Postnatal development and adult organisation of the olivocerebellar projection map in the hypogranular cerebellum of the rat

Journal of Comparative Neurology

Volumn 407, Issue 4, 1999, Pages 527-542

  Zagrebelsky, Marta ^a   Rossi, Ferdinando ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Calcitonin gene related peptide; Methylazoxymethanol acetate; Multiple climbing fibre innervation; Olivocerebellar topography; Synapse elimination; Zebrin II Purkinje cell bands

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL DEGENERATION; CLIMBING FIBER; CONTROLLED STUDY; GRANULE CELL; NERVE CELL PLASTICITY; NERVE PROJECTION; NONHUMAN; OLIVARY NUCLEUS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PURKINJE CELL; RAT; SYNAPSE; TOPOGRAPHY;

AGING; ANIMALS; ANIMALS, NEWBORN; BRAIN MAPPING; CALCITONIN GENE-RELATED PEPTIDE; CEREBELLUM; METHYLAZOXYMETHANOL ACETATE; NERVE FIBERS; NERVE TISSUE PROTEINS; OLIVARY NUCLEUS; PROTEIN SYNTHESIS INHIBITORS; PURKINJE CELLS; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION;

EID: 0033577722     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990517)407:4<527::AID-CNE5>3.0.CO;2-H     Document Type: Article

References (76)

1. Armstrong DM. 1974. Functional significance of connections of the inferior olive. Physiol Rev 54:358-417.
2. Bejar A, Roujansky P, de Barry J, Combos G. 1985. Different effect of methylazoxymethanol on mouse development depending on the age of injection. Exp Brain Res 57:279-285.
3. Benoit P, Mariani J, Delhaye-Bouchaud N, Chapuis G. 1987. Evidence for a multiple innervation of cerebellar Purkinje cells by climbing fibres in adult ferrets infected by a mink enteritis virus. Dev Brain Res 34:51-57.
4. Blatt GJ, Eisenman LM. 1993. The olivocerebellar projection in normal (+/+), heterozygous weaver (wv/+) and homozygous weaver (wv/wv) mutant mice: comparison of terminal pattern and topographic organisation. Exp Brain Res 95:187-201.
5. Bravin M, Rossi F, Strata P. 1995. Different climbing fibres innervate separate dendritic regions of the same Purkinje cell in hypogranular cerebellum. J Comp Neurol 357:395-407.
6. Brochu G, Maler L, 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.
7. Changeux JP, Danchin A. 1976. Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264:705-712.
8. Chédotal A, Sotelo C. 1992. Early development of the olivocerebellar projection in the foetal rat using CGRP immunocytochemistry. Eur J Neurosci 4:1159-1179.
9. Chédotal A, Pourquié O, Ezan F, San Clemente H, Sotelo C. 1996. BEN as a presumptive target recognition molecule during the development of the olivocerebellar system. J Neurosci 16:3296-3310.
10. Chédotal A, Bloch-Gallego E, Sotelo C. 1997. The embryonic cerebellum contains topographic cues that guide developing inferior olivary axons. Development 124:861-870.
11. Chen S, Hillman DE. 1988. Developmental factors related to abnormal cerebellar foliation induced by methylazoxymethanol acetate (MAM). Dev Brain Res 40:201-212.
12. Crepel F. 1982. Regression of functional synapses in the immature mammalian cerebellum. Trends Neurosci 5:266-269.
13. Crepel F, Delhaye-Bouchaud N. 1979. Distribution of climbing fibres on cerebellar Purkinje cells in X-irradiated rats. An electrophysiological study. J Physiol 290:97-112.
14. Crepel F, Mariani J. 1976. Multiple innervation of Purkinje cells by climbing fibres in the cerebellum of the weaver mutant mouse. J Neurobiol 7:579-582.
15. Crepel F, Mariani J, Delhaye-Bouchaud N. 1976. Evidence for a multiple innervation of Purkinje cells by climbing fibres in the immature rat cerebellum. J Neurobiol 7:567-578.
16. Crepel F, Delhaye-Bouchaud N, Guastavino JM, Sampaio I. 1980. Multiple innervation of cerebellar Purkinje cells by climbing fibres in Staggerer mutant mouse. Nature 183:483-484.
17. Eccles JC, Ito M, Szentágothái J. 1967. The cerebellum as a neuronal machine. Berlin: Springer-Verlag.
18. Ekerot C-F, Larson B. 1982. Branching of olivary axons to innervate pairs of sagittal zones in the cerebellar anterior lobe of the cat. Exp Brain Res 48:185-198.
19. Forehand CJ, Purves D. 1984. Regional innervation of rabbit ciliary ganglion cells by the terminals of preganglionic axons. J Neurosci 4:1-12.
20. Frank E, Jansen JKS, Lømo T, Westgaard RH. 1975. The interaction between foreign and original motor nerves innervating the soleus muscle of rats. J Physiol 247:725-743.
21. Fuhrman Y, Thompson MA, Piat G, Mariani J, Delhaye-Bouchaud N. 1994. Enlargement of olivo-cerebellar microzones in the agranular cerebellum of adult rats. Brain Res 638:277-284.
22. Gan W-B, Lichtman JW. 1998. Synaptic segregation at the developing neuromuscular junction. Science 282:1508-1511.
23. Goodman CS, Shatz CJ. 1993. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72/ Neuron 10 (Suppl):77-98.
24. Gravel C, Eisenmann LM, Sasseville R, Hawkes R. 1987. Parasagittal organisation of the rat cerebellar cortex: direct correlation between antigenic Purkinje cell bands revealed by mabQ113 and the organisation of the olivocerebellar projection. J Comp Neurol 265:295-310.
25. Grinnell AD, Letinsky MS, Rheuben MB. 1979. Competitive interaction between foreign nerves innervating frog skeletal muscle. J Physiol 289:241-262.
26. Hawkes R. 1997. An anatomical model of cerebellar modules. In: de Zeeuw CI, Strata P, Voogd J, editors. The cerebellum: from structure to control. Prog Brain Res Vol 114. Amsterdam: Elsevier, p 39-52.
27. Hawkes R, Brochu G, Doré L, Gravel C, Leclerc N. 1992. Zebrins: molecular markers of compartmentation in the cerebellum. In: Llinás R, Sotelo C, editors. The cerebellum revisited. New York: Springer-Verlag, p 22-55.
28. Herrup K, Kuemerle B. 1997. The compartmentalization of the cerebellum. Annu Rev Neurosci 20:61-90.
29. Hillman DE, Chen S, Ackman J. 1988. Perinatal methylazoxymethanol acetate uncouples coincidence of orientation of cerebellar folia and parallel fibres. Neuroscience 24:99-110.
30. Hume RI, Purves D. 1981. Geometry of neonatal neurones and the regulation of synapse elimination. Nature 293:469-471.
31. Ji Z, Hawkes R. 1996. Partial ablation of the neonatal external granular layer disrupts mossy fibre topography in the adult rat cerebellum. J Comp Neurol 371:578-588.
32. Kakizawa S, Watanabe M, Inoue Y, Kano M. 1998. Neural activity is required for climbing fiber synapse elimination in developing cerebellum. Soc Neurosci Abstr 24:1039.
33. Kano M, Hashimoto K, Chen C, Abeliovich A, Kurihara H, Wanatabe M, Inoue Y, Tonegawa S. 1995. Impaired synapse elimination during cerebellar development in PKCγ mutant mice. Cell 83:1223-1232.
34. Kano M, Hashimoto K, Kurihara H, Wanatabe M, Inoue Y, Aiba A, Tonegawa S. 1997. Persistent multiple climbing fibre innervation of cerebellar Purkinje cells in mice lacking mGluR1. Neuron 18:71-79.
35. Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y, Aizawa S, Mishina M. 1995. Impairment of motor coordination, Purkinje cell synapse formation and cerebellar long-term depression in GluRδ2 mutant mice. Cell 81:245-252.
36. Kubota Y, Inagaki S, Shimada S, Kito S, Zaidi M, Girgis SI, MacIntyre I, Tohyama M. 1987. Transient appearance of the calcitonin gene-related peptide-like immunoreactive fibres in the developing cerebellum of the rat. Brain Res 415:385-388.
37. Kuffler DP, Thompson W, Jansen JKS. 1977. The elimination of synapses in multiply innervated skeletal muscle fibres of the rat: Dependence of distance between end-plates. Brain Res 138:353-358.
38. Leclerc N, Gravel C, Hawkes R. 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.
39. Levenes C, Daniel H, Jaillard D, Conquet F, Crepel F. 1997. Incomplete regression of multiple climbing fibre innervation of cerebellar Purkinje cells in mGluR1 mutant mice. Neuroreport 8:571-574.
40. Lovell KL, Goetting MG, Jones MZ. 1980. Regeneration in the cerebellum following Methylazoxymethanol-induced destruction of the external germinal layer. Morphological and biochemical studies. Dev Neurosci 3:128-139.
41. Mariani J, Delhaye-Bouchaud N. 1987. Elimination of functional synapses during development of the nervous system. News Physiol Sci 2:93-97.
42. Mariani J, Crepel F, Geoffroy B, Delhaye-Bouchaud N. 1977. Anatomical, physiological and biochemical studies of the cerebellum from reeler mutant mice. Philos Trans R Soc Lond (Biol) 281:93-97.
43. Mariani J, Mulle C, Geoffroy B, Delhaye-Bouchaud N. 1987. Peripheral maps and synapse elimination in the cerebellum of the rat. II. Representation of peripheral inputs through the climbing fiber pathway in the posterior vermis of X-irradiated adult rats. Brain Res 421:211-225.
44. Mariani J, Benoit P, Hoang DM, Thompson M, Delhaye-Bouchaud N. 1990. Extent of multiple innervation of cerebellar Purkinje cells by climbing fibres in adult X-irradiated rats. Comparison of different schedules of irradiation during the first postnatal week. Dev Brain Res 57:63-70.
45. Mason CA, Christakos S, Catalano SM. 1990. Early climbing fiber interactions with Purkinje cells in the postnatal mouse cerebellum. J Comp Neurol 297:77-90.
46. Millen KJ, Hui C-C, Joyner AL. 1995. A role for En-2 and other murine homologues of Drosophila segment polarity genes in regulating positional information in the developing cerebellum. Development 121:3935-3945.
47. Morara S, Provini L, Rosina A. 1989. CGRP expression in the rat olivocerebellar system during postnatal development. Brain Res 504:315-319.
48. Oberdick J, Baader SL, Schilling K. 1998. From zebra stripes to postal zones: deciphering patterns of gene expression in the cerebellum. Trends Neurosci 21:383-390.
49. Oberdick J, Schilling K, Smeyme RJ, Corbin JG, Bocchiaro C, Morgan JI. 1993. Control of segment-like expression patterns of gene expression in the mouse cerebellum. Neuron 10:1007-1018.
50. Paradies MA, Eisenman LM. 1993. Evidence of early topographic organisation in the embryonic olivocerebellar projection: a model system for the study of pattern formation processes in the central nervous system. Dev Dynam 197:125-145.
51. Paradies MA, Grishkat H, Smeyne RJ, Oberdick J, Morgan JI, Eisenman LM. 1996. Correspondence between L7-lacZ-expressing Purkinje cells and labeled olivocerebellar fibers during late embryogenesis in the mouse. J Comp Neurol 374:451-466.
52. Puro DG, Woodward DJ. 1978. Physiological properties of afferents and synaptic reorganisation in the rat cerebellum degranulated by postnatal X-irradiation. J Neurobiol 9:195-215.
53. Purves D, Litchman J. 1985. Principles of neural development. Sunderland: Sinauer.
54. Rabacchi S, Bailly Y, Delhaye-Bouchaud N, Mariani J. 1992a. Involvement of N-methyl-D-aspartate (NMDA) receptor in synapse elimination during cerebellar development. Science 256:1823-1825.
55. Rabacchi S, Bailly Y, Delhaye-Bouchaud N, Herrup K, Mariani J. 1992b. Role of target in synapse elimination: studies in cerebellum of developing Lurcher mutants and adult chimeric mice. J Neurosci 12:4712-4720.
56. Ramón y Cajal S. 1911. Histologie du système nerveux de l'homme et des vertébrés. Paris: Maloine.
57. Robertson LT. 1987. Organisation of climbing fiber representation in the anterior lobe. In: King JS, editor. New concepts in cerebellar neurobiology. New York: Alan R. Liss. p 281-320.
58. Rossi F, Strata P. 1995. Reciprocal trophic interactions in the adult climbing fibre-Purkinje cell system. Prog Neurobiol 47:341-369.
59. Seil FJ, Johnson ML, Hawkes R. 1995. Molecular compartmentation expressed in cerebellar cultures in the absence of neuronal activity and neuron-glia interactions. J Comp Neurol 356:398-407.
60. Shambes GM, Gibson JM, Welker W. 1978. Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. Brain Behav Evol 15:94-140.
61. Sotelo C, Bourrat F, Triller A. 1984. Postnatal development of the inferior olivary complex in the rat: II. Topographic organisation of the immature olivocerebellar projection. J Comp Neurol 222:177-199.
62. Strata P, Rossi F. 1998. Plasticity of the olivocerebellar pathway. Trends Neurosci 21:407-413.
63. Voogd J, Ruigrok TJH. 1997. Transverse and longitudinal patterns in the mammalian cerebellum. In: de Zeeuw CI, Strata P, Voogd J, editors. The cerebellum: from structure to control. Prog Brain Res Vol 114. Amsterdam: Elsevier, p 21-38.
64. Voogd J, Gerrits N, Marani E. 1985. Cerebellum. In: Paxinos G, editor. The rat nervous system, vol 2. New York: Academic Press, p 251-292.
65. Wassef M, 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.
66. Wassef M, Zanetta JP, Brehier A, Sotelo C. 1985. Transient biochemical compartmentalisation of Purkinje cells during early cerebellar development. Dev Biol 111:129-137.
67. Wassef M, Sotelo C, Thomasset M, Granholm A-C, Leclerc N, Rafrafi J, Hawkes R. 1990. Expression of compartmentation antigen zebrin I in cerebellar transplants. J Comp Neurol 294:223-234.
68. Wassef M, Angaut P, Arsenio-Nunes L, Bourrat F, Sotelo C. 1992a. Purkinje cell heterogeneity: its role in organising the cerebellar cortex connections. In: Llinás R, Sotelo C, editors. The cerebellum revisited. New York: Springer-Verlag, p 5-21.
69. Wassef M, Chédotal A, Cholley B, Thomasset M, Heizmann CW, Sotelo C. 1992b. Development of the olivocerebellar projection in the rat: I transient biochemical compartmentation of the inferior olive. J Comp Neurol 323:519-536.
70. Wassef M, Cholley B, Heizmann CW, Sotelo C. 1992c. Development of the olivocerebellar projection in the rat: II Matching of the developmental compartmentation of the cerebellum and inferior olive through the projection map. J Comp Neurol 323:537-550.
71. Welker W. 1987. Spatial organisation of somatosensory projections to granule cell cerebellar cortex: functional and connectional implications of fractured somatotopy. In: King JS, editor. New concepts in cerebellar neurobiology. New York: Alan R. Liss. p 239-280.
72. Woodward DJ, Hoffer BJ, Altman J. 1974. Physiological and pharmacological properties of Purkinje cells in rat cerebellum degranulated by postnatal X-irradiation. J Neurobiol 5:283-304.
73. Woodward DJ, Bickett D, Chanda R. 1975. Purkinje cell dendritic alterations after transient developmental injury of the external granular layer. Brain Res 97:195-214.
74. Zagrebelsky M, Rossi F, Hawkes R, Strata P. 1996. Topographically arranged climbing fibre sprouting in the adult rat cerebellum. Eur J Neurosci 8:1051-1054.
75. Zagrebelsky M, Strata P, Rossi F. 1997a. Topographical organisation of the olivocerebellar projection in the hypogranular rat cerebellum. Soc Neurosci Abstr 23:1676.
76. Zagrebelsky M, Strata P, Hawkes R, Rossi F. 1997b. reestablishment of the olivocerebellar projection map by compensatory transcommissural reinnervation following unilateral transection of the inferior cerebellar peduncle in the newborn rat. J Comp Neurol 379:283-299.