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The organization of the corticonuclear and olivocerebellar climbing fiber projections to the rat cerebellar vermis: The congruence of projection zones and the zebrin pattern

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Journal of Neurocytology

Abstract

The zonal organization of the corticonuclear and the olivocerebellar climbing fiber projections to the vermis of the cerebellum of the rat was compared to the pattern of zebrin-positive and zebrin-negative bands in material double-stained for zebrin II and for different anterograde tracers injected in subnuclei of the inferior olive, or retrograde tracers injected in the cerebellar and vestibular target nuclei of the Purkinje cells of the vermis. Projection zones A1, AX, X, B, CX in the vermis and A2 (accessory A zone) and C2 in the hemisphere were defined by their efferent corticonuclear and their afferent climbing fiber connections, and were found to share the same topographical framework with the zebrin pattern.

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References

  • AHN, A. H., DZIENNIS, S., HAWKES, R. & HERRUP, K. (1994) The cloning of zebrin II reveals it identity with aldolase C. Development 120, 2081-2090.

    Google Scholar 

  • AKAIKE, T. (1992) The tectorecipient zone in the inferior olivary nucleus in the rat. Journal of Comparative Neurology 320, 398-414.

    Google Scholar 

  • APPS, R. (1990) Columnar organisation of the inferior olive projection to the posterior lobe of the rat cerebellum. Journal of Comparative Neurology 302, 236-254.

    Google Scholar 

  • APPS, R., TROTT, J. R. & DIETRICHS, E. (1991) A study of branching in the projection from the inferior olive to the x and lateral c1 zones of the cat cerebellum using a combined electrophysiological and retrograde fluorescent double-labelling technique. Experimental Brain Research 87, 141-152.

    Google Scholar 

  • ATKINS, M. J. & APPS, R. (1997) Somatotopical organisation within the climbing fibre projection to paramedian lobule and copula pyramidis of the rat cerebellum. Journal of Comparative Neurology 389, 249-263.

    Google Scholar 

  • AZIZI, S. A. & WOODWARD, D. J. (1987) Inferior olivary nuclear complex of the rat: Morphology and comments on the principles of organization within the olivocerebellar system. Journal of Comparative Neurology 263, 467-484.

    Google Scholar 

  • BOESTEN, A. J. P. & VOOGD, J. (1975) Projections of the dorsal column nuclei and the spinal cord on the inferior olive in the cat. Journal of Comparative Neurology 161, 215-238.

    Google Scholar 

  • BROCHU, G., MAIER, L. & HAWKES, R. (1990) A polypeptide antigen expressed selectively by Purkinje cells reveals compartments in the rat and fish cerebellum. Journal of Comparative Neurology 291, 538-552.

    Google Scholar 

  • BUISSERET-DELMAS, C. (1988a) Sagittal organization of the olivocerebellonuclear pathway in the rat. I. Connections with the nucleus fastigii and the nucleus vestibularis lateralis. Neuroscience Research 5, 475-493.

    Google Scholar 

  • BUISSERET-DELMAS, C. (1988b) Sagittal organization of the olivocerebellonuclear pathway in the rat. II. Connections with the nucleus interpositus. Neuroscience Research 5, 494-512.

    Google Scholar 

  • BUISSERET-DELMAS, C. & ANGAUT, P. (1989) Sagittal organisation of the olivocerebellonuclear pathway in the rat. III. Connections with the nucleus dentatus. Neuroscience Research 72, 131-143.

    Google Scholar 

  • BUISSERET-DELMAS, C. & ANGAUT, P. (1993) The cerebellar olivo-corticonuclear connections in the rat. Progress in Neurobiology 40, 63-87.

    Google Scholar 

  • BUISSERET-DELMAS, C., YATIM, N., BUISSERET, P. & ANGAUT, P. (1993) The X zone and CX subzone of the cerebellum in the rat. Neuroscience Research 16, 95-207.

    Google Scholar 

  • CAMPBELL, N. C. & ARMSTRONG, D. M. (1985) Origin in the medial accessory olive of climbing fibres to the x and lateral c1 zones of the cat cerebellum: A combined electrophysiological/WGA-HRP investigation. Experimental Brain Research 58, 520-531.

    Google Scholar 

  • CHAN-PALAY, V., NILAVER, G. T., PALAY, S. L., BEINFIELD, M. G., ZIMMERMAN, E. A., WU, J.-Y. & O'DONNEHUE, T. L. (1981) Chemical heterogeneity in cerebellar Purkinje cells: Existence and co-existence of glutamic acid decarboxylase-like and motilin-like immunoreactivities. Proceedings of the National Academy of Sciences USA 78, 7787-7791.

    Google Scholar 

  • CHAN-PALAY, V., PALAY, S. L. & WU, J.-Y. (1982a) Sagittal cerebellar microbands of taurine neurons. Immunocytochemical demonstration by using antibodies against the taurine synthesizing enzyme cysteine-sulfinic acid decarboxylase. Proceedings of the National Academy of Sciences USA 221, 4221-4225.

    Google Scholar 

  • CHAN-PALAY, V., LIN, C. T., PALAY, S. L., YAMAMOTO, M. & WU, J.-Y. (1982b) Taurine in the mammalian cerebellum: Demonstration by autoradiography with tritiated taurine and immunohistochemistry with antibodies against taurine synthesizing enzyme, cysteine sulfinic acid decarboxylase. Proceedings of the National Academy of Sciences USA 79, 2695-2699.

    Google Scholar 

  • CHEN, S. & HILLMAN, D. E. (1993). Compartmentation of the cerebellar cortex by protein kinase C delta. Neuroscience 56, 177-188.

    Google Scholar 

  • DEHNES, Y., CHAUDHRY, F. A., ULLENSVANG, K., LEHRE, K. P., STORM-MATHISEN, J. & DANBOLT, N. C. (1998) The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: A glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. Journal of Neuroscience 18, 3606-3619.

    Google Scholar 

  • DUSART, I., MOREL, M. P. & SOTELO, C. (1994) Parasagittal compartmentation of adult rat Purkinje cells expressing the low-affinity nerve growth factor receptor: Changes of pattern expression after a traumatic lesion. Neuroscience 63, 351-356.

    Google Scholar 

  • EKEROT, C.-F. & LARSON, B. (1979) The dorsal spinoolivocerebellar system in the cat. I. Functional organization and termination in anterior lobe. Experimental Brain Research 36, 201-217.

    Google Scholar 

  • EKEROT, C.-F. & LARSON, B. (1982) Branching of olivary axons to innervate pairs of sagittal zones in the cerebellar anterior lobe of the cat. Experimental Brain Research 48, 185-198.

    Google Scholar 

  • GERRITS, N. M., VOOGD, J. & NAS, W. S. C. (1985) Cerebellar and olivary projections of the external and rostral internal cuneate nuclei in the cat. Experimental Brain Research 57, 239-255.

    Google Scholar 

  • GOODMAN, R. R., HALLETT, R. E. & WELCH, R. B. (1963) Patterns of localization in the cerebellar corticonuclear projections of the albino rat. Journal of Comparative Neurology 121, 51-67.

    Google Scholar 

  • GRAVEL, C., EISENMAN, L., SASSEVILLE, R. & 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. Journal of Comparative Neurology 265, 294-310.

    Google Scholar 

  • GWYN, D. G., NICHOLSON, G. P. & FLUMERFELT, B. A. (1977) The inferior olivary nucleus of the rat: A light and electromicroscopic study. Journal of Comparative Neurology 174, 489-520.

    Google Scholar 

  • HAINES, D. E., PATRICK, G. W. & SATRULEE, P. (1982) Organization of cerebellar corticonuclear fiber systems. In The Cerebellum New Vistas (edited by PALAY, S. L. & CHAN-PALAY, V.) pp. 320-371. Berlin: Springer.

    Google Scholar 

  • HAWKES, R. & LECLERC, N. (1987) Antigenic map of the rat cerebellar cortex: The distribution of parasagittal bands as revealed by monoclonal anti-Purkinje cell antibody mabQ113. Journal of Comparative Neurology 256, 29-41.

    Google Scholar 

  • HAWKES, R. & LECLERC, N. (1989) Purkinje cell axonal distributions reflect the chemical compartmentation of the rat cerebellar cortex. Brain Research 476, 279-290.

    Google Scholar 

  • HAWKES, R. & EISENMAN, L. M. (1997). Stripes and zones: The origins of regionalization of the adult cerebellum. Perspectives in Developmental Biology 5, 95-105.

    Google Scholar 

  • JÖRNTELL, H., EKEROT, C.-F., GARWICZ, M. & LUO, X-L. (2000) Funtional organization of climbing fibre projection to the cerebellar anterior lobe of the rat. Journal of Physilogy (London) 522, 297-309.

    Google Scholar 

  • LEMANN, W., SAPER, C. B., RYE, D. B. & WAINER, B. M. (1985) Stabilization of TMB reaction product for electronmicroscopic retrograde and anterograde fiber tracing. Brain Research Bulletin 14, 277-281.

    Google Scholar 

  • MARANI, E., VOOGD, J. & BOEKEE, A. (1977) Acetylcholinesterase staining in subdivisions of the cat's inferior olive. Journal of Comparative Neurology 174, 209-226.

    Google Scholar 

  • MARANI, E. (1982) Topographical enzyme histochemistry of the mammalian cerebellum. 5′-Nucleotidase and acetylcholinesterase. Thesis Leiden.

  • MATEOS, J. M., OSORIO, A., AZUKUE, J. J., BENITEX, R., ELESGARAI, I., BILBAO, A., DIEZ, J., PUENTE, N., KUHN, R., KNOPFEL, T., HAWKES, R., DONATE-OLVER, F. & GRANDES, P. (2001) Parasagittal compartmentalization of the metabotropic glutamate receptor mGluR1b in the cerebellar cortex. European Journal of Anatomy 5, 15-21.

    Google Scholar 

  • PALAY, S. L. (1967) Principles of cellular organization in the nervous ststem. In The Neurosciences. A Study Program (edited by QUARTON, C. C., MELNECHUK, TH & SCHMITT, F. O.) pp. 25-31. New York: Rockefeller University Press.

    Google Scholar 

  • PALAY, S. L. (1982) Current status of neuroanatomical research in the cerebellum. In The Cerebellum New Vistas (edited by PALAY, S. L. & CHAN-PALAY, V.) pp. 1-7. Berlin: Springer.

    Google Scholar 

  • PARDOE, J. & APPS, R. (2002) Structure-function relations of two somatotopically corresponding regions of the rat cerebellar cortex: Olivo-cortico-nuclear connections. Cerebellum 1, 165-185.

    Google Scholar 

  • RUIGROK, T. J. H. & VOOGD, J. (1990) Cerebellar nucleoolivary projections in rat. An anterograde tracing study with Phaseolus vulgaris-leucoagglutinin (PHA-L). Journal of Comparative Neurology 298, 315-333.

    Google Scholar 

  • RUIGROK, T. J. H. & VOOGD, J. (2000) Organization of projections from the inferior olive to the cerebellar nuclei in the rat. Journal of Comparative Neurology 426, 209-228.

    Google Scholar 

  • RUIGROK, T. J. H., TEUNE, T. M., VAN DER BURG, J. & SABEL-GOEDKNEGT, H. (1995) Anteograde double labeling technique for light microscopy. A combination of axonal transport of cholera toxin B-subunit and a gold-lectin conjugate. Journal of Neuroscience Methods 61, 127-138.

    Google Scholar 

  • SARNA, J., MIRANDA, S. R. P., SCHUCHMAN, E. H., & HAWKES, R. (2001) Patterned cerebellar Purkinje cell death in a transgenic model of Niemann Pick Type A/B disease. European Journal of Neuroscience 13, 1873-1880.

    Google Scholar 

  • SCOTT, T. G. (1964) A unique pattern of localization within the cerebellum of the mouse. Journal of Comparative Neurology 122, 1-8.

    Google Scholar 

  • SUGIHARA, I., WU, H.-S. & SHINODA, Y. (1999) Morphology of single olivocerebellar axons labeled with biotinylated dextran amine in the rat. Journal of Comparative Neurology 414, 131-148.

    Google Scholar 

  • TEUNE, T. M., VAN DER BURG, J., VAN DER MOER, J., VOOGD, J. & RUIGROK, T. J. H. (2000) Topography of cerebellar nuclear projections to the brain stem in the rat. In Cerebellar Modules: Molecules, Morphology and Function (edited by GERRITS, N. M., RUIGROK, T. J. H. & DE ZEEUW, C. I.) pp. 141-172. Amsterdam: Elsevier.

    Google Scholar 

  • TROTT, J. R. & ARMSTRONG, D. M. (1987a) The cerebellar cortioconuclear projection from lobule Vb/c of the cat anterior lobe: A combined electrophysiological and autoradiographic study. I. Projections from the intermediate region. Experimental Brain Research 66, 318-338.

    Google Scholar 

  • TROTT, J. R. & ARMSTRONG, D. M. (1987b) The cerebellar cortioconuclear projection from lobule Vb/c of the cat anterior lobe: A combined electrophysiological and autoradiographic study. II. Projections from the vermis. Experimental Brain Research 66, 339-354.

    Google Scholar 

  • TROTT, J. R. & APPS, R. (1991) Lateral and medial subdivisions within the olivocerebellar zones of the paravermal cortex in lobule Vb/c of the cat anterior lobe. Experimental Brain Research 87, 126-140.

    Google Scholar 

  • VOOGD, J. & BIGARÉ, F. (1980) Topographical distribution of olivary and cortico-nuclear fibres in the cerebellum: A review. In The Olivary Nucleus. Anatomy and Physiology (edited by DE MONTIGNY, C. & COURVILLE, J.) pp. 207-234. New York: Raven Press.

    Google Scholar 

  • VOOGD, J. & RUIGROK, T. J. H. (1997) Transverse and longitudinal patterns in the mammalian cerebellum. Progress in Brain Research 114, 21-37.

    Google Scholar 

  • VOOGD, J., EISENMAN, L. M & RUIGROK, T. J. H (1993) Relation of olivocerebellar projection zones to zebrin pattern in rat cerebellum. Society of Neuroscience Abstracts 19, 1216

    Google Scholar 

  • VOOGD, J., JAARSMA, D. & MARANI, E. (1996a) The cerebellum, chemoarchitecture, and anatomy. In Handbook of Chemical Neuroanatomy. Vol.12, Integrated Systems of the CNS, Part III Cerebellum, Basal Ganglia, Alfactory System (edited by SWANSON, L. W., BJÖRKLUND, A. & HÖKFELT, T.) pp. 1-369. Amsterdam: Elsevier.

    Google Scholar 

  • VOOGD, J., GERRITS, N. M. & RUIGROK T. J. H. (1996b) Organization of the vestibulocerebellum. Annals of the New York Academy of Sciences 781, 553-579.

    Google Scholar 

  • VOOGD, J., NIEUWENHUYS, R., VAN DONGEN, P. A. M. & TEN DONKELAAR, H. J. (1998) Mammals. In The Central Nervous System of Vertebrates (edited by NIEUWENHUYS, R., TEN DONKELAAR, H. J. & NICHOLSON, C.) pp 1637-2097. Berlin: Springer.

    Google Scholar 

  • VOOGD, J., PARDOE, J., RUIGROK, T. J. H. & APPS, R. (2003a) The distribution of climbing and mossy fibre collateral branches from the copula pyramidis and the paramedian lobule. Congruence of climbing fibre cortical zones and the pattern of zebrin banding within the rat cerebellum. Journal of Neuroscience 23, 4645-4656.

    Google Scholar 

  • VOOGD, J., PARDOE, J., RUIGROK, T. J. H. & APPS, R. (2003b) The distribution of climbing and mossy fibre collateral branches from the copula pyramidis and the paramedian lobule. Congruence of climbing fibre cortical zones and the pattern of zebrin banding within the rat cerebellum. Website http://www.ErasmusMC.nl/voogd-cfcollaterals.

  • WASSEF, M., ANGAUT, P., ARSENIO-NUNES, L., BOURRAT, F. & SOTELO, C. (1992) Purkinje cell heterogeneity: Its role in organizing the topography of the cerebellar cortex connections. In The Cerebellum Revisited (edited by LLINAS, R. & SOTELO, C.) pp. 5-21. Heidelberg: Springer Verlag.

    Google Scholar 

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Voogd, J., Ruigrok, T.J.H. The organization of the corticonuclear and olivocerebellar climbing fiber projections to the rat cerebellar vermis: The congruence of projection zones and the zebrin pattern. J Neurocytol 33, 5–21 (2004). https://doi.org/10.1023/B:NEUR.0000029645.72074.2b

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