Summary
The differentiation of the cerebellar neurons and of their afferent fibres has been studied in young specimens ofSalmo gairdneri Richardson, 1836. Both light microscopic preparations, stained with haematoxylin-eosin or according to Bodian, Nissl, Klüver-Barrera or Golgi, and electron microscopic preparations were used. The ventricular matrix layer gives rise to the large neurons of the cerebellum,i.e. Purkinje, eurydendroid and Golgi cells; the secondary matrix produces the smaller neurons,i.e. the granule and stellate cells. The afferent fibres of the cerebellum are the mossy and the climbing fibres. The identification of the cell types, originating from either the ventricular matrix or from the secondary matrix, can be made earlier on the basis of the structure of their processes than on the basis of the structure of their somata. The development of the cerebellar neurons in the trout corresponds in many respects to that in higher vertebrates. In general, differentiation is characterized by a decrease in the number of free ribosomes and an increase of the other organelles, particularly of rough endoplasmic reticulum. The ganglionic layer contains, in addition to the Purkinje cells, the eurydendroid cells. The axons of these elements were in some cases observed to leave the cerebellum, whereas the axons of Purkinje cells are mainly confined to the ganglionic layer. In the trout the development of the granule cells shows a varied pattern. The mature shape of the axons of these elements depends on the migration paths followed by their precursors. T-shaped processes occur in all parts of the cerebellum and unbranched processes only in the valvula. The opinion held for mammals that the more superficial a parallel fibre is situated in the molecular layer the later it has been formed, is not valid for the trout. A number of secondary matrix cells performs tangential migration, not in the submeningeal region but deeper in the molecular layer,viz. under bundles of parallel fibres. The granule cells originating from these “deeper” matrix cells extend their axons at a lower level than the parallel fibres which have been formed previously. Throughout development “dark cells” are found in osmiumstained material. Their dark aspect is due to the presence of a fine filamentous network and of many free ribosomes in the cytoplasm. These immature cells are considered to be migratory.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altman, J.: Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer. J. Comp. Neur.145, 353–398 (1972a)
Altman, J.: Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J. Comp. Neur.145, 399–464 (1972b)
Altman, J.: Postnatal development of the cerebellar cortex in the rat. III. Maturation of the components of the granular layer. J. Comp. Neur.145, 465–514 (1972c)
Altman, J.: Experimental reorganization of the cerebellar cortex. IV. Parallel fiber reorientation following regeneration of the external germinal layer. J. Comp. Neur.149, 181–192 (1973)
Altman, J.: Postnatal development of the cerebellar cortex in the rat. IV. Spatial organization of bioplar cells, parallel fibers and glial palisades. J. Comp. Neur.163, 427–448 (1975)
Altman, J.: Experimental reorganization of the cerebellar cortex. V. Effects of early X-irradiation schedules that allow or prevent the acquisition of basket cells. J. Comp. Neur.165, 31–48 (1976)
Altman, J., Anderson, W.J.: Experimental reorganization of the cerebellar cortex. I. Morphological effects of elimination of all microneurons with prolonged X-irradiation started at birth. J. Comp. Neur.146, 355–406 (1972)
Anderson, W.J., Stromberg, M.W.: Effects of low-level X-irradiation on cat cerebella at different postnatal intervals. II. Changes in Purkinje cell morphology. J. Comp. Neur.171, 39–50 (1977)
Cajal, S. Ramon Y: Histologie du système nerveux de l'homme et des vertébrés. Tome II. Traduite par L. Azoulay. Madrid (1911)
Cammermeyer, J.: An evaluation of the significance of the “dark” neuron. Ergebn. Anat. Entw. Gesch.36, 1–61 (1962)
Cerro, M.P. del, Snider, R.S.: Studies on the developing cerebellum. II. The ultrastructure of the external granular layer. J. Comp. Neur.144, 131–164 (1972)
Chan-Palay, V., Palay, S.L., Billings-Gagliardi, S.M.: Meynert cells in the primate visual cortex. J Neurocytol.3, 631–658 (1974)
Ford, D.H., Rhodes, A.: DL-Lysine-3H uptake in “light” and “dark” neurons of the inferior olivary nucleus of euthyroid and dysthyroidal rats. Acta neuropathol.5, 316–319 (1965)
Franz, V.: Das Kleinhirn der Knochenfishe. Zool. Jb.32, 401–464 (1911)
Friede, R.L.: Interpretation of hyperchromic nerve cells. Relative significance of the type of fixative used, of the osmolarity of the cytoplasm and the surrounding fluid in the production of cell shrinkage. J. Comp. Neur.121, 137–150 (1963)
Gona, A.G.: Cerebellar changes in metamorphosing frog tadpoles. Anat. Rec.172, 317 (1972)
Gona, A.G.: Golgi studies of cerebellar maturation in frog tadpoles. Brain Res.95, 132–136 (1975)
Gona, A.G.: Autoradiographic studies of cerebellar histogenesis in the bullfrog tadpole during metamorphosis: the external granular layer. J. Comp. Neur.165, 77–88 (1976)
Hamori, J.: Developmental morphology of dentritic postsynaptic specializations.In: Recent developments of neurobiology in Hungary, vol. IV (ed. K. Lissák) pp. 9–32. Budapest: Akad. Kiado. 1973
Kornguth, S.E., Scott, G.: The role of climbing fibers in the formation of Purkinje cell dendrites. J. Comp. Neur.146, 61–82 (1972)
Kranz, D., Richter, W.: Autoradiographische Untersuchungen zur DNS synthese im Cerebelium und in der Medulla oblongata von Teleostiern verschiedenen Lebensalters. Z. mikrosk.-anat. Forsch., Leipzig82, 264–292 (1970)
Larramendi, L.M.H.: Analysis of synaptogenesis in the cerebellum of the mouse. In: Neurobiology of cerebellar evolution and development (ed. R. Llinás) pp. 803–843. Chicago: AMA. 1969
Ludueña, M.A., Wessells, N.K.: Cell locomotion, nerve elongation and microfilaments. Devel. Biol.30, 427–440 (1973)
Mareš, V., Lodin, Z., Šrajer, J.: The cellular kinetics of the developing mouse cerebellum. I. The generation cycle, growth fraction and rate of proliferation of the external granular layer. Brain Res.23, 323–342 (1970)
Mugnaini, E.: “Dark cells” in electron micrographs from the C.N.S. of vertebrates. J. Ultrastruct. Res,12, 235 (1965)
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 (ed. R. Llinás) pp. 749–782. Chicago: AMA. 1969
Nemetschek-Gansler, H., Becker, M.: Die Bedeutung der Perfusionsfixierung für die Morphologie des Zentralnervensystems. Acta anat.57, 152–162 (1964)
Nieuwenhuys, R., Pouwels, E., Smulders-Kersten, E.: The neuronal organization of cerebellar lobe C1 in the mormyrid fishGnathonemus petersii (Teleostei). Z. Anat. Entw. Gesch.144, 315–336 (1974)
O'Leary, J.L., Inukai, J., Smith, J.M.: Histogenesis of the cerebellar climbing fibre in rat. J. Comp. Neur.142, 377–392 (1971)
Palay, S.L., Chan-Palay, V.: Cerebellar cortex. Cytology and organization. Berlin-Heidelberg-New York: Springer. 1974
Pouwels, E.: On the development of the cerebellum of the trout,Salmo gairdneri. Thesis. Nijmegen. 1976
Pouwels, E.: On the development of the cerebellum of the trout,Salmo gairdneri. I. Patterns of cell migration. Anat. Embryol.152, 291–308 (1978)
Pouwels, E.: On the development of the cerebellum of the trout,Salmo gairdneri. II. Early development. Anat. Embryol.152, 309–324 (1978)
Pouwels, E.: On the development of the cerebellum of the trout,Salmo gairdnerti. IV. Development of the pattern of connectivity. Anat. Embryol.153, 55–65 (1978)
Pouwels, E.: On the development of the cerebellum of the trout,Salmo gairdneri. IV Development of and their development. Anat. Embryol.153, 67–83 (1978)
Rakic, P.: Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study inMacacus Rhesus. J. Comp. Neur.141, 283–312 (1971a)
Rakic, P.: Guidance of neurons migrating to the fetal monkey neocortex. Brain Res.33, 471–476 (1971b)
Rakic, P.: Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neur.145, 61–83 (1972)
Rakic, P.: Kinetics of proliferation and latency between final cell division and onset of differentiation of cerebellar stellate and basket neurons. J. Comp. Neur.147, 523–546 (1973)
Rakic, P., Sidman, R.L.: Organization of cerebellar cortex secondary to deficit of granule cells in Weaver mutant mice. J. Comp. Neur.152, 133–162 (1973)
Schaper, A.: Zur feineren Anatomie des Kleinhirns der Teleostier. Anat. Anz.8, 705–720 (1893)
Schaper, A.: Die morphologische und histologische Entwicklung des Kleinhirns der Teleostier, Morphol. Jb.21, 625–708 (1894)
Sotelo, C.: Formation and maintenance of Purkinje spines in the cerebellum of “mutants” and experimental animals. 7th Int. Neurobiol. Meeting, Göttingen (1975)
Sotelo, C., Arsenio-Nunes, M.L.: Development of Purkinje cells in absence of climbing fibers. Brain Res.111, 389–395 (1976)
Spooner, B.S., Yamada, K.M., Wessells, N.K.: Microfilaments and cell locomotion. J. Cell Biol.49, 595–613 (1971)
Stensaas, S.S., Edwards, C.Q., Stensaas, L.J.: An experimental study of hyperchromic nerve cells in the cerebral cortex. Exp. Neurol.36, 472–487 (1972)
Swarz, J.R., del Cerro, M.: An electron microscopic and Golgi study of the external granular layer in fetal mouse cerebellum. Neuroscience Abstr. II (1976)
Tewari, H.B., Bourne, G.H.: Histochemical studies on the “Dark” and “Light” cells of the cerebellum of rat. Acta Neuropathol.3, 1–15 (1963)
Wessells, N.K., Spooner, B.S., Ash, J.F., Bradley, M.O., Ludueña, M.A., Taylor, E.L., Wrenn, J.T., Yamada, K.M.: Microfilaments in cellular and developmental processes. Science171, 135–143 (1971)
Yamada, K.M., Spooner, B.S., Wessells, N.K.: Ultrastructure and function of growth cones and axons of cultured nerve cells. J. Cell Biol.49, 614–635 (1971)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Pouwels, E. On the development of the cerebellum of the trout,Salmo gairdneri . Anat Embryol 153, 37–54 (1978). https://doi.org/10.1007/BF00569848
Issue Date:
DOI: https://doi.org/10.1007/BF00569848