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Distribution of mGluR1α and SMI 311 immunoreactive Lugaro cells in the kitten cerebellum

  • Published:
Journal of Neurocytology

Abstract

The Lugaro cell is a feedback interneuron of the cerebellar cortex, recognizable by its characteristic morphology. Postnatal neuronal migration to the cortex has been described for several cerebellar interneurons. Since in our previous studies we observed Lugaro-like cells (LCs) in the white matter (WM) and internal granular layer (IGL) of the cerebellum of young cats, we assumed that a proportion of these cells migrate also postnatally to their destination. In the present study using and immunostaining for the metabotropic glutamate receptor mGluR1α and neurofilament protein SMI 311 the number and spatial distribution of LCs at different postnatal days were investigated.

We found that the number and distribution of both mGluR1a-immunoreactive (ir) and of SMI 311-ir LCs changed with age in the developing cerebellar cortex of kittens: developing LCs express mGluR1α already in the newborn, while expression of SMI 311-ir in LCs appears only about a week later. At postnatal day 1 (P1) relatively few mGluR1-ir LCs were detected in the WM and at the border of WM and IGL. Later, their number increased sharply until P15 (6–7 fold) and decreased continuously between P15 and P135. SMI 311-ir LCs were not present at P1 and even at P8 only a few were observed in the WM or in infraganglionic positions. Their number increased gradually (12–14 fold) until adulthood when their number was stabilized at 8.000–10.000/cerebellum. At the same time the number of probably ectopic SMI 311-ir LCs decreased with age: at P22 about one third of them was found in “ectopic” position, whereas in the adult cat only about 10–12% of LCs's was either in the WM or scattered in the whole depth of the granular layer.

These results suggest that: (1) most LCs appear in the cerebellar cortex postnatally; and (2) postnatal migration and incorporation of LCs to the cortex is a much longer process than previously expected, occurring even after the cytoarchitectonic built-up (about P65–P70 in cat) of the cerebellum.

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References

  • ALTMAN, J. (1972) Postnatal development of the cerebellar cortex in the rat: III: Maturation of the components of the granular layer. Journal of Comparative Neurology 145, 465–514.

    PubMed  Google Scholar 

  • ALTMAN, J. & BAYER, S. A. (1997) Development of the Cerebellar System: Relation to its Evolution, Structure and Functions. Boca Raton-New York-London-Tokyo: CRC Press.

    Google Scholar 

  • AOKI, E., SEMBA, R. & KASHIWAMATA, S. (1986) New candidates for GABAergic neurons in the rat cerebellum: An immunocytochemical study with anti-GABA antibody. Neuroscience Letters 68, 267–271.

    PubMed  Google Scholar 

  • BATTAGLIA, G., ARCELLI, P., GRANATA, T., SELVAGGIO, M., ANDERMANN, F., DUBEAU, F., OLIVIER, A., TAMPIERI, D., VILLEMURE, J. G., AVOLI, M., AVANZINI, G. & SPERAFICO, R. (1996) Neuronal migration disorders and epilepsy: A morphological analysis of three surgically treated patients. Epilepsy Research 26, 49–58.

    PubMed  Google Scholar 

  • BAUDE, A., NUSSER, Z., ROBERTS, J. D. B., MULVIHILL, E., MCILHINNEY, R. A. J. & SOMOGYI, P. (1993) The metabotropic glutamate receptor (mGluR1-alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771–787.

    PubMed  Google Scholar 

  • CHAN-PALAY, V. (1971) The recurrent collaterals of Purkinje cell axons: A correlated study of the rat cerebellar cortex with electron microscopy and the Golgi method. Zeitschrifts fur Anatomie und Entwicklungs-Geschichte 134, 200–234.

    Google Scholar 

  • DIEUDONNÉ, S. & DUMOULIN, A. (2000) Serotonindriven long-range inhibitory connections in the cerebellar cortex. Journal of Neuroscience 20, 1837–1848.

    PubMed  Google Scholar 

  • FOX, C. A. (1959) The intermediate cells of Lugaro in the cerebellar cortex of the monkey. Journal of Comparative Neurology 112, 39–51.

    PubMed  Google Scholar 

  • GABBOTT, P. L. A., SOMOGYI, J., STEWART, M. G. & HÁMORI, J. (1986) GABA-immunoreactive neurons in the rat cerebellum:Alight and electron microscope study. Journal of Comparative Neurology 251, 474–490.

    PubMed  Google Scholar 

  • GEURTS, F. J., TIMMERMANS, J. P., SHIGEMOTO, R. & DE SCHUTTER, E. (2001) Morphological and neurochemical differentiation of large granular layer interneurons in the adult rat cerebellum. Neuroscience 104, 499–512.

    PubMed  Google Scholar 

  • GOLGI, C. (1874) Sulla fina anatomia del cerveletto umano. Lecture, Instituto Lombardo di Scienze e Letteratura, 8 January, 1874. Ch. V. In Opera Omnia, Vol. I: Istologia Normale, 1870–1883, pp. 99–111. Milan: Ulrico Hoepli.

    Google Scholar 

  • GÖRCS, T. J., PENKE, B., BOTI, Z., KATAROVA, Z. & HÁMORI, J. (1993) Immunohistochemical visualization of a metabotropic glutamate receptor. NeuroReport 4, 283–286.

    PubMed  Google Scholar 

  • GUNDERSEN, H. J. G., BENDTSEN, T. F., KORBO, L., MARCUSSEN, N., MOLLER, A., N IELSEN, K., NYENGAARD, J. R., PAKKENBERG, B., SORENSEN, F. B., VESTERBY, A. & WEST, M. J. (1988). Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. (Review). APMIS 96, 379–394.

    PubMed  Google Scholar 

  • HÁMORI, J., TAKÁCS, J. & GÖRCS, T. J. (1996) Immunocytochemical localization of mGluR1? metabotropic glutamate receptor in inhibitory interneurons of the cerebellar cortex. Acta Biologica Hungarica 47, 181–194.

    PubMed  Google Scholar 

  • KISS, J., GÖRCS, T. J., KUHN, R., KNÖPFEL, T, CSÁKY, Á. & HALÁSZ, B. (1996) Distribution of metabotropic glutamate receptor 1a in the rat hypothalamus: An immunocytochemical study using monoclonal andpolyclonal antibody. Acta Biologica Hungarica 47, 221–237.

    PubMed  Google Scholar 

  • KALUS, P., SENITZ, D. & BECKMANN, H. (1997) Cortical layer I changes in schizophrenia: A marker for impaired brain development? Journal of Neural Transmission 104, 549–559.

    PubMed  Google Scholar 

  • LAINÉ, J. & AXELRAD, H. (1996) Morphology of the Golgiimpregnated Lugaro cell in the rat cerebellar cortex: A reappraisal with a description of its axon. Journal of Comparative Neurology 375, 618–640.

    PubMed  Google Scholar 

  • LAINÉ, J., AXELRAD, H. & RABHI, N. (1992) Intermediate cells of Lugaro are present in the immature rat cerebellar cortex at an earlier stage than previously thought. Neuroscience Letters 145, 225–228.

    PubMed  Google Scholar 

  • LARRAMENDI, L. M. H. & LEMKEY-JOHNSTON, N. (1970) The distribution of recurrent collateral synapses in the mouse cerebellar cortex: An electron microscopic study. Journal of Comparative Neurology 138, 451–482.

    PubMed  Google Scholar 

  • LEMKEY-JOHNSTON, N. & LARRAMENDI, L. M. H. (1968) Types and distribution of synapses upon basket and stellate cells of the mouse cerebellum: An electron microscopic study. Journal of Comparative Neurology 134, 73–112.

    PubMed  Google Scholar 

  • LUGARO, E. (1894) Sulle connessioni tra gli elemente nervosi della corteccia cerebellare con considerazioni generali sul significanto fisiologico dei rapporti tra gli elementi nervosi. Rivista Sperimntale di Freniatria 20, 297–331.

    Google Scholar 

  • LURTON, D., YACUBIAN, E. M., SANABRIA, E. G., DA SILVA, A. V., VIANNA, R., GARZON, E., SAKAMOTO, A., SPERAFICO, R. & CAVALHEIRO, E. A. (2002) Immunohistochemical study of six cases of Taylor's type focal cortical dysplasia: Correlation with electroclinical data. Epilepsia 43, 217–219.

    PubMed  Google Scholar 

  • MARTIN, L. J., BLACKSTONE, C. D., HUGANIR, R. L. & PRICE, D. L. (1992) Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron 9, 259–270.

    PubMed  Google Scholar 

  • NACHER, J., CRESPO, C. & MCEWEN, B. C. (2001) Doublecortin expression in the adult rat telencephalon. European Journal of Neuroscience 14, 629–644.

    PubMed  Google Scholar 

  • NAGASAKI, S. & DEURA, S. (1989) Difference in the postnatal development of the layer structures in the phylogenetically different cat cerebellar cortices. Acta Anatomica Nipponica 64, 539–549.

    PubMed  Google Scholar 

  • NÉGYESSY, L., VIDNYÁNSZKY, Z., KUHN, R., KNÖPFEL, T., GÖrcs, T. J. & HÁmori, J. (1997) Light and electron microscopic demonstration of mglur5 metabotropic glutamate receptor immunoreactive neuronal elements in the rat cerebellar cortex. journal of comparative neurology 385, 641–650

    Google Scholar 

  • NUNZI, M. G., SHIGEMOTO, R. & MUGNAINI, E. (2002) Differential expression of calretinin and metabotropic glutamate receptor mGluR1-alpha defines subsets of unipolar brush cells in mouse cerebellum. Journal of Comparative Neurology 451, 189–199.

    PubMed  Google Scholar 

  • OTTERSEN, O. P., STORM-MATHISEN, J. & SOMOGYI, P. (1988) Colocalization of glycine-like and GABA-like immunoreactivities in Golgi cell terminals in the rat cerebellum: Apostembedding light and electron microscopic study. Brain Research 450, 342–353.

    PubMed  Google Scholar 

  • PALAY, S. L. & CHAN-PALAY, V. (1974) Cerebellar Cortex, Cytology and Organization. pp. 133–141. New York: Springer-Verlag.

    Google Scholar 

  • RAMÓN Y CAJAL, S. (1911) Histologie du Systeme Nerveux de l'Homme et des Vertébrés. (Translated by Pasik-P. Vols. I. and II). New York: Springer-Verlag 1999–2000. Madrid: Consejo Superior de Investigaciones Cientificas.

    Google Scholar 

  • ROGERS, J. H. (1989) Immunoreactivity for calretinin and other calcium-binding proteins in cerebellum. Neuroscience 31, 711–721.

    PubMed  Google Scholar 

  • SAHIN, M. & HOCKFIELD, S. (1990) Molecular identification of the Lugaro cell in the cat cerebellar cortex. Journal of Comparative Neurology 301, 575–584.

    PubMed  Google Scholar 

  • SANABRIA, E. R. G., DA SILVA, A. V., SPERAFICO, R. & CAVALHEIRO, E. A. (2002) Damage, reorganization, and abnormal neocortical hyperexcitability in the pilocarpine model of temporal lobe epilepsy. Epilepsia 43, 96–106.

    Google Scholar 

  • TAKÁCS, J. & HÁMORI, J. (1994) Developmental dynamics of Purkinje-cells and of dendritic spines in rat cerebellar cortex. Journal of Neuroscience Research 38, 515–530.

    PubMed  Google Scholar 

  • TAKÁCS, J., HÁMORI, J. & GÖRCS, T. J. (1994) mGluR1? immunoreactivity in Purkinje cells of the developing rat cerebellar cortex. Eur J Neuroscienc Suppl 7, 51.

    Google Scholar 

  • TAKÁCS, J., BOROSTYÁNKÖI, Z. S., VEISENBERGER, E., VIG, J., VASTAGH, C. S., GÖRCS, T. J. & HÁMORI, J. (2000) Postnatal development of unipolar brush cells in the cerebellar cortex of cat. Journal of Neuroscience Research 61, 107–115.

    PubMed  Google Scholar 

  • TAKÁCS, J., MARKOVA, L., BOROSTYÁNKÖI, Z. S., GÖRCS, T. & HÁMORI, J. (1999) Metabotrop glutamate receptor type 1a expressing unipolar brush cells in the cerebellar cortex of different species: A comparative quantitative study. Journal of Neuroscience Research 55, 733–748.

    PubMed  Google Scholar 

  • ULFIG, N., NICKEL, J. & BOHL, J. (1998) Monoclonal antibodies SMI 311 and SMI 312 as tools to investigate the maturation of nerve cells and axonal patterns in human fetal brain. Cell and Tissue Research 291, 433–443.

    PubMed  Google Scholar 

  • WEIBEL, E. R. (1979) Stereological Methods. Vol.1. Practical Methods for Biological Morphometry. London-New York: Academic Press.

    Google Scholar 

  • WRIGHT, D. D., BLACKSTONE, C. D., HUGANIR, R. L. & RYUGO, D. K. (1996) Immunocytochemical localization of the mGluR1a metabotropic glutamate receptor in the dorsal cochlear nucleus. Journal of Comparative Neurology 364, 729–745.

    PubMed  Google Scholar 

  • ZHANG, L. & GOLDMAN, J. E. (1996) Generation of cerebellar interneurons from dividing progenitors in the white matter. Neuron 16, 47–54.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Neurobiology Research Group, United Research Organization of the Hungarian Academy of Sciences and Semmelweis University, Budapest, Hungary

    Julianna Víg, József Takács, Csaba Vastagh & József Hámori

  2. Department of Anatomical Sciences and Neurobiology, School of Medicine, University of Louisville, Louisville, Kentucky, USA

    Zsolt Baldauf

  3. Department of General Zoology and Neurobiology, University of Pécs, Hungary

    Eleonóra Veisenberger

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  1. Julianna Víg
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  2. József Takács
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  6. József Hámori
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Víg, J., Takács, J., Vastagh, C. et al. Distribution of mGluR1α and SMI 311 immunoreactive Lugaro cells in the kitten cerebellum. J Neurocytol 32, 217–227 (2003). https://doi.org/10.1023/B:NEUR.0000010081.54613.94

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