Advertisement

Purkinje Cell Heterogeneity: Its Role in Organizing the Topography of the Cerebellar Cortex Connections

  • Marion Wassef
  • Pierre Angaut
  • Leonor Arsenio-Nunes
  • Frank Bourrat
  • Constantino Sotelo

Abstract

The cerebellar cortex comprises a few cell types and two main afferent systems arranged in a stereotyped synaptic pattern that is repeated monotonously throughout. The regularity of the laminated structure of the cerebellar cortex permits the identification of the main cell types, even on conventionally stained sections, based on their position and size. Contrasting with its regular architecture, the cerebellar cortex is subdivided into a mosaic of small functional zones defined by the precise pattern of their afferent and efferent connections. In this chapter, we report and discuss work from our laboratory aimed at understanding how such a precise organization of the cerebellar projection maps is achieved during development. Different lines of evidence are presented in favor of the hypothesis that, during development, the cerebellar cortex develops an intrinsic topographic map through its subdivision into small sets of biochemically different Purkinje cells (PC). We propose that this PC heterogeneity is subsequently recognized by afferent fibers and thus underlies the topography of the cerebellar cortex connections. Before presenting our results, a brief description of the early stages of the embryonic development of the cerebellum in rats and mice is worthwhile.

Keywords

Purkinje Cell Cerebellar Cortex Inferior Olive Climbing Fiber Sagittal Band 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Altman, J. (1972a): Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer. J. Comp. Neurol., 145, 353–398.Google Scholar
  2. Altman, J. (1972b): Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and the molecular layer. J. Comp. Neurol., 145, 399–464.Google Scholar
  3. Altman, J. (1972c): Postnatal development of the cerebellar cortex in the rat. III. Maturation of the components of the granular layer. J. Comp. Neurol, 145, 465–514.Google Scholar
  4. Altman, J., and Bayer, S.A. (1978): Prenatal development of the cerebellar system in the rat. I. Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum. J. Comp. Neurol, 179, 23–48.Google Scholar
  5. Altman, J., and Winfree, A.R. (1977): Postnatal development of the cerebellar cortex in the rat. V. Spatial organization of Purkinje cell perikarya. J. Comp. Neurol, 171, 1–16.Google Scholar
  6. Alvarado-Mallart, R.M, and Sotelo C. (1982): Differentiation of cerebellar anlage heterotopically transplanted to adult rat brain: A light and electron microscopic study. J. Comp. Neurol, 212, 247–267.PubMedCrossRefGoogle Scholar
  7. Armstrong, D.M, Harvey, R.J., and Schild, R.F. (1973): The spatial organization of climbing fibre branching in the cat cerebellum. Exp. Brain Res., 18, 40–58.PubMedGoogle Scholar
  8. Armstrong, D.M, Harvey, R.J, and Schild, R.F. (1974) Topographical localization in the olivocerebellar projection: An electrophysiological study in the cat. J. Comp. Neurol, 154, 287–302.PubMedCrossRefGoogle Scholar
  9. Arsenio-Nunes, M.L, and Sotelo, C. (1985): Development of spinocerebellar system in the postnatal rat. J. Comp. Neurol, 237, 291–306.PubMedCrossRefGoogle Scholar
  10. Arsenio-Nunes, M.L, Sotelo, C, and Wehrle, R. (1988): Organization of spinocerebellar projection map in three types of agranular cerebellum: Purkinje cells vs. granule cells as organizer element. J. Comp. Neurol, 273, 120–136.Google Scholar
  11. Azizi, S.A, and Woodward, D.J. (1987): Inferior olivary nuclear complex of the rat: Morphology and comments on the principles of organization within the olivocerebellar system. J. Comp. Neurol, 263, 467–484.PubMedCrossRefGoogle Scholar
  12. Brown, B.L, and Graybiel, A.M. (1983): Zonal organization in the cerebellar vermis of the cat. Anat. Rec, 205, 25A.Google Scholar
  13. Campbell, N.C, and Armstrong, D.M. (1983a): The olivocerebellar projection in the rat: An autoradiographic study. Brain Res., 275, 215–233.PubMedCrossRefGoogle Scholar
  14. Campbell, N.C, and Armstrong, D.M. (1983b): Topographical localization in the olivocerebellar projection in the rat: An autoradiographic study. Brain Res., 275, 235–249.PubMedCrossRefGoogle Scholar
  15. Chan-Palay, V, Nilaver, G, Palay, S.L, Beinfeld, M.C, Zimmerman, E.A, Wu, J.Y, and O’Donohue, T.L. (1981): Chemical heterogeneity in cerebellar Purkinje cells: Existence and coexistence of glutamic acid decarboxylase-like and motilin-like immunoreactivities. Proc. Natl Acad. Sci. USA, 78, 7787–7791.PubMedCrossRefGoogle Scholar
  16. Chan-Palay, V, Palay, S.L, and Wu, J.Y. (1982): Sagittal cerebellar microbands of taurine neurons: Immunocytochemical demonstration by using antibodies against the taurine-synthesizing enzyme cystein sulfinic acid decarboxylase. Proc. Natl Acad. Sci. USA, 79, 4421–4225.Google Scholar
  17. Crepel, F. (1971): Maturation of climbing fiber responses in the rat. Brain Res., 35, 272–276.PubMedCrossRefGoogle Scholar
  18. Crepel, F, Mariani, J, and Delhaye-Bouchaud, N. (1976): Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J. Neurobiol, 7, 567–578.CrossRefGoogle Scholar
  19. Crepel, F, Delhaye-Bouehaud, N, and Dupont, J.L. (1981): Fate of the multiple innervation of cerebellar Purkinje cells by climbing fibers in immature control, X-irradiated and hypothyroid rats. Dev. Brain Res., 1, 59–71.Google Scholar
  20. Das, G.D. (1973): Transplantation of cerebellar tissue in the cerebellum of neonate rabbits. Brain Res., 50, 170–173.PubMedCrossRefGoogle Scholar
  21. De Camilli, P., Miller, P, Levitt, P, Walter, U, and Greengard, P. (1984): Anatomy of cerebellar Purkinje cells in the rat determined by a specific immunohistochemical marker. Neuroscience, 11, 761–817.PubMedCrossRefGoogle Scholar
  22. Eisenman, L. (1981): Olivocerebellar projections of the pyramis and copula pyramidis in the rat: Differential projections to parasagittal zones. J. Comp. Neurol, 199, 65–76.PubMedCrossRefGoogle Scholar
  23. Ekerot, C.F, and Larson, B. (1982): Branching of olivary axons to innervate pairs of sagittal zones in the cerebellar anterior lobe of the cat. Exp. Brain Res., 48, 185–198.PubMedCrossRefGoogle Scholar
  24. Feirabend, H.P.K. (1983): Anatomy and development of longitudinal patterns in the architecture of the cerebellum of the white Leghorn (Gallus Domesticus). Leiden University, Leiden, Thesis.Google Scholar
  25. Gravel, C, Eisenman, L, Sasseville, R, and Hawkes, R. (1987): Parasagittal organization of the rat cerebellar cortex: A direct correlation between antigenic bands revealed by mabQ113 and the topography of the olivocerebellar projection. J. Comp. Neurol, 265, 294–310.PubMedCrossRefGoogle Scholar
  26. Groenewegen, H.J, and Voogd, J. (1977): The parasagittal zonation within the olivocerebellar projection. I. Climbing fiber distribution in the vermis of cat cerebellum. J. Comp. Neurol, 174, 417–488.Google Scholar
  27. Groenewegen, H.J, Voogd J, and Freedman, S.L. (1979): The parasagittal zonation within the olivocerebellar projection. II. Climbing fiber distribution in the intermediate and hemispheric parts of cat cerebellum. J. Comp. Neurol, 183, 551–602.Google Scholar
  28. Hanaway, J. (1967): Formation and differentiation of the external granular layer of the chick cerebellum. J. Comp. Neurol, 131, 1–14.PubMedCrossRefGoogle Scholar
  29. Hawkes, R, Colonnier, M, and Leclerc, N. (1985): Monoclonal antibodies reveal saggital banding in the rodent cerebellar cortex. Brain Res., 333, 359–365.PubMedCrossRefGoogle Scholar
  30. Hawkes, R, and Leclerc, N. (1987): Antigenic map of the rat cerebellar cortex: The distribution of parasagittal bands as revealed by a monoclonal anti-Purkinje cell antibody mabQ113. J. Comp. Neurol, 256, 29–41.PubMedCrossRefGoogle Scholar
  31. Hess, D.H, and Voogd, J. (1986): Chemoarchitectonic zonation of the monkey cerebellum. Brain Res., 369, 383–387.PubMedCrossRefGoogle Scholar
  32. Ingram, V.M, Ogren, M.P, Chatot, C.L, Gossel, J.M, and Owens, B.B. (1985): Diversity among Purkinje cells in the monkey cerebellum. Proc. Natl. Acad. Sci. USA, 82, 7131–7135.PubMedCrossRefGoogle Scholar
  33. Jande, S.S, Maler, L, and Lawson, D.E.M. (1981): Immunocytochemical mapping of vitamin D-dependent calcium-binding protein in brain. Nature (Lond.), 294, 765–767.CrossRefGoogle Scholar
  34. Landis, S.C. (1973): Ultrastructural changes in the mitochondria of cerebellar Purkinje cells of the “nervous” mutant mice. J. Cell Biol, 57, 782–797.PubMedCrossRefGoogle Scholar
  35. Lange, W, Unger, J, Pitzl, H, and Weindl, A. (1986): Is motilin a cerebellar peptide? Anat. Embryol, 173, 371–376.CrossRefGoogle Scholar
  36. Langley, O.K., Reeber, A, Vincendon, G, and Zanetta, J.P. (1982): Fine structural localization of a new Purkinje cell-specific glycoprotein subunit: Immunoelectron microscopical study. J. Comp. Neurol, 208, 335–344.PubMedCrossRefGoogle Scholar
  37. Larramendi, L.M.H. (1969): Analysis of the synaptogenesis in the cerebellum of the mouse. In: Neurobiology of Cerebellar Evolution and Development (R. Llinas, ed.). Chicago: American Medical Association, pp. 803–843.Google Scholar
  38. Leclerc N, Gravel, C, and Hawkes, R. (1988): Development of parasagittal zonation in the rat cerebellar cortex: MabQ113 antigenic bands are created postnatally by the suppression of antigen expression in a subset of Purkinje cells. J. Comp. Neurol, 273, 399–420.PubMedCrossRefGoogle Scholar
  39. Legrand, C, Thomasset, M, Parkes, CO, Clavel, M.C, and Rabie, A. (1983): Calcium-binding protein in the developing rat cerebellum. An immunohistochemical study. Cell Tissue Res., 233, 389–402.Google Scholar
  40. Lohmann, S.M, Walter, U, Miller, P.E, Greengard, P, and De Camilli, P. (1981): Immunohistochemical localization of cyclic GMP-dependent protein kinase in mammalian brain. Proc. Natl Acad. Sci. USA, 78, 653–657.PubMedCrossRefGoogle Scholar
  41. Marani, E, and Voogd, J. (1973): Some aspects of the localization of the enzyme 5’-nucleotidase in the molecular layer of the cerebellum of the mouse. Acta Morphol. Neerl Scand., 11, 353–354.Google Scholar
  42. Marani, E, and Voogd, J. (1977): An acetylcholinesterase band pattern in the molecular layer of the cerebellum of the cat. J. Anat., 124, 335–345.PubMedGoogle Scholar
  43. Mariani, J, and Changeux, J.P. (1981): Ontogenesis of olivocerebellar relationships. I. Studies by intracellular recordings of the multiple innervation of Purkinje cells by climbing fibers in the developing rat cerebellum. J. Neurosci, 1, 696–701.Google Scholar
  44. Meinhardt, H. (1982): Models of Biological Pattern Formation. London: Academic Press.Google Scholar
  45. Meinhardt, H. (1983): Cell determination boundaries as organizing regions for secondary embryonic fields. Dev. Biol. 96, 375–385.PubMedCrossRefGoogle Scholar
  46. Miale, I.L, and Sidman, R.L. (1961): An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp. Neurol, 4, 277–296.PubMedCrossRefGoogle Scholar
  47. Mullen, R.J., Eicher, E.M, and Sidman, R.L. (1976): Purkinje cell degeneration, a new neurological mutation in the mouse. Proc. Natl Acad. Sci. USA, 73, 208–212.PubMedCrossRefGoogle Scholar
  48. Neustadt, A, Frostholm, A, and Rotter, A. (1988): Topographical distribution of muscarinic cholinergic receptors in the cerebellar cortex of the mouse, rat, guinea pig and rabbit: A species comparison. J. Comp. Neurol, 212, 317–330.CrossRefGoogle Scholar
  49. Nilaver, G, Defendini, R, Zimmerman, E.A, Beinfeld, M.C, and O’Donohue, T.L. (1982): Motilin in the Purkinje cell of the cerebellum. Nature, 295, 597–598.PubMedCrossRefGoogle Scholar
  50. Puro, D.G, and Woodward, D.J. (1977a): Maturation of evoked climbing fiber input to rat cerebellar Purkinje cells (I). Exp. Brain Res., 28, 85–100.PubMedGoogle Scholar
  51. Puro, D.G, and Woodward, D.J. (1977b): Maturation of evoked mossy fiber input to rat cerebellar Purkinje cell (II). Exp. Brain Res., 28, 427–441.PubMedGoogle Scholar
  52. Reeber, A, Vincendon, G, and Zanetta, J.P. (1981): Isolation and immunohistochemical localization of a Purkinje cell specific glycoprotein subunit from rat cerebellum. Brain Res., 229, 53–65.PubMedCrossRefGoogle Scholar
  53. Scott, T.G. (1964): A unique pattern of localization within the cerebellum of the mouse. J. Comp. Neurol, 22, 1–7.CrossRefGoogle Scholar
  54. Shimono, T, Nasaka, S, and Sasaki, K. (1976): Electrophysiological study on the postnatal development of neural mechanisms in the rat cerebellar cortex. Brain Res., 108, 279–294.PubMedCrossRefGoogle Scholar
  55. Sidman, R.L, and Green, M.C. (1970): “Nervous”, a new mutant mouse with cerebellar disease. In: Les Mutants Pathologiques Chez l’nimal (M. Sabourdy, ed.) Paris: Centre National de la Recherche Scientifique, pp. 69–79.Google Scholar
  56. Sotelo, C, and Changeux, J.P. (1974a): Transsynaptic degeneration “en cascade” in the cerebellar cortex of staggerer mutant mice. Brain Res., 67, 519–526.PubMedCrossRefGoogle Scholar
  57. Sotelo, C, and Changeux, J.P. (1974b): Bergmann fibers and granular cell migration in the cerebellum of homozygous weaver mutant mouse. Brain Res., 77, 484–491.PubMedCrossRefGoogle Scholar
  58. Sotelo, C, and Triller, A. (1979): Fate of presynaptic afferents of Purkinje cells in adult nervous mutant mouse: A model to study presynaptic stabilization. Brain Res., 175, 11–36.PubMedCrossRefGoogle Scholar
  59. Sotelo, C, Bourrat, F, and Triller, A. (1984) Postnatal development of the inferior olivary complex in the rat. II. Topographic organization of the immature olivocerebellar projection. J. Comp. Neurol, 222, 177–199.Google Scholar
  60. Sperry, R.W. (1944): Optic nerve regeneration with return of vision in anurans. J. Neurophysiol, 1, 57–69.Google Scholar
  61. Sperry, R.W. (1963): Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA, 50, 703–710.PubMedCrossRefGoogle Scholar
  62. Toshio, S, Schoichiro, N, and Kazuo, S. (1976): Electrophysiological study on the postnatal development of neuronal mechanisms in the rat cerebellar cortex. Brain Res., 108, 279–294.CrossRefGoogle Scholar
  63. Von der Malsburg, Ch, and Willshaw, D.J. (1977): How to label nerve cells so that they can interconnect in an ordered fashion. Proc. Natl. Acad. Sci. USA, 74, 5176–5178.PubMedCrossRefGoogle Scholar
  64. Wassef, M, and Sotelo, C. (1984): Asynchrony in the expression of guanosine 3’:5’-phosphate-dependent protein kinase by clusters of Purkinje cells during the perinatal development of rat cerebellum. Neuroscience, 13, 1217–1241.PubMedCrossRefGoogle Scholar
  65. Wassef, M, Zanetta, J.P, Brehier, A, and Sotelo, C. (1985): Transient biochemical compartmentalization of Purkinje cells during early cerebellar development. Dev. Biol, 111, 129–137.PubMedCrossRefGoogle Scholar
  66. Wassef, M, Simons, J, Tappaz, M.L, and Sotelo, C. (1986): Non-Purkinje cell Gabaergic innervation in the deep cerebellar nuclei: A quantitative immunocytochemical study in C57BL and in Purkinje cell degeneration mutant mice. Brain Res., 399, 125–135.PubMedCrossRefGoogle Scholar
  67. Wassef, M, Sotelo, C, Cholley, B, Brehier, A, and Thomasset, M. (1987): Cerebellar mutations affecting the postnatal survival of Purkinje cells in the mouse disclose a longitudinal pattern of differentially sensitivity cells. Dev. Biol 124, 379–389.PubMedCrossRefGoogle Scholar
  68. West, M.J, and Del Cerro, M. (1976): Early formation of synapses in the molecular layer of the fetal rat cerebellum. J. Comp. Neurol, 165, 137–160.PubMedCrossRefGoogle Scholar
  69. Ziai, R, Pan, Y.C.E, Hulmes, J.D, Sangameswaran, L, and Morgan, J.I. (1986): Isolation, sequence, and developmental profile of a brain-specific polypeptide, PEP-19. Proc. Natl. Acad. Sci. USA, 83, 8420–8423.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York, Inc. 1992

Authors and Affiliations

  • Marion Wassef
  • Pierre Angaut
  • Leonor Arsenio-Nunes
  • Frank Bourrat
  • Constantino Sotelo

There are no affiliations available

Personalised recommendations