smooth dendritic shafts and the perikaryon of the Purkinje cell. Climbing fibers and basket cell axons run along parallel with each other but without forming axo-axonic synapses as they ascend over the surface of the Purkinje dendrites. Both fibers form especially elaborate intertwined festoons at the branching points of the major dendrites. The kinds of synapses found are described in detail, and the functional implications are discussed.
The hypothesis is developed that the dendritic thorn is a device for isolating the subsynaptic membrane from electrical events in the rest of the dendrite at the cost of reducing the effectiveness of the synapse. This principle is incorporated in the Purkinje dendrite—parallel fiber synapses, in which an individual fiber can be expected to have little importance. The disadvantage of using thorns as postsynaptic surfaces can be mitigated by clustering them and increasing the number of thorns contacted by each presynaptic terminal. This method is utilized at the junctions between the climbing fiber and the Purkinje dendrite to produce one of the most powerful excitatory synapses known. It is furthermore suggested that the elaborate plexus of climbing fibers and basket cell axons synapsing in the crotches of branching dendrites is strategically located to control the flow of information in the Purkinje cell dendritic tree.
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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.
Colonnier, M.: Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res. 9, 268–287 (1968).
Diamond, J., Gray, E. G., Yasargil, G. M.: The function of dendritic spines: an hypothesis. J. Physiol. (Lond.) 202, 116P (1969).
Eccles, J. C., Ito, M., Szentágothai, J.: The cerebellum as a neuronal machine. Berlin-Heidelberg-New York: Springer 1967.
— Llinás, R., Sasaki, K.: The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J. Physiol. (Lond.) 182, 268–296 (1966a).
——— Voorhoeve, P. E.: Interaction experiments on the responses evoked in Purkinje cells by climbing fibers. J. Physiol. (Lond.) 182, 297–315 (1966b).
Eide, E., Fedina, L., Jansen, J., Lundberg, A., Vyklický, L.: Unitary excitatory post-synaptic potentials in Clarke's column neurones. Nature (Lond.) 215, 1176–1177 (1967).
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.
Fox, C. A. Hillman, D. E., Siegesmund, K. A., Dutta, C. R.: The primate cerebellar cortex: A Golgi and electron microscopic study. In: The cerebellum (C. A. Fox and R. S. Snider, eds.). Progr. Brain Res. 25, 174–225 (1967).
Gobel, S.: Electron microscopical studies of the cerebellar molecular layer. J. Ultrastruct. Res. 21, 430–458 (1967).
Granit, R., Phillips, C. G.: Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum of cats. J. Physiol. (Lond.) 133, 520–547 (1956).
Gray, E. G.: Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study. J. Anat. (Lond.) 93, 420–433 (1959).
— The granule cells, mossy synapses and Purkinje spine synapses of the cerebellum: light and electron microscope observations. J. Anat. (Lond.) 95, 345–356 (1961).
Gray, E. G. Electron microscopy of excitatory and inhibitory synapses: a brief review. In: Mechanisms of synaptic transmission (K. Akert and P. G. Waser, eds.). Progr. Brain Res. 31, 141–155 (1969).
Hámori, J., Szentágothai, J.: Identification under the electron microscope of climbing fibers and their synaptic contacts. Exp. Brain Res. 1, 65–81 (1966).
Hillman, D. E.: Neuronal organization of the cerebellar cortex in amphibia and reptilia. In: Neurobiology of cerebellar evolution and development (R. Llinás, ed.), p. 279–324. Chicago: AMA-ERF Institute for Biomedical Research 1969.
Jones, E. G., Powell, T. P. S.: Morphological variations in the dendritic spines of the neocortex. J. Cell Sci. 5, 509–529 (1969).
Kaiserman-Abramof, I. R., Palay, S. L.: Fine structural studies of the cerebellar cortex in a mormyrid fish. In: Neurobiology of cerebellar evolution and development (R. Llinás, ed.), p. 171–204. Chicago: AMA-ERF Institute for Biomedical Research 1969.
Kirsche, W., David, H., Winkelmann, E., Marx, I.: Elektronenmikroskopische Untersuchungen an synaptischen Formationen im Cortex cerebelli von Rattus rattus norvegicus, Berkenhoot. Z. mikr.-anat. Forsch. 72, 49–80 (1964).
Koller, T., Harford, A. G., Lee, Y. K., Beer, M.: New methods for the preparation of nucleic acid molecules for electron microscopy. Micron 1, 110–118 (1969).
Kornguth, S. E., Anderson, J. W., Scott, G.: The development of synaptic contacts in the cerebellum of Macaca mulatta. J. comp. Neurol. 132, 531–545 (1968).
Kuno, M., Miyahara, J. T.: Factors responsible for multiple discharge of neurons in Clarke's column. J. Neurophysiol. 31, 624–638 (1968).
—— Analysis of synaptic efficacy in spinal motoneurones from “quantum” aspects. J. Physiol. (Lond.) 201, 479–493 (1969).
Larramendi, L. M. H., Victor, T.: Synapses on the Purkinje cell spines in the mouse. An electronmicroscopic study. Brain Res. 5, 15–30 (1967).
Larsell, O.: The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat. J. comp. Neurol. 97, 281–356 (1952).
Llinás, R., Hillman, D. E.: Physiological and morphological organization of the cerebellar circuits in various vertebrates. In: Neurobiology of cerebellar evolution and development (R. Llinás, ed.), p. 43–73. Chicago: AMA-ERF Institute for Biomedical Research 1969.
— Nicholson, C.: Electrophysiological analysis of alligator cerebellar cortex: a study on dendritic spikes. In: Neurobiology of cerebellar evolution and development (R. Llinás, ed.), p. 431–464. Chicago: AMA-ERF Institute for Biomedical Research 1969.
—— Freeman, J. A., Hillman, D. E.: Dendritic spikes and their inhibition in alligator Purkinje cells. Science 160, 1132–1135 (1968).
—— Precht, W.: Preferred centripetal conduction of dendritic spikes in alligator Purkinje cells. Science 163, 184–187 (1969).
Morest, D. K.: The collateral system of the medial nucleus of the trapezoid body of the cat, its neuronal architecture and relation to the olivo-cochlear bundle. Brain Res. 9, 288–311 (1968).
— Morest, R. R.: Perfusion-fixation of the brain with chrome-osmium solutions for the rapid Golgi method. Amer. J. Anat. 118, 811–831 (1966).
Mugnaini, E.: Ultrastructural studies on the cerebellar histogenesis. II. Maturation of nerve cell populations and establishment of synaptic connections in the cerebellar cortex of the chick. In: Neurobiology of cerebellar evolution and development (R. Llinás, ed.), p. 749–782. Chicago: AMA-ERF Institute for Biomedical Research 1969.
— Neurones as synaptic targets. In: Excitatory synaptic mechanisms (P. Andersen and J. K. S. Jansen, Jr., eds.), p. 149–169. Oslo: Universitets Forlaget 1970.
Palay, S. L.: The structural basis for neural action. In: Brain function, II: RNA and brain function; memory and learning (M. A. B. Brazier, ed.), p. 69–108. Berkeley: University of California Press 1964.
— 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.
— McGee-Russell, S. M., Gordon, S., Grillo, M. A.: Fixation of neural tissues for electron microscopy by perfusion with solutions of osmium tetroxide. J. Cell Biol. 12, 385–410 (1962).
Peters, A., Kaiserman-Abramof, I. R.: The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Amer. J. Anat. 127, 321–355 (1970).
Richardson, K. C., Jarett, L., Finke, E. H.: Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960).
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).
—— On the nature of dendritic spines. Commun. Behav. Biol., Part A 1, 231–265 (1968).
Sotelo, C.: Ultrastructural aspects of the cerebellar cortex of the frog. In: Neurobiology of cerebellar evolution and development (R. Llinás, ed.), p. 327–367. Chicago: AMA-ERF Institute for Biomedical Research 1969.
Uchizono, K.: Synaptic organization of the mammalian cerebellum. In: Neurobiology of cerebellar evolution and development (R. Llinás, ed.), p. 549–581. Chicago: AMA-ERF Institute for Biomedical Research 1969.
Westrum, L. E.: Observations on initial segments of axons in the prepyriform cortex of the rat. J. comp. Neurol. 139, 337–355 (1970).
Wuerker, R. B., Palay, S. L.: Neurofilaments and microtubules in anterior horn cells of the rat. Tissue and Cell 1, 387–402 (1969).
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Supported by U.S. Public Health Service Research Grant NS03659 and Training Grant NS05591 from the National Institute of Neurological Diseases and Stroke.
Postdoctoral trainee in Anatomy under Training Grant GM906 from the National Institute of General Medical Sciences.
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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). https://doi.org/10.1007/BF00523377
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DOI: https://doi.org/10.1007/BF00523377