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The Purkinje cell class may extend beyond the cerebellum

  • Published:
Journal of Neurocytology

Summary

The cerebellum develops from a germinal zone at the rhombic lip of the metencephalon. This region, like the telencephalic vesicle which gives rise to the cerebral cortex, presumably consists of germinative units showing a rather repetitive neurogenetic pattern. In all cerebellar folia, cortical neurons, and especially the Purkinje cells, express highly stereotyped phenotypes, although some variations in their chemical make-up have been uncovered with monoclonal antibodies. Here, we demonstrate for the first time that three independent murine mutations,Lurcher, Purkinje cell degeneration andstaggerer, which result in the postnatal degeneration of Purkinje cells, also cause the elimination of cartwheel cells of the dorsal cochlear nucleus. The cerebellar granule cell mutation,weaver, which spares most Purkinje cells in the lateral cerebellum, also spares cartwheel cells. These data support the notion that the cerebellar germinative zone extends to the caudal portion of the rhombic lip, which gives rise to the dorsal cochlear nucleus.

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References

  • Altman, J. &Bayer, S. A. (1985) Embryonic development of the rat cerebellum. III. Regional differences in the time of origin, migration, and settling of Purkinje cells.Journal of Comparative Neurology 231, 42–65.

    Google Scholar 

  • Altman, J. &Das, G. (1966) Autoradiographic and histological studies of postnatal histogenesis. II. A longitudinal investigation of kinetics, migration and transformation of cells incorporating thymidine in infant rats with special reference to postnatal neurogenesis in some brain regions.Journal of Comparative Neurology 126, 337–90.

    Google Scholar 

  • Berrebi, A. S. &Mugnaini, E. (1988) Effects of the murine mutation ‘nervous’ on neurons in cerebellum and dorsal cochlear nucleus.Journal of Neurocytology 17, 465–84.

    Google Scholar 

  • Blatt, G. J. &Eisenman, L. M. (1985a) A qualitative and quantitative light microscopic study of the inferior olivary complex in the adult staggerer mutant mouse.Journal of Neurogenetics 2, 51–66.

    Google Scholar 

  • Blatt, G. J. &Eisenman, L. M. (1985b) A qualitative and quantitative light microscopic study of the inferior olivary complex of normal, reeler, and weaver mutant mice.Journal of Comparative Neurology 232, 117–28.

    Google Scholar 

  • Breakefield, X. O. (1979)Neurogenetics: Genetic Approaches to the Nervous System. New York: Elsevier.

    Google Scholar 

  • Caddy, K. W. T. &Biscoe, T. J. (1976) The number of Purkinje cells and olive neurones in the normal and Lurcher mutant mouse.Brain Research 111, 396–8.

    Google Scholar 

  • Chang, A. C., Triarhou, L. C., Alyea, C. J., Low, W. C. &Ghetti, B. (1989) Developmental expression of polypeptide PEP-19 in cerebellar cell suspensions transplanted into the cerebellum ofpcd mutant mice.Experimental Brain Research 76, 639–45.

    Google Scholar 

  • Green, M. C. (1981)Genetic Variants and Strains of the Laboratory Mouse. New York: Gustav Fischer Verlag.

    Google Scholar 

  • Hatten, M. E., Liem, R. K. H. &Mason, C. A. (1986) Weaver mouse cerebellar granule neurons fail to migrate on wild-type astroglial processesin vitro.Journal of Neuroscience 6, 2676–83.

    Google Scholar 

  • Hawkes, R., Colonnier, M. &Leclerc, N. (1985) Monoclonal antibodies reveal sagittal banding in the rodent cerebellar cortex.Brain Research 333, 359–65.

    Google Scholar 

  • Herrup, K. &Mullen, R. (1979a) Regional variation and absence of large neurons in the cerebellum of the staggerer mouse.Brain Research 172, 1–12.

    Google Scholar 

  • Herrup, K. &Mullen, R. (1979b) Staggerer chimeras: Intrinsic nature of Purkinje cell defects and implications for normal cerebellar development.Brain Research 178, 443–57.

    Google Scholar 

  • Herrup, K. &Trenkner, E. (1987) Regional differences in cytoarchitecture of the weaver cerebellum suggest a new model for weaver gene action.Neuroscience 23, 871–5.

    Google Scholar 

  • Hirano, A. &Dembitzer, H. M. (1975) The fine structure of staggerer cerebellum.Journal of Neuropathology and Experimental Neurology 34, 1–11.

    Google Scholar 

  • Hockfield, S. (1987) A Mab to a unique cerebellar neuron generated by immunosuppression and rapid immunization.Science 237, 67–70.

    Google Scholar 

  • Jacobson, M. (1978)Developmental Neurobiology. New York: Plenum Press.

    Google Scholar 

  • Landis, S. C. (1973) Ultrastructural changes in the mitochondria of cerebellar Purkinje cells of ‘nervous’ mutant mice.Journal of Cell Biology 57, 782–97.

    Google Scholar 

  • Lasek, R. J. &Black, M. M. (1988) (editors)Intrinsic Determinants of Neuronal Form and function. New York: Alan R. Liss.

    Google Scholar 

  • Mugnaini, E. (1972) The histology and cytology of the cerebellar cortex. InThe Comparative Anatomy and Histology of the cerebellum: The Human Cerebellum, Cerebellar Connections, and Cerebellar Cortex (edited byLarsell, O. &Jansen, J.) pp. 201–265. Minneapolis: University of Minnesota Press.

    Google Scholar 

  • Mugnaini, E. (1985) GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: light and electron microscopic immunocytochemistry.Journal of Comparative Neurology 235, 61–81.

    Google Scholar 

  • Mugnaini, E., Berrebi, A. S., Dahl, A-L. &Morgan, J. I. (1987) The polypeptide PEP-19 is a marker for Purkinje neurons in cerebellar cortex and cartwheel neurons in dorsal cochlear nucleus.Archives Italiennes de Biologie 126, 41–67.

    Google Scholar 

  • Mugnaini, E. &Morgan, J. I. (1987) The neuropeptide cerebellin is a marker for two similar neuronal circuits in rat brain.Proceedings of the National Academy of Sciences (USA) 84, 8692–6.

    Google Scholar 

  • Mullen, R. J. (1977) Site ofpcd gene action and Purkinje cell mosaicism in cerebella of chimeric mice.Nature 270, 245–7.

    Google Scholar 

  • Mullen, R. J., Eicher, E. M. &Sidman, R. L. (1976) Purkinje cell degeneration, a new neurological mutation in the mouse.Proceedings of the National Academy of Sciences (USA) 73, 208–12.

    Google Scholar 

  • Osen, K. K., Ottersen, O. P. &Storm-Mathisen, J. (1987) Glycine-like immunoreactivity in the rat dorsal cochlear nucleus (DCN).Neuroscience (The Second World Congress of Neuroscience Abstracts) 22 supplement, S788.

    Google Scholar 

  • Palay, S. L. &Chan-Palay, V. (1974)Cerebellar Cortex: Cytology and Organization. New York: Springer-Verlag.

    Google Scholar 

  • Pierce, E. T. (1967) Histogenesis of the dorsal and ventral cochlear nuclei in the mouse. An autoradiographic study.Journal of Comparative Neurology 131, 27–54.

    Google Scholar 

  • Rakic, P. (1988) Specification of cerebral cortical areas.Science 241, 170–6.

    Google Scholar 

  • Rakic, P. &Sidman, R. L. (1973) Sequence of developmental abnormalities leading to granule cell deficit in cerebellar cortex of weaver mutant mice.Journal of Comparative Neurology 152, 103–32.

    Google Scholar 

  • Sidman, R. L. (1968) Development of interneuronal connections in brains of mutant mice. InPhysiological and Biochemical Aspects of Nervous Integration (edited byCarlson, F. D.) pp. 163–93. New Jersey: Prentice-Hall.

    Google Scholar 

  • Sidman, R. L., Lane, P. W. &Dickie, M. M. (1962) Staggerer, a new mutation in the mouse affecting the cerebellum.Science 137, 610–12.

    Google Scholar 

  • Smeyne, R. J. &Goldowitz, D. (1989) Development and death of external granular layer cells in the weaver mouse cerebellum: A quantitative study.Journal of Neuroscience 9, 1608–20.

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

    Google Scholar 

  • Sternberger, L. A. (1979)Immunocytochemistry (2nd edition). New York: John Wiley.

    Google Scholar 

  • Wassef, M., Sotelo, C., Cholley, B., Brehier, A. &Thomasset, M. (1987) Cerebellar mutations affecting the postnatal survival of Purkinje cells in the mouse disclose a longitudinal pattern of differentially sensitive cells.Developmental Biology 124, 379–89.

    Google Scholar 

  • Wenthold, R. J., Huie, D., Altshuler, R. A. &Reeks, K. A. (1987) Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex.Neuroscience 22, 897–912.

    Google Scholar 

  • Wetts, R. &Herrup, K. (1982) Interaction of granule, Purkinje, and inferior olivary neurons in Lurcher chimeric mice.Journal of Embryology and Experimental Morphology 68, 87–98.

    Google Scholar 

  • Willard, F. H. &Martin, J. F. (1986) The development and migration of large multipolar neurons into the cochlear nucleus of the North American Opossum.Journal of Comparative Neurology 248, 119–32.

    Google Scholar 

  • Wouterlood, F. G. &Mugnaini, E. (1984) Cartwheel neurons of the dorsal cochlear nucleus. A Golgi-electron microscopic study in the rat.Journal of Comparative Neurology 227, 136–57.

    Google Scholar 

  • Yoon, C. H. (1976) Pleiotropic effect of the staggerer gene.Brain Research 109, 206–15.

    Google Scholar 

  • Ziai, R., Pan, Y-C. E., Mulmes, J. D., Sangameswaran, L. &Morgan, J. I. (1986) Isolation, sequence, and developmental profile of a brain-specific polypeptide, PEP-19.Proceedings of the National Academy of Sciences (USA) 83, 8420–3.

    Google Scholar 

  • Ziai, M. R., Sangameswaran, L., Hempstead, J. L., Danho, W. &Morgan, J. I. (1988) An immunochemical analysis of the distribution of a brain-specific polypeptide, PEP-19.Journal of Neurochemistry 51, 1771–6.

    Google Scholar 

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Authors and Affiliations

  1. Laboratory of Neuromorphology, U-154, Biobehavioral Sciences Graduate Degree Program, The University of Connecticut, 06269-4154, Storrs, CT, USA

    A. S. Berrebi & E. Mugnaini

  2. Department of Neuroscience, Roche Institute of Molecular Biology, Roche Research Center, 07110, Nutley, NJ, USA

    J. I. Morgan

Authors
  1. A. S. Berrebi
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  2. J. I. Morgan
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  3. E. Mugnaini
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Berrebi, A.S., Morgan, J.I. & Mugnaini, E. The Purkinje cell class may extend beyond the cerebellum. J Neurocytol 19, 643–654 (1990). https://doi.org/10.1007/BF01188033

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  • DOI: https://doi.org/10.1007/BF01188033

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