Ultrastructural analysis of climbing fiber-purkinje cell synaptogenesis in the rat cerebellum

Neuroscience

Volumn 108, Issue 4, 2001, Pages 655-671

  Morara, S ^a   Van Der Want, J J L ^b   De Weerd, H ^b   Provinp, L ^a,c   Rosina, A ^a  

^a CNR   (Italy)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

CGRP; Electron microscopy; Immunocytochemistry; NPY; Olivocerebellar system; Purkinje cell

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; NEUROPEPTIDE Y;

ANIMAL; ARTICLE; CEREBELLUM; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; IMMUNOELECTRON MICROSCOPY; NERVE TRACT; OLIVARY NUCLEUS; PHYSIOLOGY; PURKINJE CELL; RAT; RAT STRAIN; SYNAPSE; ULTRASTRUCTURE;

ANIMAL; CALCITONIN GENE-RELATED PEPTIDE; CEREBELLUM; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; NEURAL PATHWAYS; NEUROPEPTIDE Y; OLIVARY NUCLEUS; PURKINJE CELLS; RATS; RATS, WISTAR; SUPPORT, NON-U.S. GOV'T; SYNAPSES;

EID: 0035226499     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(01)00433-X     Document Type: Article

References (66)

1. Altman, J., 1972. Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J. Comp. Neurol. 145, 399-464.
2. Altman, J., 1982. Morphological development of the rat cerebellum and some of its mechanisms. In: Palay, S.L., Chan-Palay, V. (Eds.), The Cerebellum - New Vistas. Springer-Verlag, New York, pp. 8-46.
3. Armengol, J.A., Sotelo, C., 1991. Early dendritic development of Purkinje cells in the rat cerebellum. A light and electron microscopic study using axonal tracing in 'in vitro' slices. Dev. Brain Res. 64, 95-114.
4. Ashwell, K.W., Zhang, L.L., 1992. Ontogeny of afferents to the fetal rat cerebellum. Acta Anat. 145, 17-23.
5. Bishop, G.A., Ho, R.H., King, J.S., 1985. An immunohistochemical study of serotonin development in the opossum cerebellum. Anat. Embryol. 171, 325-338.
6. Blanchette-Mackie, E.J., Scow, R.O., 1981. Lipolysis and lamellar structures in white adipose tissue of young rats: lipid movement in membranes. J. Ultrastruct. Res. 77, 295-318.
7. Blanchette-Mackie, E.J., Scow, R.O., 1983. Movement of lipolytic products to mitochondria in brown adipose tissue of young rats: an electron microscope study. J. Lipid Res. 24, 229-244.
8. Bourrat, F., Sotelo, C., 1984. Postnatal development of the inferior olivary complex in the rat. III. A morphometric analysis of volumetric growth and neuronal cell number. Dev. Brain Res. 16, 241-251.
9. Bradley, P., Berry, M., 1976. The effects of reduced climbing and parallel fibre input on Purkinje cell dendritic growth. Brain Res. 109, 133-151.
10. Chedotal, A., Sotelo, C., 1992. Early development of olivocerebellar projections in the fetal rat using CGRP immunocytochemistry. Eur. J. Neurosci. 4, 1159-1179.
11. Chedotal, A., Sotelo, C., 1993. The 'creeper stage' in cerebellar climbing fiber synaptogenesis precedes the 'pericellular nest' - ultrastructural evidence with parvalbumin immunocytochemistry. Dev. Brain Res. 76, 207-220.
12. Crepel, F., Delhaye-Bouchaud, N., Dupont, J.L., 1981. Fate of the multiple innervation of cerebellar Purkinje cells by climbing fibers in immature control, X-irradiated and hypothyroid rats. Dev. Brain Res. 1, 59-71.
13. Crepel, F., Mariani, J., Delhaye-Bouchaud, N., 1976. Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J. Neurobiol. 7, 567-578.
14. Cummings, S.L., Scott Young, W., III, King, J.S., 1994. Early development of cerebellar afferent systems that contain corticotropin-releasing factor. J. Comp. Neurol. 350, 534-549.
15. Del Cerro, M.P., Snider, R.S., 1968. Studies on the developing cerebellum. Ultrastructure of the growth cones. J. Comp. Neurol. 133, 341-362.
16. Delhaye-Bouchaud, N., Geoffroy, B., Mariani, J., 1985. Neuronal death and synapse elimination in the olivocerebellar system. I. Cell counts in the inferior olive of developing rats. J. Comp. Neurol. 232, 299-308.
17. Denis-Donini, S., 1989. Expression of dopaminergic phenotype in the mouse olfactory bulb induced by the calcitonin-gene related peptide. Nature 339, 701-703.
18. Desclin, J.C., Colin, F., 1980. The olivocerebellar system. II. Some ultrastructural correlates of inferior olive destruction in the rat. Brain Res. 187, 29-46.
19. Fontaine, B., Klarsfeld, A., Changeux, J.-P., 1987. Calcitonin gene-related peptide and muscle activity regulate acetylcholine receptor α-subunit mRNA levels by distinct intracellular pathways. J. Cell Biol. 105, 1337-1342.
20. Ha, B.K., Bishop, G.A., King, J.S., Burry, R.W., 2000. Corticotropin releasing factor induces proliferation of cerebellar astrocytes. J. Neurosci. Res. 62, 789-798.
21. Haas, C.A., Reddington, M., Kreutzberg, G.W., 1991. Calcitonin gene-related peptide stimulates the induction of c-fos gene expression in rat astrocyte cultures. Eur. J. Neurosci. 3, 708-712.
22. Hámori, J., 1969. Development of synaptic organization in the partially agranular and in the transneuronally atrophied cerebellar cortex. In: Llinàs, R. (Ed.), Neurobiology of Cerebellar Evolution and Development. AMA/ERF, Chicago, IL, pp. 845-858.
23. Higashi, Y., Murayama, S., Pentchev, P.G., Suzuki, K., 1995. Peripheral nerve pathology in Niemann-Pick type C mouse. Acta Neuropathol. 90, 158-163.
24. Hildebrand, C., Bowe, C.M., Nilsson Remahl, I., 1994. Myelination and myelin sheath remodelling in normal and pathological PNS nerve fibers. Prog. Neurobiol. 43, 85-141.
25. Iversen, L.L., 1995. Neuropeptides: promise unfulfilled? Trends Neurosci. 18, 49-50.
26. Kawaguchi, S., Yamamoto, T., Mizuno, N., Iwahori, N., 1975. The role of climbing fibers in the development of the Purkinje cell dendrites. Neurosci. Lett. 1, 301-304.
27. Kornguth, S.E., Scott, G., 1972. The role of climbing fibers in the formation of Purkinje cell dendrites. J. Comp. Neurol. 146, 61-82.
28. Kubota, Y., Inagaki, S., Shimada, S., Kito, S., Zaidi, M., Girgis, S.I., MacIntyre, I., Tohyama, M., 1987. Transient appearance of calcitonin gene-related peptide-like immunoreactive fibers in the developing cerebellum of the rat. Brain Res. 415, 385-388.
29. Larramendi, L.M.H., 1969. Analysis of synaptogenesis in the cerebellum of the mouse. In: Llinàs, R. (Ed.), Neurobiology of Cerebellar Evolution and Development. AMA/ERF, Chicago, IL, pp. 803-843.
30. Larramendi, L.M.H., Victor, T., 1967. Synapses on the Purkinje cell spines in the mouse. An electron microscopic study. Brain Res. 5, 15-30.
31. Lazar, P., Reddington, M., Streit, W., Raivich, G., Kreutzberg, G.W., 1991. The action of calcitonin gene-related peptide on astrocyte morphology and cyclic AMP accumulation in astrocyte cultures from neonatal rat brain. Neurosci. Lett. 130, 99-102.
32. Maley, B.E., 1990. Ultrastructural identification of neuropeptides in the central nervous system. J. Electron Microsc. Tech. 15, 67-80.
33. Martin, G.F., Culberson, J.L., Hazlett, J.C., 1983. Observations on the early development of ascending spinal pathways. Studies using the North American opossum. Anat. Embryol. 166, 191-207.
34. Mason, C.A., 1986. Axon development in mouse cerebellum: embryonic axon forms and expression of synapsin I. Neuroscience 19, 1319-1333.
35. Mason, C.A., Christakos, S., Catalano, S.M., 1990. Early climbing fiber interactions with Purkinje cells in the postnatal mouse cerebellum. J. Comp. Neurol. 297, 77-90.
36. Mason, C.A., Gregory, E., 1984. Postnatal maturation of cerebellar mossy and climbing fibers: transient expression of dual features on single axons. J. Neurosci. 4, 1715-1735.
37. Meller, K., Glees, P., 1969. The development of the mouse cerebellum. A Golgi and electron microscopical study. In: Llinàs, R. (Ed.), Neurobiology of Cerebellar Evolution and Development. AMA/ERF, Chicago, IL, pp. 783-801.
38. Morara, S., Marcotti, W., Provini, L., Rosina, A., 1997. Neuropeptide Y (NPY) expression is up-regulated in the rat inferior olive during development. NeuroReport 8, 3743-3747.
39. Morara, S., Provini, L., Rosina, A., 1989. CGRP expression in the rat olivocerebellar system during postnatal development. Brain Res. 504, 315-319.
40. Morara, S., Rosina, A., Provini, L., 1992. CGRP as a marker of the climbing fibers during the development of the cerebellum in the rat. Ann. NY Acad. Sci. 657, 461-463.
41. Morara, S., Rosina, A., Provini, L., Forloni, G., Caretti, A., Wimalawansa, S.J., 2000. Calcitonin gene-related peptide receptor expression in the neurons and glia of developing rat cerebellum: an autoradiographic and immunohistochemical analysis. Neuroscience 100, 381-391.
42. Morara, S., Sternini, C., Provini, L., Rosina, A., 1995. Developmentally regulated expression of α- and β-calcitonin gene-related peptide mRNA and calcitonin gene-related peptide immunoreactivity in the rat inferior olive. J. Comp. Neurol. 354, 27-38.
43. Morara, S., van der Want, J.J.L., de Wolf, A., Provini, L., Rosina, A., 1993. Ultrastructural study of CGRP immunoreactivity in the neonatal cerebellum. Soc. Neurosci. Abstr. 19, 1215.
44. Morris, R.J., Beech, J.N., Heizmann, C.W., 1988. Two distinct phases and mechanisms of axonal growth shown by primary vestibular fibres in the brain, demonstrated by parvalbumin immunohistochemistry. Neuroscience 27, 571-596.
45. Mugnaini, E., 1969. Ultrastructural studies on the cerebellar histogenesis. II. Maturation of nerve cell populations and establishment of synaptic connections in the cerebellar cortex of the chick. In: Llinàs, R. (Ed.), Neurobiology of Cerebellar Evolution and Development. AMA/ERF, Chicago, IL, pp. 749-782.
46. Palacios-Prü, E.L., Palacios, L., Mendoza, R.V., 1981. Synaptogenetic mechanisms during chick cerebellar cortex development. J. Submicrosc. Cytol. 13, 145-167.
47. Palay, S.L., Chan-Palay, V., 1974. Cerebellar Cortex. Cytology and Organization. Springer-Verlag, Berlin.
48. Parsons, A.M., Seybold, V.S., 1997. Calcitonin gene-related peptide induces the formation of second messengers in primary cultures of neonatal rat spinal cord. Synapse 26, 235-242.
49. Priller, J., Haas, C.A., Reddington, M., Kreutzberg, G.W., 1995. Calcitonin gene-related peptide and ATP induce immediate early gene expression in cultured rat microglial cells. Glia 15, 447-457.
50. Ramón y Cajal, S., 1911. Histologie du Système Nerveux de l'Homme et des Vertébrés, vol. II. Maloine, Paris.
51. Rosina, A., Provini, L., Morara, S., 1989. Development of olivocerebellar somatotopic maps. In: Strata, P. (Ed.), The Olivocerebellar System in Motor Control. Exp. Brain Res. Ser. 17. Springer-Verlag, Berlin, pp. 150-154.
52. Rubenstein, J.L., 2000. Intrinsic and extrinsic control of cortical development. Novartis Found. Symp. 228, 67-75.
53. Schoen, S.W., Graeber, M.B., Tóth, L., Kreutzberg, G.W., 1991. Synaptic 5′-nucleotidase is transient and indicative of climbing fiber plasticity during the postnatal development of rat cerebellum. Dev. Brain Res. 61, 125-138.
54. Sotelo, C., Arsenio-Nunes, M.L., 1976. Development of Purkinje cells in absence of climbing fibers. Brain Res. 111, 389-395.
55. Takeda, T., Maekawa, K., 1989. Transient direct connection of vestibular mossy fibers to the vestibulocerebellar Purkinje cells in early postnatal development of kittens. Neuroscience 32, 99-111.
56. Tanaka, J., Nakamura, H., Miyawaki, S., 1988. Cerebellar involvement in murine sphingomyelinosis: a new model of Niemann-Pick disease. J. Neuropathol. Exp. Neurol. 47, 291-300.
57. Terrado, J., Gerrikagoitia, I., Dominguez, L., Raldua, D., Martinez-Millán, L., Sarasa, M., 1999. Expression of the genes for α-type and β-type calcitonin gene-related peptide during rat embryogenesis. Neuroscience 92, 713-727.
58. Terrado, J., Gerrikagoitia, I., Martinez-Millán, L., Pascual, F., Climent, S., Muniesa, P., Sarasa, M., 1997. Expression of the genes for α-type and β-type calcitonin gene-related peptide during postnatal rat brain development. Neuroscience 80, 951-970.
59. Ueyama, T., Houtani, T., Nakagawa, H., Baba, K., Ikeda, M., Yamashita, T., Sugimoto, T., 1994. A subpopulation of olivocerebellar projection neurons express neuropeptide Y. Brain Res. 634, 353-357.
60. van den Pol, A.N., Gores, T., 1986. Synaptic relationships between neurons containing vasopressin, gastrin-releasing peptide, vasoactive intestinal polypeptide, and glutamate decarboxylase immunoreactivity in the suprachiasmatic nucleus: dual ultrastructural immunocytochemistry with gold-substituted silver peroxidase. J. Comp. Neurol. 252, 507-521.
61. van der Want, J.J., Voogd, J., 1987. Ultrastructural identification and localization of climbing fiber terminals in the fastigial nucleus of the cat. J. Comp. Neurol. 258, 81-90.
62. Voogd, J., Bigaré, F., 1980. Topographical distribution of olivary and cortico nuclear fibers in the cerebellum: a review. In: Courville, J., De Montigny, C., Lamarre, Y. (Eds.), The Inferior Olivary Nucleus: Anatomy and Physiology. Raven, New York, pp. 207-234.
63. West, M.J., Del Cerro, M., 1976. Early formation of synapses in the molecular layer of the fetal rat cerebellum. J. Comp. Neurol. 165, 137-160.
64. White, R.H., Michaud, N.A., 1981. Disruption of insect photoreceptor membrane by divalent ions: dissimilar sensitivity of light- and dark-adapted mosquito rhabdomeres. Cell Tissue Res. 216, 403-411.
65. ++ -induced structural changes in photoreceptor microvilli of diptera. Cell Tissue Res. 206, 225-232.
66. Zhang, X., Åman, K., Hokfelt, T., 1995. Secretory pathways of neuropeptides in rat lumbar dorsal root ganglion neurons and effects of peripheral axotomy. J. Comp. Neurol. 352, 481-500.