Afferent-target interactions during olivocerebellar development: Transcommissural reinnervation indicates interdependence of Purkinje cell maturation and climbing fibre synapse elimination

European Journal of Neuroscience

Volumn 22, Issue 11, 2005, Pages 2681-2688

  Lohof, Ann M ^a   Mariani, Jean ^a   Sherrard, Rachel M ^b  

^a Groupe Enzymologie Moléculaire et Fonctionnelle   (France)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Cerebellum; Plasticity; Rat; Synaptic regression; Synaptogenesis

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL INTERACTION; CELL MATURATION; CELL STRUCTURE; CEREBELLUM; CONTROLLED STUDY; DENDRITE; INNERVATION; NERVE FIBER; NERVE GROWTH; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT; SENSORY NERVE CELL; SYNAPSE; SYNAPTOGENESIS;

AGING; ANIMALS; AXONS; CEREBELLUM; ELECTROPHYSIOLOGY; MALE; MESENCEPHALON; NERVE FIBERS; NEURONS, AFFERENT; OLIVARY NUCLEUS; PATCH-CLAMP TECHNIQUES; PURKINJE CELLS; RATS; RATS, WISTAR; SYNAPSES;

EID: 29144482648     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04493.x     Document Type: Article

References (57)

1. Adcock, K.H., Metzger, F. & Kapfhammer, J.P. (2004) Purkinje cell dendritic tree development in the absence of excitatory neurotransmission and of brain-derived neurotrophic factor in organotypic slice cultures. Neuroscience, 127, 137-145.
2. 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.
3. Altman, J. & Anderson, W.J. (1971) Irradiation of the cerebellum in infant rats with low-level x-ray: histological and cytological effects during infancy and adulthood. Exp. Neurol., 30, 492-509.
4. Armengol, I.A. & Sotelo, C. (1991) Early dendritic development of Purkinje cells in the rat cerebellum. A light and electron microscopic study using axon tracing in 'in vitro' slices. Dev. Brain Res., 64, 95-114.
5. von Bartheld, C.S., Byers, M.R., Williams, R. & Bothwell, M. (1996) Anterograde transport of neurotrophins and axodendritic transfer in the developing visual system. Nature, 379, 830-833.
6. Berry, M. & Bradley, P. (1976) The growth of the dendritic trees of Purkinje cells in the cerebellum of the rat. Brain Res., 112, 1-35.
7. Bondy, C.A. (1991) Transient IGF-I gene expression during the maturation of functionally related central projection neurones. J. Neurosci., 11, 3442-3455.
8. Bower, A.J. (1988) Observations on the effect of deafferentation on the granule cells of the neonatal rat cerebellum. Neurosci. Lett. Suppl., 30, S50.
9. Bower, A.J. & Waddington, G. (1981) A simple operative technique for chronically severing the cerebellar peduncles in neonatal rats. J. Neurosci. Meth., 4, 181-188.
10. Bradley, P. & Berry, M. (1976) Quantitative effects of climbing fibre deafferentation on the adult Purkinje cell dendritic tree. Brain Res., 112, 133-140.
11. 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.
12. Castro-Alamancos, M.A., Arevalo, M.A. & Torres-Aleman, I. (1996) Involvement of protein kinase C and nitric oxide in the modulation by insulin-like growth factor-I of glutamate-induced GABA release in the cerebellum. Neuroscience, 70, 843-847.
13. Cerminara, N.L., Makarabhirom, K. & Rawson, J.A. (2003) Somatosensory properties of cuneocerebellar neurones in the main cuneate nucleus of the rat. Cerebellum, 2, 131-145.
14. 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., 1, 567-578.
15. Fukudome, Y., Tabata, T., Miyoshi, T., Haruki, S., Araishi, K., Sawada, S. & Kano, M. (2003) Insulin-like growth factor-1 as a promoting factor for cerebellar Purkinje cell development. Eur. J. Neurosci., 17, 2006-2016.
16. Gardette, R., Crepel, F., Alvarado-Mallart, R.M. & Sotelo, C. (1990) Fate of grafted embryonic Purkinje cells in the cerebellum of the adult 'Purkinje cell degeneration' mutant mouse. II. Development of synaptic responses: an in vitro study. J. Comp. Neurol., 295, 188-196.
17. Gomez, T.M. & Spitzer, N.C. (1999) In vivo regulation of axon extension and pathfinding by growth-cone calcium transients. Nature, 397, 350-355.
18. Hashimoto, K. & Kano, M. (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron, 38, 785-796.
19. Hua, J.Y. & Smith, S.J. (2004) Neural activity and the dynamics of central nervous system development. Nature Neurosci., 7, 327-332.
20. Jhaveri, S., Edwards, M.A. & Schneider, G.E. (1991) Initial stages of retinofugal axon development in the hamster: evidence for two distinct modes of growth. Exp. Brain Res., 87, 371-382.
21. Katz, L.C. & Shatz, C.J. (1996) Synaptic activity and the construction of synaptic circuits. Science, 274, 1133-1138.
22. Llano, I., Marry, A., Armstrong, C.M. & Konnerth, A. (1991) Synaptic- and agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices. J. Physiol. (Lond.), 434, 183-213.
23. Mariani, J., Benoit, P., Hoang, M.D., Thomson, M.A. & Delhaye-Bouchaud, N. (1990) Extent of multiple innervation of cerebellar Purkinje cells by climbing fibers in adult X-irradiated rats. Comparison of different schedules of irradiation during the first postnatal week. Dev. Brain Res., 57, 63-70.
24. Mariani, J. & Changeux, J.-P. (1981) Ontogenesis of olivocerebellar relationships. I. Studies by intracellular recordings of the multiple innervation of Purkinje cells by climbing fibres in the developing rat cerebellum. J. Neurosci., 1, 696-702.
25. McCallister, A.K., Katz, L.C. & Lo, D.C. (1999) Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci., 22, 295-318.
26. van Mier, P. & Lichtman, J.W. (1994) Regenerating muscle fibers induce directional sprouting from nearby nerve terminals: studies in living mice. J. Neurosci., 14, 5672-5686.
27. Mooney, R.D., Savage, S.V., Hobler, S., King, T.D. & Rhoades, R.W. (1992) Normal development and effects of deafferentation on the morphology of superior collicular neurons projecting to the lateral posterior nucleus in hamster. J. Comp. Neurol., 315, 413-430.
28. Morris, R.J., Beech, J.N., Barber, P.C. & Raisman, G. (1985a) Early stages of Purkinje cell maturation demonstrated by Thy-1 immunohistochemistry on postnatal rat cerebellum. J. Neurocytol., 14, 427-452.
29. Morris, R.J., Beech, J.N., Barber, P.C. & Raisman, G. (1985b) Late emergence of Thy-1 on climbing fibres demonstrates a gradient of maturation from the fissures to the folial convexities in developing rat cerebellum. J. Neurocytol., 14, 453-467.
30. Morrison, M.E. & Mason, C.A. (1998) Granule neuron regulation of Purkinje cell development: striking a balance between neurotrophin and glutamate signaling. J. Neurosci., 18, 3563-3573.
31. Neppi-Modona, M., Rossi, F. & Strata, P. (1999) Phenotype changes of inferior olive neurons following collateral reinnervation. Neuroscience, 94, 209-215.
32. Portera-Cailliau, C., Weimer, R.M., De Paola, V., Caroni, P. & Svoboda, K. (2005) Diverse modes of axon elaboration in the developing neocortex. PLoS Biol., 3, e272.
33. Rabacchi, S.A., Bailly, Y., Delhaye-Bouchaud, N., Herrup, K. & Mariani, J. (1992) Role of the target in synapse elimination: studies in cerebellum of developing Lurcher mutants and adult chimeric mice. J. Neurosci., 12, 4712-4720.
34. Rocamora, N., Garcia-Ladona, F.J., Palacios, J.M. & Mengod, G. (1993) Differential expression of brain-derived neurotrophic factor, neurotrophin-3 and low-affinity nerve growth factor receptor during postnatal development of the rat cerebellar system. Mol. Brain Res., 17, 1-8.
35. Rossi, F., Jankovski, A. & Sotelo, C. (1995) Target neuron controls the integrity of afferent axon phenotype - a study on the Purkinje cell-climbing fiber system in cerebellar mutant mice. J. Neurosci., 15, 2040-2056.
36. Sabel, B.A. & Schneider, G.E. (1988) The principle of 'conservation of total axonal arborisation' massive compensatory sprouting in the hamster subcortical visual system after early tectal lesions. Exp. Brain Res., 73, 505-518.
37. Scelfo, B. & Strata, P. (2005) Correlation between multiple climbing fibre regression and parallel fibre response development in the postnatal mouse cerebellum. Eur. J. Neurosci., 21, 971-978.
38. Scelfo, B., Strata, P. & Knopfel, T. (2003) Sodium imaging of climbing fiber innervation fields in developing mouse Purkinje cells. J. Neurophysiol., 89, 2555-2563.
39. Sherman, S.M., Hoffman, K.P. & Stone, J. (1972) Loss of a specific cell type from the dorsal lateral geniculate nucleus in visually deprived cats. J. Neurophysiol., 35, 532-541.
40. Sherrard, R.M. & Bower, A.J. (2002) Climbing fiber development: do neurotrophins have a part to play? Cerebellum, 1, 265-275.
41. Singh, K.K. & Miller, F.D. (2005) Activity regulates positive and negative neurotrophin-derived signals to determine axon competition. Neuron, 45, 837-845.
42. Sotelo, C. & Arsenio-Nunes, M.L. (1976) Development of Purkinje cells in the absence of climbing fibres. Brain Res., 111, 389-395.
43. Sotelo, C. & Mariani, J. (1999) Research strategies for the analysis of neurological mutants in the mouse. In Crusio, W. & Gerlai, R. (eds), Handbook of Molecular-Genetic Techniques for Brain and Behavior Research (Techniques in the Behavioral and Neural Sciences). Elsevier Science BV, Amsterdam, pp. 132-146.
44. Strata, P., Tempia, F., Zagrebelsky, M. & Rossi, F. (1997) Reciprocal trophic interactions between climbing fibres and Purkinje cells in the rat cerebellum. Prog. Brain Res., 114, 263-282.
45. Sugihara, I. (2005) Microzonal projection and climbing fiber remodeling in single olivocerebellar axons of newborn rats at postnatal days 4-7. J. Comp. Neurol., 487, 93-106.
46. Sugihara, I., Bailly, Y. & Mariani, J. (2000) Olivocerebellar climbing fibers in the granuloprival cerebellum: morphological study of individual axonal projections in the X-irradiated rat. J. Neurosci., 20, 3745-3760.
47. Sugihara, I., Lohof, A.M., Letellier, M., Mariani, J. & Sherrard, R.M. (2003) Post-lesion transcommissural growth of olivary climbing fibres creates functional synaptic microzones. Eur. J. Neurosci., 18, 3027-3036.
48. Sugihara, I., Wu, H.S. & Shinoda, Y. (2001) The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to cerebellar compartmentalization. J. Neurosci., 21, 7715-7723.
49. Takei, N., Inamura, N., Kawamura, M., Namba, H., Hara, K., Yonezawa, K. & Nawa, H. (2004) Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J. Neurosci., 24, 9760-9769.
50. Tempia, F., Bravin, M. & Strata, P. (1996) Postsynaptic currents and short-term synaptic plasticity in Purkinje cells grafted onto an uninjured adult cerebellar cortex. Eur. J. Neurosci., 8, 2690-2701.
51. Thompson, W. (1983) Synapse elimination in neonatal rat muscle is sensitive to pattern of muscle use. Nature, 302, 614-615.
52. Tolbert, D.L. & Gutting, J.C. (1997) Quantitative analysis of cuneocerebellar projections in rats: differential topography in the anterior and posterior lobes. Neuroscience, 80, 359-371.
53. Torres-Aleman, I., Pons, S. & Arevalo, M.A. (1994) The insulin-like growth factor I system in the rat cerebellum: developmental regulation and role in neuronal survival and differentiation. J. Neurosci. Res., 39, 117-126
54. Tucker, K.L., Meyer, M. & Barde, Y.-A. (2001) Neurotrophins are required for nerve growth during development. Nature Neuroscience, 4, 29-37.
55. Wiesel, T.N. & Hubel, D.H. (1965) Comparison of the effects of unilateral and bilateral unit responses in kittens. J. Neurophysiol., 28, 1029-1040.
56. Zagrebelsky, M., Strata, P., Hawkes, R. & Rossi, F. (1997) 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.
57. Zuddas, A., Corsini, G.U., Barker, J.L., Kopin, I.J. & Di Porzio, U. (1991) Specific reinnervation of lesioned mouse striatum by grafted mesencephalic dopaminergic neurons. Eur. J. Neurosci., 3, 72-85.