Partial ablation of the neonatal external granular layer disrupts mossy fiber topography in the adult rat cerebellum

Journal of Comparative Neurology

Volumn 371, Issue 4, 1996, Pages 578-588

  Ji, Zhongqi ^a,b   Hawkes, Richard ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b MARYLAND PSYCHIATRIC RESEARCH CENTER   (United States)

Author keywords

granule cell; methylazoxymethanol; Purkinje cell; spinocerebellar; zebrin

Indexed keywords

CELL PROTEIN; METHYLAZOXYMETHANOL; UNCLASSIFIED DRUG; ZEBRIN II;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; GRANULE CELL; MOSSY FIBER; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT; SPINOCEREBELLAR TRACT;

ANIMALS; ANIMALS, NEWBORN; BRAIN MAPPING; CELL COMPARTMENTATION; CELL DIVISION; CEREBELLAR CORTEX; METHYLAZOXYMETHANOL ACETATE; MITOSIS; NERVE ENDINGS; NERVE FIBERS; NERVE TISSUE PROTEINS; PURKINJE CELLS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD;

EID: 0029817329     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960805)371:4<578::AID-CNE7>3.0.CO;2-1     Document Type: Article

References (58)

1. Ahn, A.H., S. Dziennis, R. Hawkes, and K. Herrup (1994) The cloning of zebrin II reveals its identity with aldolase c. Development 120:2081-2090.
2. 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.
3. Altman, J. (1972b) Postnatal development of the cerebellar cortex in the rat. III. Maturation of the components of the granular layer. J. Comp. Neurol. 145:465-514.
4. Arsenio-Nunes, M.L., and C. Sotelo (1985) Development of the spinocerebellar system in the postnatal rat. J. Comp. Neurol. 237:291-306.
5. Arsenio-Nunes, M.L., C. Sotelo, and R. Wehrle (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.
6. Bejar, A., P. Roujansky, J. De Barry, and G. Gombos (1985) Different effect of methylazoxymethanol on mouse cerebellar development depending on the age of injection. Exp. Brain Res. 57:279-285.
7. Brochu, G., L. Maler, and R. Hawkes (1990) Zebrin II: a polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. J. Comp. Neurol. 291:538-552.
8. Chan-Palay, V., S.L. Palay, and J.-Y. Wu (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. U.S.A. 79:4221-4225.
9. Chen, S., and D.E. Hillman (1988) Developmental factors related to abnormal cerebellar foliation induced by methylazoxymethanol acetate (MAM). Dev. Brain Res. 40:201-212.
10. Chen, S., and D.E. Hillman (1993) Compartmentation of the cerebellar cortex by protein kinase C delta. Neuroscience 56:177-188.
11. Chockkan, V., and R. Hawkes (1994) Functional and antigenic maps in the rat cerebellum: zebrin compartmentation and vibrissal receptive fields in lobule IXa. J. Comp. Neurol. 345:33-45.
12. Eisenman, L.M., and L. Arlinghaus (1991) Spinocerebellar projection in the meandertail mutant mouse: organization in the granular posterior lobe and the agranular anterior lobe. Brain Res. 558:149-152.
13. Eisenman, L.M., and R. Hawkes (1990) 5′-nucleotidase and the mabQ113 antigen share a common distribution in the cerebellar cortex of the mouse. Neuroscience 31:231-235.
14. Eisenman, L.M., and R. Hawkes (1993) Antigenic compartmentation in the mouse cerebellar cortex: Zebrin and HNK-1 reveal a complex, overlapping molecular topography. J. Comp. Neurol. 335:586-605.
15. Eisenman, L.M., J.R. Pruett, L. Arlinghaus, and R. Hawkes (1991) Zebrin I expression in the meandertail mutant mouse. Eur. Neurosci. Assoc. Meeting, Cambridge, U.K., p. 278.
16. Garcia-Ladona, F.J., J. de Barry, C. Girard, and G. Gombos (1991) Ectopic granule cell layer in mouse cerebellum after methyl-azoxy-methanol (MAM) treatment. Exp. Brain Res. 86:90-96.
17. Gravel, C., and R. Hawkes (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.
18. Gravel, C., L.M. Eisenman, R. Sasseville, and R. Hawkes (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. 265:294-310.
19. Hawkes, R. (1992) Antigenic markers of cerebellar modules in the adult mouse. Biochem. Soc. Trans. 20:391-395.
20. Hawkes, R., and C. Gravel (1991) The modular cerebellum. Prog. Neurobiol. 36:309-327.
21. Hawkes, R., and N. Leclerc (1987) Antigenic map of the rat cerebellar cortex: the distribution of parasagittal bands as revealed by monoclonal anti-Purkinje cell antibody mabQ113. J. Comp. Neurol. 256:29-41.
22. Hawkes, R., and C. Mascher (1994) The development of molecular compartmentation in the cerebellar cortex. Acta Anat (Basel) 151:139-149.
23. Hawkes, R., and R.W. Turner (1994) Compartmentation of NADPH-diaphorase activity in the mouse cerebellar cortex. J. Comp. Neurol. 346:499-516.
24. Hawkes, R., E. Niday, and J. Gordon (1982) A dot immunobinding assay for monoclonal and other antibodies. Anal. Biochem. 119:142-147.
25. Hawkes, R., M. Colonnier, and N. Leclerc (1985) Monoclonal antibodies reveal sagittal banding in the rodent cerebellar cortex. Brain Res. 333:359-365.
26. Hawkes, R., G. Brochu, L. Doré, C. Gravel, and N. Leclerc (1992) Zebrins: molecular markers of compartmentation in the cerebellum. In R. Llinás and C. Sotelo (eds): The Cerebellum Revisited. New York: Springer-Verlag, pp. 22-55.
27. Hillman, D.E., S. Chen, and V. Chen (1988) Ectopic glial cells in rat cerebella following neonatal administration of methylazoxymethanol acetate. Brain Res. 447:353-359.
28. Ji, Z., and R. Hawkes (1994) Topography of Purkinje cell compartments and mossy fiber terminal fields in lobules II and III of the rat cerebellar cortex: spinocerebellar and cuneocerebellar projections. Neuroscience 61:935-954.
29. Ji, Z., and R. Hawkes (1995) Developing mossy fiber terminal fields in the rat cerebellar cortex may segregate because of Purkinje cell compartmentation and not competition. J. Comp. Neurol. 359:197-212.
30. Ji, Z., J.-E. Aas, J. Laake, F. Walberg, and O.P. Ottersen (1991) An electron microscopic, immunogold analysis of glutamate and glutamine in terminals of rat spinocerebellar fibers. J. Comp. Neurol. 307:296-310.
31. Johnson, M.V., and J.T. Coyle (1982) Cytotoxic lesions and the development of transmitter systems. Trends Neurosci. 5:153-156.
32. Jones, M., M. Yang, and O. Mickelsen (1972) Effects of methylazoxymethanol glucoside and methylazoxymethanol acetate on the cerebellum of the postnatal Swiss albino mouse. Fed. Proc. 31:1508-1511.
33. Lannoo, M.J., G. Brochu, L. Maler, and R. Hawkes (1991) Zebrin II immunoreactivity in the rat and in the weakly electric teleost Eigenmannia (Gymnotiformes) reveals three modes of Purkinje cell development. J. Comp. Neurol. 310:215-233.
34. Leclerc, N., C. Gravel, and R. Hawkes (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.
35. Leclerc, N., G. Schwarting, K. Herrup, R. Hawkes, and M. Yamamoto (1992) Compartmentation in mammalian cerebellum: Zebrin II and P-path antibodies define three classes of sagittally organized bands of Purkinje cells. Proc. Natl. Acad. Sci. U.S.A. 89:5006-5010.
36. Liang, F., and X.S.T. Wan (1989) Improvement of the tetramethyl benzidine reaction with ammonium molybdate as a stabilizer for light and electron microscopic ligand-HRP neurohistochemistry, immunocytochemistry and double-labeling. J. Neurosci. Methods 28:155-162.
37. Marani, E., and J.K. Mai (1992) Expression of the carbohydrate epitope 3-fucosyl-N-acetyl-lactosamine (CD15) in the vertebrate cerebellar cortex. Histochem. J. 24:852-868.
38. 4,3 in the cerebellar external granular layer of the immature rabbit. Histochemistry 78:157-161.
39. Matsushita, M., B. Ragnarson, and G. Grant (1991) Topographic relationship between sagittal Purkinje cell bands revealed by monoclonal antibody to zebrin I and spinocerebellar projections arising from the central cervical nucleus in the rat. Exp. Brain. Res. 84:133-141.
40. Miller, M.W., and R.S. Nowakowski (1988) Use of bromodeoxyuridine-immunocytochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res. 457:44-52.
41. Olucha, F., F. Martinez-Garcia, and C. Lopez-Garcia (1985) A new stabilizing agent for the tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP). J. Neurosci. Methods 13:131-138.
42. Schilling, K., H.H.H.W. Schmidt, and S.L. Bader (1994) Nitric oxide synthase expression reveals compartments of cerebellar granule cells and suggests a role for mossy fibers in their development. Neuroscience 59:893-903.
43. Scott, T.G. (1963) A unique pattern of localization in the cerebellum. Nature 200:793.
44. Seil, F.J., M.L. Johnson, and R. Hawkes (1995) Molecular compartmentation expressed in cerebellar cultures in the absence of neuronal activity and neuron-glia interactions. J. Comp. Neurol. 356:398-407.
45. Sotelo, C. (1987) Cerebellar synaptogenesis and the organization of afferent projection maps. Pontificiae Acad. Scient. Scripta Varia 59:65-90.
46. Sotelo, C., and M. Wassef (1991a) Purkinje cell heterogeneity in four cerebellar mutations revealed by zebrin I expression. Soc. Neurosci. (Abstr.) 17:918.
47. Sotelo, C., and M. Wassef (1991b) Cerebellar development: afferent organization and Purkinje cell heterogeneity. Philos. Trans. R. Soc. Lond. [Biol.] 331:307-313.
48. Takahashi, T., R.S. Nowakowski, and V.S Caviness, Jr. (1992) BUdR as an S-phase marker for quantitative studies of cytokinetic behaviour in the murine cerebral ventricular zone. J. Neurocytol. 21:185-197.
49. Tano, D., J.A. Napieralski, L.M. Eisenman, A. Messer, J. Plummer, and R. Hawkes (1992) Novel developmental boundary in the cerebellum revealed by zebrin expression in the Lurcher (Lc/+) mutant mouse. J. Comp. Neurol. 323:128-136.
50. Tolbert, D.L., T. Pittman, J.M. Alisky, and B.R. Clark (1994) Chronic NMDA receptor blockade or muscimol inhibition of cerebellar cortical neuronal activity alters the development of spinocerebellar afferent topography. Dev. Brain Res. 80:268-274.
51. Vogel, M.W., and J. Prittie (1994) Topographic spinocerebellar mossy fiber projections are maintained in the lurcher mutant. J. Comp. Neurol. 343:341-351.
52. Voogd, J. (1967) Comparative aspects of the structure and fibre connections of the mammalian cerebellum. Prog. Brain Res. 25:94-135.
53. Voogd, J. (1969) The importance of fiber connections in the comparative anatomy of the mammalian cerebellum. In R. Llinás (ed): Neurobiology of Cerebellar Evolution and Development. Chicago: Am. Med. Assoc., pp. 493-514.
54. Voogd, J., N.M. Gerrits, and E. Marani (1985) Cerebellum. In G. Paxinos (ed): The Rat Nervous System. New York: Academic Press, vol. 2, pp. 251-291.
55. Wassef, M., J.P. Zanetta, A. Brehier, and C. Sotelo (1985) Transient biochemical compartmentalization of Purkinje cells during early cerebellar development. Dev. Biol. 111:129-137.
56. Wassef, M., C. Sotelo, M. Thomasset, A.C. Granholm, N. Leclerc, J. Rafrafi, and R. Hawkes (1990) Expression of compartmentation antigen zebrin I in cerebellar transplants. J. Comp. Neurol. 294:223-234.
57. Wassef, M., P. Angaut, L. Arsenio-Nunes, F. Bourrat, and C. Sotelo (1992) Purkinje cell heterogeneity: Its role in organizing the topography of the cerebellar cortex connections. In R. Llinás and C. Sotelo (eds): The Cerebellum Revisited. New York: Springer-Verlag, pp. 5-21.
58. Yan, X.X., L.S. Yen, and L.J. Garey (1993) Parasagittal patches in the granular layer of the developing and adult rat cerebellum as demonstrated by NADPH-diaphorase histochemistry. Neuroreport 4:1227-1230.