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Membrane structure of parallel-fibre synaptic terminals in the cerebellum of the jaundiced Gunn rat: freeze-fracture and E-PTA study

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Journal of Neurocytology

Summary

Parallel-fibre synaptic membranes were examined by freeze-fracture and ethanolic-phosphotungstic acid methods in the cerebellum of homozygous (j/j) Gunn rats with hereditary jaundice. Parallel-fibre synapses with dendritic spines of Purkinje cell were severely affected since many Purkinje cells degenerated during the early postnatal period. Some parallel-fibre synaptic terminals lacked their postsynaptic partners and faced astrocytic processes from 18 days of age to the adult stage. These parallel-fibre terminals contained clusters of synaptic vesicles adjacent to synaptic membranes, and synaptic membranes and synaptic cleft materials were identical to those of parallel fibres with postsynaptic partners, as visualized by conventional electron microscopy with osmium tetroxide postfixation and staining of sections with uranyl acetate and lead citrate. In freeze-fractured specimens, the presynaptic membrane of parallel fibres had diffusely distributed large particles and tiny pits on the P-face and protuberances on the E-face, together representing synaptic vesicle attachment sites. Such vesicle attachment sites were present on the presynaptic membranes of parallel fibres without postsynaptic partners from day 18 to the adult stage. After ethanolic-phosphotungstic acid staining, parallel-fibre terminals displayed presynaptic dense projections, intercleft materials and postsynaptic thickening, but some parallel fibres lacked postsynaptic thickening. These observations suggest that the presynaptic membrane structure of the parallel fibre is preserved, even in the absence of a postsynaptic partner, in j/j cerebella. A mechanism for persistence of presynaptic membrane structures without postsynaptic partners in j/j cerebella is discussed.

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References

  • Aghajanian, G. K. &Bloom, F. E. (1967) The formation of synaptic junctions in developing rat brain: a quantitative electron microscopic study.Brain Research 6, 716–27.

    Google Scholar 

  • Akert, K. (1973) Dynamic aspects of synaptic ultrastructure.Brain Research 49, 511–18.

    Google Scholar 

  • Altman, J. (1972) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer.Journal of Comparative Neurology 145, 399–464.

    Google Scholar 

  • Altman, J. &Anderson, W. J. (1972) Experimental reorganization of the cerebellar cortex. I. Morphological effects of elimination of all microneurons with prolonged x-irradiation started at birth.Journal of Comparative Neurology 146, 355–406.

    Google Scholar 

  • Bloom, F. E. (1972) The formation of synaptic junctions in developing rat brain. InStructure and Function of Synapse (edited byPappas, G. D. &Purpura, D. P.), pp. 101–20, New York, Raven Press.

    Google Scholar 

  • Bloom, F. E. &Aghajanian, G. K. (1968) Fine structural and cytochemical analysis of the staining of synaptic junctions with phosphotungstic acid.Journal of Ultrastructure Research 22, 361–75.

    Google Scholar 

  • Burry, R. W., Kniss, D. A. &Scribner, L. R. (1984) Mechanisms of synaptic formation and maturation. InCurrent Topics in Research on Synapses, Volume 1 (edited byJones, D. G.), pp. 1–51, New York: Alan R. Liss, Inc.

    Google Scholar 

  • Colonnier, M., Tremblay, J. P. &McLennan, H. (1979) Synaptic contacts on glial cells in the abdominal ganglion ofAplysia californica.Journal of Comparative Neurology 188, 391–400.

    Google Scholar 

  • Foelix, R. F. &Oppenheim, R. (1974) The development of synapses in the cerebellar cortex of the chick embryo.Journal of Neurocytology 3, 277–94.

    Google Scholar 

  • Güldner, F.-H. &Wolff, J. R. (1973) Neurono-glial synaptoid contacts in the median eminence of the rat: ultrastructure, staining properties and distribution on tanycytes.Brain Research 61, 217–34.

    Google Scholar 

  • Gulley, R. L. (1978) Changes in the presynaptic membrane of the synapses of the anteroventral cochlear nucleus with different levels of acoustic stimulation.Brain Research 146, 373–9.

    Google Scholar 

  • Gunn, C. K. (1938) Hereditary acholuric jaundice in a new mutant strain of rats.Journal of Heredity 29, 137–9.

    Google Scholar 

  • Hanna, R. B., Hirano, A. &Pappas, G. D. (1976) Membrane specializations of dendritic spines and glia in the weaver mouse cerebellum: a freeze-fracture study.Journal of Cell Biology 68, 403–10.

    Google Scholar 

  • Hartkop, T. H. &Jones, M. Z. (1977) Methylazoxy-methanol-induced aberrant Purkinje cell dendritic development.Journal of Neuropathology and Experimental Neurology 36, 519–32.

    Google Scholar 

  • Herndon, R. M., Margolis, G. &Kilham, L. (1971) The synaptic organization of the malformed cerebellum induced by perinatal infection with the feline panleukopenia virus (PLV). II. The Purkinje cell and its afferents.Journal of Neuropathology and Experimental Neurology 30, 557–70.

    Google Scholar 

  • Hirano, A., Dembitzer, H. M. &Jones, M. (1972) An electron microscopic study of cycasin-induced cerebellar alterations.Journal of Neuropathology and Experimental Neurology 31, 113–25.

    Google Scholar 

  • Hirano, A. &Dembitzer, H. M. (1973) Cerebellar alterations in the weaver mouse.Journal of Cell Biology 56, 478–86.

    Google Scholar 

  • Jones, D. G. (1978)Some current concepts of synaptic organization. Advances in Anatomy, Embryology and Cell Biology 55. Fasc. 4, Berlin: Springer-Verlag.

    Google Scholar 

  • Landis, D. M. D. &Reese, T. S. (1974) Differences in membrane structure between excitatory and inhibitory synapses in the cerebellar cortex.Journal of Comparative Neurology 155, 93–126.

    Google Scholar 

  • Landis, D. M. D. &Reese, T. S. (1977) Structure of the Purkinje cell membrane in staggerer and weaver mutant mice.Journal of Comparative Neurology 171, 247–60.

    Google Scholar 

  • Landis, D. M. D. &Sidman, R. L. (1978) Electron microscopic analysis of postnatal histogenesis in the cerebellar cortex of staggerer mutant mice.Journal of Comparative Neurology 179, 831–64.

    Google Scholar 

  • Lovell, K. L. &Jones, M. Z. (1980) Partial external germinal layer regeneration in the cerebellum following methylazoxymethanol administration: effects on Purkinje cell dendritic spines.Journal of Neuropathology and Experimental Neurology 39, 541–8.

    Google Scholar 

  • Mariani, J., Crepel, F., Mikoshiba, K., Changeux, J.-P. &Sotelo, C. (1977) Anatomical, physiological and biochemical studies of the cerebellum fromreeler mutant mouse.Philosophical Transactions of the Royal Society of London (B) 281, 1–28.

    Google Scholar 

  • Pfenninger, K. H. &Rovainen, C. M. (1974) Stimulation- and calcium-dependence of vesicle attachment sites in the presynaptic membrane; a freeze-cleave study on the lamprey spinal cord.Brain Research 72, 1–23.

    Google Scholar 

  • Rakic, P. (1976) Synaptic specificity in the cerebellar cortex: study of anomalous circuits induced by single gene mutations in mice.Cold Spring Harbor Symposia on Quantitative Biology 40, 333–46.

    Google Scholar 

  • Rakic, P. &Sidman, R. L. (1973) Organization of cerebellar cortex secondary to deficit of granule cells in weaver mutant mice.Journal of Comparative Neurology 152, 133–62.

    Google Scholar 

  • Saint Marie, R. L. &Carlson, S. D. (1982) Synaptic vesicle activity in stimulated and unstimulated photoreceptor axons in the housefly: a freeze-fracture study.Journal of Neurocytology 11, 747–61.

    Google Scholar 

  • Sawasaki, Y., Yamada, N. &Nakajima, H. (1976) Developmental features of cerebellar hypoplasia and brain bilirubin levels in a mutant (Gunn) rat with hereditary hyperbilirubinaemia.Journal of Neurochemistry 27, 577–83.

    Google Scholar 

  • Schutta, H. S. &Johnson, L. J. (1967) Bilirubin encephalopathy in the Gunn rat: a fine structure study of the cerebellar cortex.Journal of Neuropathology and Experimental Neurology 26, 377–96.

    Google Scholar 

  • Siggins, G. R., Henriksen, S. J. &Landis, S. C. (1976) Electrophysiology of Purkinje neurons in the weaver mouse: iontophoresis of neurotransmitters and cyclic nucleotides, and stimulation of the nucleus locus coeruleus.Brain Research 114, 53–69.

    Google Scholar 

  • Sotelo, C. (1975) Anatomical, physiological and biochemical studies of the cerebellum from mutant mice. II. Morphological study of cerebellar cortical neurons and circuits in the weaver mouse.Brain Research 94, 19–44.

    Google Scholar 

  • Sotelo, C. (1980) Mutant mice and the formation of cerebellar circuitry.Trends in Neuroscience 3, 33–6.

    Google Scholar 

  • Sotelo, C. &Changeux, J.-P. (1974) Transsynaptic degeneration ‘en cascade’ in the cerebellar cortex of staggerer mutant mice.Brain Research 67, 519–26.

    Google Scholar 

  • Sotelo, C. &Triller, A. (1979) Fate of presynaptic afferents to Purkinje cells in the adult nervous mutant mouse: a model to study presynaptic stabilization.Brain Research 175, 11–36.

    Google Scholar 

  • Takagishi, Y. (1989) Development of cerebellar hypoplasia in jaundiced Gunn rats: a morphological study.Congenital Anomalies 29, 275–94.

    Google Scholar 

  • Takagishi, Y. &Yamamura, H. (1989a) Purkinje cell abnormalities and synaptogenesis in genetically jaundiced rats (Gunn rats).Brain Research 492, 116–28.

    Google Scholar 

  • Takagishi, Y. &Yamamura, H. (1989b) Severity of cerebellar hypolasia is predictable from total plasma bilirubin level at 3 to 7 days of age in jaundiced Gunn rats.Laboratory Animal Science 39, 158–60.

    Google Scholar 

  • Vrensen, G., Cardozo, J. N., Müller, L. &Want, J. V. (1980) The presynaptic grid: a new approach.Brain Research 184, 23–40.

    Google Scholar 

  • Woodward, D. J., Hoffer, B. J., Siggins, G. R. &Bloom, F. E. (1971) The ontogenetic development of synaptic junctions, synaptic activation and responsiveness to neurotransmitter substances in rat cerebellar Purkinje cells.Brain Research 34, 73–97.

    Google Scholar 

  • Yamano, T., Shimada, M., Nakao, K., Nakamura, T., Wakaiuzumi, S. &Kusunoki, T. (1978) Maturation of Purkinje cells in mouse cerebellum after neonatal administrations of cytosine arabinoside.Acta Neuropathologica 44, 41–5.

    Google Scholar 

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Takagishi, Y., Yamamura, H. Membrane structure of parallel-fibre synaptic terminals in the cerebellum of the jaundiced Gunn rat: freeze-fracture and E-PTA study. J Neurocytol 23, 39–48 (1994). https://doi.org/10.1007/BF01189815

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  • DOI: https://doi.org/10.1007/BF01189815

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