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Zebrins: Molecular Markers of Compartmentation in the Cerebellum

  • Richard Hawkes
  • Gino Brochu
  • Louise Doré
  • Claude Gravel
  • Nicole Leclerc

Abstract

Ordered projections in the brain are established in several stages. Initially, the formation of an afferent pathway depends on white matter interactions, such as contact guidance along genetically determined pathways and selective axon fasciculation, to guide neurites to the correct target fields. Subsequently, target cell recognition by afferent growth cones and competition between growth cones for targets (and between targets for inputs) serve to eliminate superfluous or incorrect projections and may refine the topography. Many regions, including the neocortex, the superior colliculus, the striatum, and the dorsal column nuclei, are functionally organized in the form of patches or stripes that correspond to the discrete segregation of the afferent or efferent axons. The same appears to be true in the cerebellum. Studies using the retrograde-anterograde axonal transport of tracers, electrophysiological recording, somatotopic mapping, and molecular mapping have all revealed a parasagittal bandlike topographical organization of the cerebellar cortex and its afferent and efferent connections. We are using pattern formation in the cerebellar cortex as a model to explore the rules that give rise to topographically ordered projections.

Keywords

Purkinje Cell Cerebellar Cortex Granular Layer Mossy Fiber Cerebellar Nucleus 
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.

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References

  1. Altman, J. (1972): Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkirije cells and of the molecular layer. J. Comp. Neurol., 145, 399–464.Google Scholar
  2. Armstrong, D.M., Campbell, N.C., Edgley, S.A., Schild, R.F., and Trott, J.R. (1982): Investigations of the olivocerebellar and spino-olivary pathways. In: The Cerebellum: New Vistas. (S. Palay and V. Chan-Palay, eds). Berlin: Springer-Verlag, pp. 195–232.CrossRefGoogle Scholar
  3. 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.Google Scholar
  4. Armstrong, D.M., and Schild, R.F. (1978): An investigation of the cerebellar corticonuclear projections in the rat using an autoradiographic tracing method. I. Projections from the vermis. Brain Res., 141, 1–19.Google Scholar
  5. Arsenio-Nunes, M.L., and Sotelo, C. (1985): Development of the spinocerebellar system in the postnatal rat. J. Comp. Neurol., 237, 291–306.PubMedCrossRefGoogle Scholar
  6. Beinfeld, M.C., and Korchak, D.M. (1985): The regional distribution and the chemical, chromatographic immunologic characterization of motilin brain peptide: The evidence for a difference between brain and intestinal motilin-immunoreactive material. J. Neurosci, 5, 2502–2509.PubMedGoogle Scholar
  7. Beyerl, B.D., Borges, L.F., Swearingen, B., and Sidman, R.L. (1982): Parasagittal organization of the olivocerebellar projection in the mouse. J. Comp. Neurol., 209, 339–346.PubMedCrossRefGoogle Scholar
  8. Bishop, G.A. (1982) The pattern of distribution of the local axonal collaterals of Purkinje cells in the intermediate cortex of the anterior lobe and paramedian lobule of the cat cerebellum. J. Comp. Neurol., 210, 1–9.PubMedCrossRefGoogle Scholar
  9. Bloedel, J.R., and Courville, J. (1981): Cerebellar afferent systems. In: Handbook of Physiology. (J.M. Brookhart, V.B. Mountcastle, and V.B. Brooks, eds). Bethesda, MD: American Physiology Society, 2, 735–829.Google Scholar
  10. Boegman, R., Parent, A., and Hawkes, R. (1988) Zonation in the rat cerebellar cortex: Patches of high acetylcholinesterase activity in the granular layer are congruent with Pukinje cell compartments. Brain Res., 448, 237–251.PubMedCrossRefGoogle Scholar
  11. Brochu, G., Maler, L., and Hawkes, R. (1990): Zebrin II: A polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. J. Comp. Neurol., 291, 538–552.PubMedCrossRefGoogle Scholar
  12. Brodal, A. (1976): The olivocerebellar projection in the cat as studied with the method of retrograde axonal transport of horseradish peroxidase. II. The projection to the uvula. J. Comp. Neurol, 166, 417–426.Google Scholar
  13. Brodal,A.(1980): Olivocerebellocortical projection in the cat as determined with the method of retrograde axonal transport of horseradish peroxidase 2. Topographical pattern in relation to the longitudinal sub-division of the cerebellum. In: The Inferior Olivary Nucleus: Anatomy and Physiology (J. Courville, C. de Montigny, and Y. Lamarre eds). New York: Raven Press, pp. 187–205.Google Scholar
  14. Brodal, A., Walberg, F., and Hoddevik, G.H. (1975): The olivocerebellar projection in the cat as studied with the method of retrograde axonal transport of horseradish peroxidase I. The projection to the paramedian lobule. J. Comp. Neurol., 164,449–470.CrossRefGoogle Scholar
  15. Brown, B.L., and Graybiel, A.M. (1983): Zonal organization in the cerebellar vermis of the cat. Anat. Rec., 205, 25A.Google Scholar
  16. Campbell, N.C., and Armstrong, D.M. (1983a): The olivocerebellar projection in the rat: An autoradiographic study. Brain Res., 275, 215–233.PubMedCrossRefGoogle Scholar
  17. 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
  18. Campistron, G., Geffard, M., and Buijs, R.M. (1986): Immunological approach to the detection of taurine and immunocytochemical results. J. Neurochem., 46, 862–868.PubMedCrossRefGoogle Scholar
  19. Chambers, W.W., and Sprague, J.M. (1955a): A functional localization in the cerebellum: I. Organization in longitudinal corticonuclear zones and their contribution to the control of posture, both extrapyramidal and pyramidal. J. Comp. Neurol., 103, 105–130.CrossRefGoogle Scholar
  20. Chambers, W.W., and Sprague, J.M. (1955b): Functional localization in the cerebellum: II. Somatotopic organization in cortex and nuclei. Arch. Neurol. Psychiatry, 74, 653–680.Google Scholar
  21. Changeux, J.P., and Danchin, A. (1976): Selective stabilization of developing synapses, a mechanism for the specification of neuronal networks. Nature, 264, 705–712.PubMedCrossRefGoogle Scholar
  22. Chan-Palay, V. (1971): The recurrent collaterals of Purkinje cell axons: A correlated study of the rat’s cerebellar cortex with electron microscopy and the Golgi method. Z. Anat. Entwickl.-Gesch., 134, 200–234.CrossRefGoogle Scholar
  23. 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 co-existence of glutamic acid decarboxylase-like and motilin-like immunoreactivities. Proc. Natl. Acad. Sci. USA, 78,7787–7791.PubMedCrossRefGoogle Scholar
  24. Chan-Palay, V., Palay, S.L., Brown, J.T, and Van Itallie, C. (1977): Sagittal organization of olivocerebellar and reticulocerebellar projections: Autoradiographic studies with 35S-methionine. Exp. Brain Res., 30, 561–576.PubMedCrossRefGoogle Scholar
  25. 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 cysteine sulfinic acid decarboxylase. Proc. Natl. Acad. Sci. USA, 79, 4221–4225.PubMedCrossRefGoogle Scholar
  26. Constantine-Paton, M. (1982): The retinotectal hookup: the process of neural mapping. In Developmental Order: Its Origin and Regulation (S. Subtelny, ed). New York: Alan R. Liss Inc, pp. 317–349.Google Scholar
  27. Courville, J. (1975): Distribution of olivocerebellar fibers demonstrated by a radioautographic tracing method. Brain Res., 95, 253–263.PubMedCrossRefGoogle Scholar
  28. Courville, J., and Diakiw, N. (1976): Cerebellar corticonuclear projection in the cat. The vermis of anterior and posterior lobes. Brain Res., 110, 1–20.Google Scholar
  29. Courville, J., and Faraco-Cantin, F. (1978): On the origin of the climbing fibers of the cerebellum. An experimental study in the cat with an autoradio¬graphic tracer method. Neuroscience, 3, 797–809.PubMedCrossRefGoogle Scholar
  30. Crepel, F. (1971): Maturation of climbing fiber responses in the rat. Brain Res., 35, 272–276.PubMedCrossRefGoogle Scholar
  31. Crepel, F. (1982): Regression of functional synapses in the immature mammalian cerebellum. Trends Neurosci., 5, 266–269.CrossRefGoogle Scholar
  32. Crepel, F., Mariani, J., and Delhaye-Bouchard, N. (1976): Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J. Neurobiol., 1, 567–578.CrossRefGoogle Scholar
  33. Doré, L., Jacobson, C.D., and Hawkes, R. (1990): The organization and postnatal development of zebrin II antigenic compartmentation in the cerebellar vermis of the grey opossum, Monodelphis domestica. J. Comp. Neurol, 291,431–449.CrossRefGoogle Scholar
  34. Eisenman, L. (1981) Olivocerebellar projections to the pyramis and copula pyramidis in the rat: Differential projections to parasagittal zones. J. Comp. Neurol, 199, 65–76.PubMedCrossRefGoogle Scholar
  35. Eisenman, L.M. (1984): Organization of the olivocerebellar projection to the uvula in the rat. Brain Behav. Evol, 24, 1–12.PubMedCrossRefGoogle Scholar
  36. Eisenman, L.M., and Goracchi, G.P. (1983): A double label retrograde tracing study of the olivocerebellar projection to the pyramis and uvula in the rat. Neurosci. Lett., 41, 15–20.PubMedCrossRefGoogle Scholar
  37. Eisenman, L.M., and Hawkes, R. (1990): 5’-nucleotidase and the mabQ113 antigen share a common distribution in the cerebellar cortex of the mouse. Neuroscience, 31, 231–235.CrossRefGoogle Scholar
  38. Eisenman, L.M, Sieger, D.D., and Blatt, G.J. (1983): The olivocerebellar projection to the uvula in the mouse. J. Comp. Neurol, 221, 53–59.PubMedCrossRefGoogle Scholar
  39. Goodman, D.C, Hellitt, R.E, and Welch, R.B. (1963): Patterns of localization in the cerebellar corticonuclear projections of the albino rat. J. Comp. Neurol, 121, 51–68.PubMedCrossRefGoogle Scholar
  40. Gravel, C, Eisenman, L.M, Sasseville, R, and Hawkes, R, (1987): Parasagittal organization of the rat cerebellar cortex: direct correlation between antigenic Purkinje cell bands revealed by mabQ113 and the organization of the olivocerebellar projection. J. Comp. Neurol., 265, 295–310.CrossRefGoogle Scholar
  41. Gravel, C., and Hawkes, R. (1990): Parasagittal organization of the rat cerebellar cortex: Direct comparison of Purkinje cell compartments and the organization of the spinocerebellar projection. J. Comp. Neurol., 291, 79–102.PubMedCrossRefGoogle Scholar
  42. Gravel, C., Leclerc, N., Plioplys, A., and Hawkes, R. (1986): Focal axonal swellings in rat cerebellar Purkinje cells during normal development. Brain Res., 363, 325–332.PubMedCrossRefGoogle Scholar
  43. 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
  44. Groenewegen, H.J., Voogd, J., and Freeman, 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
  45. Haines, D.E., Patrick, G.W., and Satrulee, P. (1982): Organization of cerebellar corticonuclear fiber systems. In: The Cerebellum—New Vistas (S.L.Palayand V. Chan-Palay,eds). Berlin-Heidelburg-New York: Springer-Verlag, pp. 320–367.CrossRefGoogle Scholar
  46. Hawkes, R., Colonnier, ML, and Leclerc, N. (1985): Monoclonal antibodies reveal sagittal banding in the rodent cerebellar cortex. Brain Res., 333,359–365.PubMedCrossRefGoogle Scholar
  47. Hawkes, R., and Leclerc, N. (1986): Immunocytochemical demonstration of topographic ordering of Purkinje cell axon terminals in the fastigial nuclei of the rat. J. Comp. Neurol., 244, 481–491.PubMedCrossRefGoogle Scholar
  48. Hawkes, R., and Leclerc, N. (1987): Antigenic map of the rat cerebellar cortex: the distribution of parasagittal bands as revealed by monoclonal anti-Purkinje cell antibody mabQl 13. J. Comp. Neurol., 256,29–41.PubMedCrossRefGoogle Scholar
  49. Hawkes, R., and Leclerc, N. (1989): Purkinje cell axon collateral distributions reflect the chemical compartmentation of the rat cerebellar cortex. Brain Res., 476, 279–290.PubMedCrossRefGoogle Scholar
  50. Hazlett, J.C., Martin, G.F., and Dom, R. (1971): Spinocerebellar fibers of the opossum Didelphis marsupialis virginiana. Brain Res., 33, 257–271.PubMedCrossRefGoogle Scholar
  51. Hess, D.T., and Hess, A. (1986): 5’-nucleotidase of cerebellar molecular layer: Reduction in Purkinje cell-deficient mice. Brain Res., 394, 93–100.PubMedGoogle Scholar
  52. Hess, D.T., and Voogd, J. (1986): Chemoarchitectonic zonation of the monkey cerebellum. Brain Res., 369, 383–387.PubMedCrossRefGoogle Scholar
  53. Hillman, D.E., and Chen, S. (1981): Vunerability of cerebellar development in malnutrition. I. Quantitation of layer volume and neuron numbers. Neuro- science, 6, 1249–1262.Google Scholar
  54. Ingram, V.I., Ogren, M.P., Chatot, C.L., Gossels, 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
  55. Jansen, J., and Brodal, A. (1940): Experimental studies on the intrinsic fibers of the cerebellum II. The corticonuclear projection. J. Comp. Neurol., 73, 267–321.CrossRefGoogle Scholar
  56. Jansen, J., and Brodal, A. (1942): Experimental studies on the intrinsic fibers of the cerebellum. The corticonuclear projection in the rabbit and in the monkey (Macacus rhesus). Nor she Vid. Akad., Oslo, Avh. I. Mat. Naturv, Kl.,3, 1–50.Google Scholar
  57. Joseph, J.W., Shambes, G.M., Gibson, J.M., and Welker, W. (1978): Tactile projections to granule cells in caudal vermis of the rat’s cerebellum. Brain Behav. Evol., 15, 141–149.PubMedCrossRefGoogle Scholar
  58. Kassel, J., Shambes, G.M., and Welker, W. (1984): Fractured cutaneous projections to the granule cell layer of the posterior cerebellar hemisphere of the domestic cat. J. Comp. Neurol., 225, 458–468.PubMedCrossRefGoogle Scholar
  59. Killackey, H.P., and Belford, G.R. (1980): Central correlates of peripheral pattern alterations in the trigeminal system of the rat. Brain Res., 183, 205–210.PubMedCrossRefGoogle Scholar
  60. Lange,W. (1982): Regional differences in the cytoarchitecture of the cerebellar cortex. In: The Cerebellum— New Vistas. (S.L. PalayandV. Chan-Palay, eds). Berlin-Heidelburg-New York: Springer-Verlag, pp. 93–105.CrossRefGoogle Scholar
  61. Lange, W., Unger, J., Pitzl, H., and Weindl, A. (1986): Is motilin a cerebellar peptide in the rat? Anat. Embryol, 173, 371–376.CrossRefGoogle Scholar
  62. Law, M.I., and Constantine-Paton, M. (1980): Right and left eye bands in frogs with unilateral tectal ablations. Proc. Natl. Acad’. Sci. USA, 11,2314–2318.CrossRefGoogle Scholar
  63. Leclerc, N., Beesley, P.W., Colonnier, M., Brown, I., Gurd, J.W., Paladino, T, and Hawkes, R. (1990a): Synaptophysin expression during synaptogenesis in the rat cerebellar cortex. J. Comp. Neurol, 280,197–212.CrossRefGoogle Scholar
  64. Leclerc, N., Doré, L., Parent, A., and Hawkes, R. (1990b): The compartmentation of the monkey and rat cerebellar cortex: zebrin I and cytochrome oxidase. Brain Res., 506, 70–78.PubMedCrossRefGoogle Scholar
  65. Leclerc, N., Gravel, C., and Hawkes, R. (1988): Development of parasagittal zonation in the rat cerebellar cortex: MabQl 13 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
  66. Leclerc, N., Herrup, K., Hawkes, R., Schwarting, G., and Yamamoto, M. (1990c): Zebrin II and O-acetyl GD3 divide all Purkinje cells into two distinct complementary sets. 20th Annual Meeting of the Society of Neuroscience 16, 642.Google Scholar
  67. Madsen, S., Ottersen, O.P., and Storm-Mathisen, J. (1985): Immunocytochemical visualization of taurine: Neuronal localization in the rat cerebellum. Neurosci. Lett, 60, 255–260.PubMedCrossRefGoogle Scholar
  68. Magnussen, K.R., Madl, J.E, Clements, J.R, Wu, J.-Y, Larson, A.A, and Beitz, A.J. (1988): Colocalization of taurine- and cysteine sulfinic acid decarboxylase-like immunoreactivity in the cerebellum of the rat with monoclonal antibodies against taurine. J. NeuroscL, 8, 4551–4564.Google Scholar
  69. Marani, E. (1982a): Topographic enzyme histochemistry of the mammalian cerebellum: 5’-nucleotidase and acetylcholinesterase. Thesis, University of Leiden.Google Scholar
  70. Marani, E.(1982b): The ultrastructural localization of 5’-nucleotidase in the molecular layer of the mouse cerebellum. In: Neurotransmitter Interaction and Compartmentation (H.F. Bradford, ed). New York: Plenum Publishing Corp, pp. 557–571.Google Scholar
  71. Marani, E, and Voogd, J. (1977): An acetylcholinesterase band pattern in the molecular layer of the cat cerebellum. J. Anat., 124, 335–345.PubMedGoogle Scholar
  72. 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. NeuroscL, 1, 696–702.Google Scholar
  73. Mason, C.A, and Gregory, E. (1984): Postnatal maturation of cerebellar mossy and climbing fibers: Transient expression of dual features on single axons. J. NeuroscL, 4, 1715–1735.Google Scholar
  74. Morest, D.K. (1969): The growth of dendrites in the mammalian brain. Z. Anat. entwickl-Gesch., 128, 290–317.CrossRefGoogle Scholar
  75. O’Leary, D.D.M., Fawcett, J.M., and Cowan, W.M. (1986): Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. J. NeuroscL, 6, 3692–3705.Google Scholar
  76. O’Leary, J.L., Petty, J., Smith, J.M., O’Leary, M., and Inukai, S. (1968): Cerebellar cortex of rat and other animals. A structural and ultrastructural study. J. Comp. Neurol, 134, 401–432.Google Scholar
  77. Oscarsson, O. (1969): The sagittal organization of the cerebellar anterior lobe as revealed by the projection patterns of the climbing fiber system. In: Neurobiology of Cerebellar Organization and Development. (R. Llinas, ed). Chicago: American Medical Association, pp. 525–532.Google Scholar
  78. Oscarsson, O.(198Q): Functional organization of olivary projection to the cerebellar anterior lobe. In: The Inferior Olivary Nucleus: Anatomy and Physiology (J. Courville, C de Montigny, and Y. Lamarre, eds). New York: Raven Press, pp. 279–289.Google Scholar
  79. Oscarsson, O., and Sjolund, B. (1977): The ventral spino-olivocerebellar system in the cat 1. Identification of five paths and their termination in the cerebellar anterior lobe. Exp. Brain Res., 28, 469–486.Google Scholar
  80. Oster-Granite, M.L., and Gearhart, J. (1982): Cell lineage analyses of Purkinje cells in murine chimeras. In: The Cerebellum—New Vistas (S.L. Palay and V. Chan-Palay, eds). Berlin-Heidelberg-New York: Springer-Verlag, pp. 75–92.CrossRefGoogle Scholar
  81. Palay, S.L., and Chan-Palay, V. (1974): Cerebellar Cortex, Cytology and Organization. New York-Heidelburg-Berlin: Springer-Verlag.CrossRefGoogle Scholar
  82. Palkovits, M., Mezey, M., Hamori, J., and Szentagothai, J. (1977): Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and on synapses. Exp. Brain. Res., 28, 189–209.Google Scholar
  83. Plioplys, A.V., and Hawkes, R. (1986): A survey of mabQ113 immunoreactivity in the adult rat brain: Differential staining of the lateral and medial habe-nular nuclei. Brain Res., 375, 1–12.PubMedCrossRefGoogle Scholar
  84. Plioplys, A.V., and Hawkes, R. (1987): The development of differential mabQl 13 immunoreactivity in the rat habenular complex. Brain Res. Bull, 18, 19–24.PubMedCrossRefGoogle Scholar
  85. Plioplys, A.V., and Hawkes, R. (1988): Developmental expression of monoclonal antibody mabQl 13 immunoreactivity in the rat cerebral cortex: Differential sublayering of layer I and labelling of radial glia. J. Neurosci. Res., 20, 359–375.PubMedCrossRefGoogle Scholar
  86. Plioplys, A.V., Thibault, J., and Hawkes, R. (1985): Selective staining of a subset of Purkinje cells in the human cerebellum with monoclonal antibody mabQl 13. J. Neurol. ScL, 70, 245–256.CrossRefGoogle Scholar
  87. Puro, D.G., and Woodward, D.J. (1977): Maturation of evoked climbing fiber input to rat Purkinje cells. Exp. Brain Res., 28, 85–110.PubMedGoogle Scholar
  88. Ramon-Moliner, E. (1972): Acetylthiocholinesterase distribution in the brainstem of the cat. Ergeb. Anat., 46, 1–52.Google Scholar
  89. Ramon y Cajal, S. (1911): Histologic du Systeme Nerveux de l’Homme et des Vertebres. Paris: Maloine.Google Scholar
  90. Robertson, B., Grant, G, and Bjorkeland, M. (1983): Demonstration of spinocerebellar projections in cat using anterograde WGA-HRP with some observations on spinomesencephalic and spinothalamic projections. Exp. Brain Res., 52, 99–104.PubMedGoogle Scholar
  91. Scheibel, A. (1977): Sagittal organization of mossy fiber terminal systems in the cerebellum of the rat: A Golgi study. Exp. Neurol, 57, 1067–1070.PubMedCrossRefGoogle Scholar
  92. Scott, T.G. (1963): A unique pattern of localization in the cerebellum. Nature, 200, 793.PubMedCrossRefGoogle Scholar
  93. Scott, T.G. (1964): A unique pattern of localization within the cerebellum of the mouse. J. Comp. Neurol, 122, 1–8.CrossRefGoogle Scholar
  94. Shambes, G.M., Beerman, D.H., and Welker, W. (1978a): Multiple tactile area in cerebellar cortex: Another patchy cutaneous projection to granule cell columns in rat. Brain Res., 157, 123–128.PubMedCrossRefGoogle Scholar
  95. Shambes, G.M., Gibson, J.M., and Welker, W. (1978b): Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. Brain Behav. Evol, 15, 94–140.PubMedCrossRefGoogle Scholar
  96. Sotelo, C. (1987): Cerebellar synaptogenesis and the organization of afferent projection maps. Pontificae Acad. Scient. Scripta Varia, 59, 65–90.Google Scholar
  97. 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
  98. Tomida, Y, and Kimura, H. (1987): Immunohisto-chemical and biochemical studies of substances with taurine-like immunoreactivity in the brain. Acta Histochem. Cytochem., 20, 31–40.CrossRefGoogle Scholar
  99. Van der Loos, H, and Woolsey, T.A. (1973): Somatosensory cortex: Structural alterations following early injury to sense organs. Science, 179, 395–398.PubMedCrossRefGoogle Scholar
  100. Van Gilder, J.C, and O’Leary, J.L. (1970): Topical projection of the olivocerebellar system in the cat: an electrophysiological study. J. Comp. Neurol, 140, 69–80.CrossRefGoogle Scholar
  101. Von de Malsburg, C, and Willshaw, D.J. (1976): Mechanism for producing continuous neural mapping: Ocularity dominance stripes and ordered retinotectal projections. Exp. Brain. Res., Suppl 1, 463–469.Google Scholar
  102. Voogd, J. (1964): The Cerebellum of the Cat. Assen: Van Gorcum.Google Scholar
  103. Voogd, J. (1967): Comparative aspects of the structure and fibre connections of the mammalian cerebellum. Prog. Brain Res., 25, 94–135.PubMedCrossRefGoogle Scholar
  104. Voogd, J. (1969): The importance of fiber connections in the comparative anatomy of the mammalian cerebellum. In: Neurobiology of Cerebellar Evolution and Development (R. Llinas, ed). Chicago: American Medical Association, pp. 493–514.Google Scholar
  105. Voogd, J. and Bigaré, F. (1980): The topographical distribution of olivary and corticonuclear fibers in the cerebellum. A review. In: The Inferior Olivary Nucleus: Anatomy and Physiology (J. Courville, C. de Montigny, and Y. Lamarre, eds). New York: Raven Press, pp. 207–234.Google Scholar
  106. Voogd, J.Gerrits, N.M, and Marani, E. (1985): Cerebellum. In: The Rat Nervous System (G. Paxinos, ed). New York: Academic Press, 2, 251–291.Google Scholar
  107. 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
  108. Wassef, M, Sotelo, C, Thomasset, M, Granholm, A-C, Leclerc, N, Rafrafi, R, and Hawkes, R. (1990): Expression of compartmentation antigen zebrin I in cerebellar transplants. J. Comp. Neurol, 294, 223–234.PubMedCrossRefGoogle Scholar
  109. 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
  110. Welker, W.(1987): Spatial organization of somatosensory projections to granule cell cerebellar cortex: Functional and connectional implications of fractured somatotopy. In: New Concepts in Cerebellar Neurobiology (J.S. King ed). New York: Alan R. Liss Inc., pp. 239–280.Google Scholar
  111. Welker, W, and Shambes, G.M. (1985): Tactile cutaneous representation in cerebellar granule cell layer of the opossum, Didelphis virginiana. Brain Behav. Evol. 27, 57–79.CrossRefGoogle Scholar
  112. Yaginuma, H, and Matsushita, M. (1986): Spinocerebellar projection fields in the horizontal plane of lobules of the cerebellar anterior lobe in the cat: An anterograde wheat germ agglutinin-horseradish peroxidase study. Brain Res., 365, 345–349.PubMedCrossRefGoogle Scholar

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© Springer-Verlag New York, Inc. 1992

Authors and Affiliations

  • Richard Hawkes
  • Gino Brochu
  • Louise Doré
  • Claude Gravel
  • Nicole Leclerc

There are no affiliations available

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