Synapse elimination in the central nervous system: Functional significance and cellular mechanisms

Reviews in the Neurosciences

Volumn 7, Issue 2, 1996, Pages 85-101

  Lohof, Ann M ^a   Delhaye Bouchaud, Nicole ^a   Mariani, Jean ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

Cerebellum; Climbing fiber; Development; Purkinje cell; Synapse elimination; Synapse redundancy

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

BRAIN DEVELOPMENT; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CLIMBING FIBER; GRANULE CELL; MORPHOLOGY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE;

EID: 0030055566     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/REVNEURO.1996.7.2.85     Document Type: Review

References (138)

1. Armengol JA, Lopez-Roman A. Left unilateral interior pedunculotomy prevents neuronal death during postnatal development of the remaining left inferior olivary complex in the rat. Eur J Neurosci 1992; 4: 640-647.
2. Bailly Y, Debain D, Delhaye-Bouchaud N, Mariani J. The multiple innervation of cerebellar Purkinje cells by climbing fibers is totally maintained in adult rats which received a single postnatal irradiation. Proceedings of "Neurobiology of the cerebellar systems: A centenary of Ramon y Cajal's description of the cerebellar circuits", 1988.
3. Bailly Y, Schoen SW, Delhaye-Bouchaud N, Kreutzberg GW, Mariani J. Localisation synaptique de l'activité 5′-nucléotidase dans le cortex cérébelleux du rat adulte irradié aux rayons X après la naissance. CR Acad Sci Paris 1990; 311, Série III: 487-493.
4. Balice-Gordon RJ, Chua CK, Nelson CC, Lichtman JW. Gradual loss of synaptic cartels precede axon withdrawal at developing neuromuscular junctions. Neuron 1993; 11: 801-815.
5. Balice-Gordon RJ, Lichtman JW. Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 1994; 372: 519-524.
6. Balice-Gordon RJ, Lichtman JW. In vivo observations of pre- and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. J Neurosci 1993; 13: 834-855.
7. Barragan LA, Delhaye-Bouchaud N. Harmaline-induced activation of the olivo-cerebellar system in young rabbits: Further evidence for a transient multiinnervation of Purkinje cells by climbing fibres. Neuropharmacology 1980; 19: 305-310.
8. Bear MF, Kleinschmidt A, Gu Q, Singer W. Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist. J Neurosci 1990; 10: 909-925.
9. Benoit P, Changeux, J-P. Consequences of tenotomy on the evolution of multi-innervation in developing rat soleus muscle. Brain Res 1975; 99: 354-358.
10. Benoit P, Delhaye-Bouchaud N, Changeux J-P, Mariani J. Stability of multiple innervation of Purkinje cells by climbing fibers in the agranular cerebellum of old rats X-irradiated at birth. Dev Brain Res 1984; 14: 310-313.
11. Benoit P, Mariani J, Delhaye-Bouchaud N, Chappuis G. Evidence for a multiple innervation of cerebellar Purkinje cells by climbing fibers in adult ferrets infected at birth by a mink enteritis virus. Dev Brain Res 1987; 34: 51-57.
12. Betz WJ, Caldwell JH, Rochester RR. The effects of partial denervation at birth on the development of muscle fibres and motor units in rat lumbrical muscle. J Physiol 1980; 303: 265-279.
13. Betz WJ, Chua M, Ridge RMAP. Inhibitory interactions between motoneuron terminals in neonatal rat lumbrical muscle. J Physiol (Lond) 1989; 417: 25-51.
14. Bourgeois J-P, Rakic P. Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci 1993; 13: 2801-2820.
15. Bourrat F, Sotelo C. Postnatal development of the inferior olivary complex in the rat. III. A morphometric analysis of volumetric growth and neuronal cell number. Dev Brain Res 1984; 16: 241-251.
16. Brown MC, Holland RL, Hopkins WG. Restoration of focal multiple innervation in rat muscles by transmission block during a critical stage of development. J Physiol (Lond) 1981; 318: 355-364.
17. Brown MC, Jansen JKS, Van Essen D. Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. J Physiol (Lond) 1976; 261: 387-422.
18. Cabelli RJ, Hohn A, Shatz CJ. Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 1995; 267: 1662-1666.
19. Caddy KWT, Biscoe TJ. Structural and quantitative studies on the normal C3H and Lurcher mutant mouse. Philos Trans R Soc Lond (Biol) 1979; 287: 167-201.
20. Callaway EM, Soha JM, Van Essen DC. Competition favouring inactive over active motor neurons during synapse elimination. Nature 1987; 328: 422-426.
21. Callaway EM, Soha JM, Van Essen DC. Differential loss of neuromuscular connections according to activity level and spinal position of neonatal rabbit soleus motor neurons. J Neurosci 1989; 9: 1806-1824.
22. Callaway EM, Van Essen DC. Slowing of synapse elimination by alpha-bungarotoxin superfusion of the neonatal rabbit soleus muscle. Dev Biol 1989; 131: 356-365.
23. Campbell G, Shatz CJ. Synapses formed by identified retinogeniculate axons during the segregation of eye input. J Neurosci 1992; 12: 1847-1858.
24. Campbell NC, Armstrong DM. Topographical localization in the olivocerebellar projection in the rat: an autoradiographic study. Brain Res 1983; 275: 235-249.
25. Changeux J-P, Danchin A. Selective stabilization of developing synapses as a mechanism for the specification of neuronal networks. Nature 1976; 264: 705-712.
26. Chedotal A, Sotelo C. Early development of olivocerebellar projections in the fetal rat using CGRP immunocytochemistry. Eur J Neurosci 1992; 4: 1159-1179.
27. Chedotal A, Sotelo C. The "creeper stage" in cerebellar climbing fiber synaptogenesis precedes the "pericellular nest" - ultrastructural evidence with parvalbumin immunocytochemistry. Dev Brain Res 1993; 76: 207-220.
28. Cline HT, Constantine-Paton M. NMDA receptor agonists and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection. J Neurosci 1990; 10: 1197-1216.
29. Cline HT, Constantine-Paton M. NMDA receptor antagonists disrupt the retinotectal topographic map. Neuron 1989; 3: 413-429.
30. Colman H, Lichtman JW. Weakening of synaptic inputs due to low quantal content and efficacy at developing neuromuscular junctions. Society for Neuroscience Abstracts 1993; Abstract #526.3.
31. Connold AL, Evers JV, Vrbova G. Effect of low calcium and protease inhibitors on synapse elimination during postnatal development in the rat soleus muscle. Dev Brain Res 1986; 28: 99-107.
32. Cowan, WM, Fawcett JW, O'Leary DDM, Stanfield BB. Regressive events in neurogenesis. Science 1984; 225: 1258-1265.
33. Crepel F. Maturation of Purkinje cells by climbing fiber responses in the rat. Brain Res 1971; 35: 272-276.
34. Crepel F, Delhaye-Bouchaud N., Dupont JL. Fate of the multiple innervation of cerebellar Purkinje cells by climbing fibers in immature control, X-irradiated and hypothyroid rats. Dev Brain Res 1981; 1: 59-71.
35. Crepel F, Delhaye-Bouchaud N, Guastavino JM, Sampaio I. Multiple innervation of cerebellar Purkinje cells by climbing fibers in staggerer mutant mouse. Nature 1980; 283: 483-484.
36. Crepel F, Mariani J. Multiple innervation of Purkinje cells by climbing fibers in the cerebellum of the weaver mutant mouse. J Neurobiol 1976; 7: 579-582.
37. Crepel F, Mariani J, Delhaye-Bouchaud N. Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J Neurobiol 1976; 7: 567-578.
38. Crepel F, Delhaye-Bouchaud N, Legrand J. Electrophysiological analysis of the circuitry and of the corticonuclear relationships in the agranular cerebellum of irradiated rats. Arch Ital Biol 1976; 114: 49-74.
39. Dan Y, Poo MM. Hebbian depression of isolated neuromuscular synapses in vitro. Science 1992; 256: 1570-1573.
40. Dan Y, Poo M. Quantal transmitter secretion from myocytes loaded with acetylcholine. Nature 1992; 359: 733-736.
41. Dan Y, Poo M. Retrograde interactions during formation and elimination of neuromuscular synapses. Curr Opin Neurobiol 1994; 4: 95-100.
42. Dehay C, Kennedy H, Bullier J. Characterization of transient cortical projections from auditory, somatosensory, and motor cortices to visual areas 17, 18, and 19 in the kitten. J Comp Neurol 1988; 272: 68-89.
43. Delhaye-Bouchaud N, Geoffroy B, Mariani J. Neuronal death and synapse elimination in the olivocerebellar system. I. Cell counts in the inferior olive of developing rat. J Comp Neurol 1985; 232:299-308.
44. Delhaye-Bouchaud N, Mory G, Crepel F. Differential role of granule cells in the specification of synapses between climbing fibers and cerebellar Purkinje cells in the rat. Neurosci Lett 1978; 9: 51-58.
45. Dumesnil-Bousez N, Sotelo, C. Early development of the Lurcher cerebellum: Purkinje cell alterations and impairment of synaptogenesis. J Neurocytol 1992; 21: 506-529.
46. Dupont J-L, Delhaye-Bouchaud N, Crepel F. Autoradiographic study of the distribution of olivocerebellar connections during the involution of multiple innervation of Purkinje cells by climbing fibers in the developing rat. Neurosci Lett 1981; 26: 215-220.
47. Dupont J-L, Gardette R, Crepel F. Postnatal development of the chemosensitivity of rat cerebellar Purkinje cells to excitatory amino acids. An in vitro study. Dev Brain Res 1987; 34: 59-68.
48. Eddi F, Mariant J, Waysand G. Transient synaptic redundancy in the developing cerebellum and isostatic random stacking of hard spheres. Biol Cybernet 1995, in press.
49. Eisen JS, Myers PZ, Westerfield M. Pathway selection by growth cones of identified motoneurones in live zebra fish embryos. Nature 1986; 320: 269-271.
50. English AW, Schwartz G. Ciliary neurotrophic factor promotes the retention of multiple innervation of developing skeletal muscle fibers. Society for Neuroscience Abstracts 1992; Abstract #267.15.
51. English AW, Schwartz G. Is there a sensitive period for the effect of ciliary neurotrophic factor on neuromuscular synapse elimination? Society for Neuro-science Abstracts 1993; Abstract #454.3.
52. Fox K, Daw NW. Do NMDA receptors have a critical function in visual cortical plasticity? TINS 1993; 16: 116-122.
53. Fuhrman Y, Thomson M-A, Piat G, Mariani J, Delhaye-Bouchaud N. Enlargement of olivo-cerebellar microzones in the agranular cerebellum of adult rats. Brain Res 1994; 638: 277-284.
54. Fuhrman Y, Piat G, Thomson M-A, Mariani J, Delhaye-Bouchaud N. Abnormal ipsilateral functional vibrissae projection onto Purkinje cells multiply innervated by climbing fibers in the rat. Dev Brain Res 1995; 87: 172-178.
55. Gardette R, Crepel F, Alvarado-Mallart RM, Sotelo C. 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 1990; 295: 188-196.
56. Goodman CS, Shatz CJ. Developmental mechanisms that generate precise patterns of neuronal connectivity. Neuron 1993; 10(Suppl): 77-98.
57. Gurney ME, Kwon YW. Neurotrophic factors reset the timing of programmed synapse elimination in neonatal muscles. Society for Neuroscience Abstracts 1993; Abstract #454.2.
58. Hahm J-O, Langdon RB, Sur M. Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature 1991; 351: 568-570.
59. Hata Y, Stryker MP. Control of thalamocortical afferent rearrangement by postsynaptic activity in developing visual cortex. Science 1994; 265: 1732-1735.
60. Howe JR, Cull-Candy SG, Colquhoun D. Currents through single glutamate receptor channels in outside-out patches from rat cerebellar granule cells. J Physiol (Lond) 1991; 432: 143-202.
61. Innocenti GM. The development of interhemispheric connections. TINS 1981; 4: 142-144.
62. Innocenti GM. Growth and reshaping of axons in the establishment of visual callosal connections. Science 1981; 212: 824-827.
63. Innocenti GM, Clarke S, Koppel H. Transitory macrophages in the white matter of the developing visual cortex. II. Development and relations with axonal pathways. Dev Brain Res 1983; 11: 55-66.
64. Jackson H, Parks TN. Functional synapse elimination in the developing avian cochlear nucleus with simultaneous reduction in cochlear nerve axon branching. J Neurosci 1982; 2: 1736-1743.
65. Johnson DA, Purves D. Post-natal reduction of neural unit size in the rabbit ciliary ganglion. J Physiol 1981; 318: 143-159.
66. Jordan CL. Ciliary neurotrophic factor delays synapse elimination in the rat levator ani muscle. Society for Neuroscience Abstracts 1993; Abstract #454.4.
67. Kang H, Schuman EM. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 1995; 267: 1658-1662.
68. Kashiwabuci N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y, Aizawa S, Mishina M. Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR-delta-2 mutant mice. Cell 1995; 81: 245-252.
69. Kim HG, Wang T, Olafsson P, Lu B. Neurotrophin 3 potentiates neuronal activity and inhibits gamma-aminobutyratergic synaptic transmission in cortical neurons. Proc Natl Acad Sci USA 1994; 91: 12341-12345.
70. Knipper M, Berzaghi M, Blöchl A, Breer H, Thoenen H, Lindholm D. Positive feedback between acetylcholine and the neurotrophins nerve growth factor and brain-derived neurotrophic factor in the rat hippocampus. Eur J Neurosci 1994; 6: 668-671.
71. Krupa M, Crepel F. Transient sensitivity of rat cerebellar Purkinje cells to N-methyl-D-aspartate during development. A voltage clamp study in in vitro slices. Eur J Neurosci 1990; 2: 312-316.
72. Kwon YW, Abbondanzo SJ, Stewart CL, Gurney ME. Synapse withdrawal from developing neuromuscular junctions occurs earlier in LIF deficient transgenic mice. Society for Neuroscience Abstracts 1994; Abstract #451.12.
73. Landis DMD, Payne HR, Weinstein LA. Changes in the structure of synaptic junctions during climbing fiber synaptogenesis. Synapse 1989; 4: 281-293.
74. Landis DMD, Reese TS. Differences in membrane structure between excitatory and inhibitory synapses in the cerebellar cortex. J Comp Neurol 1974; 155: 93-126.
75. Landmesser L. The development of motor projection patterns in the chick hind limb. J Physiol 1978; 284: 391-414.
76. Larramendi LMH. Analysis of synaptogenesis in the cerebellum of the mouse. In: Llinas R, ed. Neurobiology of Cerebellar Evolution and Development. Chicago: Amer Med Assoc, 1969; 803-843.
77. Lessmann V, Gottmann K, Heumann R. BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. NeuroReport 1994; 6: 21-25.
78. Lichtman JW. The reorganization of synaptic connexions in the rat submandibular ganglion during post-natal development. J Physiol 1977; 273: 155-177.
79. Lichtman JW, Purves D. The elimination of redundant preganglionic innervation to hamster sympathetic ganglion cells in early post-natal life. J Physiol 1980; 301: 213-228.
80. Liu Y, Fields RD, Festoff BW, Nelson PG. Proteolytic action of-thrombin is required for electrical activity-dependent synapse reduction. Proc Natl Acad Sci USA 1994; 91: 10300-10304.
81. Liu Y, Fields RD, Fitzgerald S, Festoff BW, Nelson PG. Proteolytic activity, synapse elimination, and the Hebb synapse. J Neurobiol 1994; 25: 325-335.
82. Liu Y, Fields RD, Fitzgerald S, Nyhus W, Nelson PG. A protease inhibitor reduces activity-dependent synapse elimination at the mouse neuromuscular junction in vitro. Society for Neuroscience Abstracts 1992; Abstract #469.10.
83. Lo YJ, Poo MM. Activity-dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses. Science 1991; 254: 1019-1022.
84. Lohof AM, Ip NY, Poo MM. Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 1993; 263: 350-353.
85. Lopez-Roman A, Ambrasiani J, Armengol JA. Transient ipsilateral innervation of the cerebellum by developing olivocerebellar neurons. A retrograde double-labelling study with Fast Blue and Diamidino Yellow. Neuroscience 1993; 56: 485-497.
86. Lopez-Roman A, Armengol JA. Morphological evidence for the presence of ipsilateral inferior olivary neurons during postnatal development of the olivocerebellar projection in the rat. J Comp Neurol 1994; 350: 485-496.
87. Magchielse T, Meeter E. The effect of neuronal activity on the competitive elimination of neuromuscular junctions in tissue culture. Dev Brain Res 1986; 25: 211-220.
88. Mariani J. Extent of multiple innervation of Purkinje cells by climbing fibers in the olivo-cerebellar system of weaver, reeler and staggerer mutant mice. J Neurobiol 1982; 13: 119-126.
89. Mariani J. Elimination of synapses during the development of the central nervous system. Prog Brain Res 1983; 58: 383-392.
90. Mariani J, Benoit P, Hoang MD, Thomson M-A, Delhaye-Bouchaud N. 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 1990; 57: 63-70.
91. Mariani J, Changeux J-P. Ontogenesis of olivocerebellar relationships. I. Studies by intracellular recordings of the multiple innervation of Purkinje cells by climbing fibers in the developing rat cerebellum. J Neurosci 1981; 1: 696-702.
92. Mariani J, Changeux J-P. Etude par enregistrements intracellulaires de l'innervation multiple des cellules de Purkinje par les fibres grimpantes dans le cervelet du rat en développement. CR Acad Sci Paris 1980; 291: 97-100.
93. Mariani J, Changeux J-P. Multiple innervation of Purkinje cells by climbing fibers in the cerebellum of the adult staggerer mutant mouse. J Neurobiol 1980; 11: 41-50.
94. Mariani J, Crepel F, Mikoshiba K, Changeux J-P, Sotelo C. Anatomical, physiological and biochemical studies of the cerebellum from reeler mutant mouse. Phil Trans R Soc Ser B 1977; 281: 1-28.
95. Mariani J, Delhaye-Bouchaud N. Elimination of functional synapses during the development of the nervous system. NIPS 1987; 2: 93-97.
96. Mariani J, Mulle C, Geoffroy B, Delhaye-Bouchaud N. 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 1987; 421: 211-225.
97. Meister M, Wong ROL, Baylor DA, Shatz CJ. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 1991; 252: 939-943.
98. Missler M, Wolff A, Merker H-J, Wolff JR. Pre- and postnatal development of the primary visual cortex of the common marmoset. II. Formation, remodelling, and elimination of synapses as overlapping processes. J Comp Neurol 1993; 333: 53-67.
99. Mulle C, Delhaye-Bouchaud N, Mariani J. Peripheral maps and synapse elimination in the cerebellum of the rat. I. Representation of peripheral inputs through the climbing fiber pathway in the posterior vermis of the normal adult rat. Brain Res 1987; 421: 194-210.
100. Nabekura J, Lichtman JW. Progressive loss of synaptic efficacy during synapse elimination. Society for Neuroscience Abstracts 1989; Abstract #70.13.
101. Nelson PG, Fields RD, Liu Y. Neural activity, neuronglia relationships, and synapse development. Perspectives on Dev Neurobiol 1995; 2: 399-407.
102. Nelson PG, Fields RD, Yu C, Liu Y. Synapse elimination from the mouse neuromuscular junction in vitro: a non-Hebbian activity-dependent process. J Neurobiol 1993; 24: 1517-1530.
103. O'Brien RAD, Östberg, AJC, Vrbova G. Observations on the elimination of polyneuronal innervation in developing mammalian skeletal muscle. J Physiol 1978; 282: 571-582.
104. O'Leary JL, Inukai J, Smith JM. Histogenesis of the cerebellar climbing fiber in the rat. J Comp Neurol 1971; 142: 377-392.
105. Oppenheim RW. Cell death during development of the nervous system. Ann Rev Neurosci 1991; 14: 453-501.
106. O'Rourke NA, Cline HT, Fraser SE. Rapid remodeling of retinal arbors in the tectum with and without blockade of synaptic transmission. Neuron 1994; 12: 921-934.
107. Oscarsson O. Functional units of the cerebellum - sagittal zones and microzones. TINS 1979; 2: 143-145.
108. Piat G, Thomson M-A, Fuhrman Y, Mariani J, Delhaye-Bouchaud N. L'élimination synaptique joue-t-elle un rôle dans la formation des microzones cérébelleuses de projection des afférences grimpantes? CR Acad Sci Paris 1991; 313: 131-138.
109. Puro DG, Woodward DJ. The climbing fiber system in the weaver mutant. Brain Res 1977; 129: 141-146.
110. Purves D, Hadley RD, Voyvodic JT. Dynamic changes in the dendritic geometry of individual neurons visualized over periods of up to three months in the superior cervical ganglion of living mice. J Neurosci 1986; 6: 1051-1060.
111. Purves D, Voyvodic JT, Magrassi L, Yawo H. Nerve terminal remodeling visualized in living mice by repeated examination of the same neuron. Science 1987; 238: 1122-1126.
112. Rabacchi SA, Bailly Y, Delhaye-Bouchaud N, Herrup K, Mariani J. Role of the target in synapse elimination: Studies in cerebellum of developing lurcher mutants and adult chimeric mice. J Neurosci 1992; 12: 4712-4720.
113. Rabacchi SA, Bailly Y, Delhaye-Bouchaud N, Mariani J. Involvement of the N-methyl D-aspartate (NMDA) receptor in synapse elimination during cerebellar development. Science 1992; 256: 1823-1825
114. Redfern PA. Neuromuscular transmission in new-born rats. J Physiol (Lond) 1970; 209: 701-709.
115. Ronnevi L-O. Origin of the glial processes responsible for the spontaneous postnatal phagocytosis of boutons on cat spinal motoneurons. Cell Tiss Res 1978; 189: 203-217.
116. Ronnevi L-O, Conradi S. Ultrastructural evidence for spontaneous elimination of synaptic terminals on spinal motoneurons in the kitten. Brain Res 1974; 80: 335-339.
117. Rosenmund C, Legendre P, Westbrook GL. Expression of NMDA channels on cerebellar Purkinje cells acutely dissociated from newborn rats. J Neurophysiol 1992; 68: 1901-1905.
118. Schlaggar BL, Fox K, O'Leary DDM. Postsynaptic control of plasticity in developing somatosensory cortex. Nature 1993; 364: 623-626.
119. Schoen SW, Graeber MB, Toth L, Kreutzberg GW. Synaptic 5′-nucleotidase is transient and indicative of climbing fiber plasticity during the postnatal development of rat cerebellum. Dev Brain Res 1991; 61: 125-138.
120. Shatz CJ. Impulse activity and the patterning of connections during CNS development. Neuron 1990; 5: 745-756.
121. Shatz CJ, Stryker MP. Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 1988; 242: 87-89.
122. Sherrard RM, Bower AJ. An ipsilateral olivocerebellar connection: an autoradiographic study in the unilaterally pedunculotomised neonatal rat. Exp Brain Res 1986; 61: 355-363.
123. Siggins G, Henriksen J, Landis SC. Electrophysiology of Purkinje neurons in the weaver mouse: iontophoresis of neurotransmitters and cyclic nucleotides, and stimulation of the nucleus coeruleus. Brain Res 1976; 114: 53-69.
124. Simon DK, Prusky GT, O'Leary DDM, Constantine-Paton M. N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map. Proc Natl Acad Sci USA 1992; 89: 10593-10597.
125. Sotelo C. Cerebellar synaptogenesis: What we can learn from mutant mice. J Exp Biol 1990; 153: 225-249.
126. Sotelo C. Development of synaptic connections in genetic and experimentally induced cerebellar malformations. In: Garrod DR, Feldman JD, eds. Development of the Nervous System. Cambridge: Cambridge University Press, 1981; 61-83.
127. Sotelo C, Alvarado-Mallart RM. Growth and differentiation of cerebellar suspensions transplanted into the adult cerebellum of mice with heredodegenerative ataxia. Proc Natl Acad Sci USA 1986; 83: 1135-1139.
128. Sotelo C, Alvarado-Mallart RM, Gardette R, Crepel F. Fate of grafted embryonic Purkinje cells in the cerebellum of the adult "Purkinje cell degeneration" mutant mouse. I. Development of reciprocal graft-host interactions. J Comp Neurol 1990; 295: 165-187.
129. Sotelo C, Bourrat F, Triller A. Postnatal development of the inferior olivary complex in the rat. II. Topographic organization of the immature olivocerebellar projection. J Comp Neurol 1984; 222: 177-179.
130. Stanfield BB. Postnatal reorganization of cortical projections: the role of collateral elimination. TINS 1984; 7: 37-41.
131. Stoop R, Poo M-M. Potentiation of neurotransmitter secretion by ciliary neurotrophic factor requires somatic signaling. Science 1995; 267: 695-699.
132. Thomson M-A, Piat G, Cordonnier V, Ellouze-Kallel L, Delhaye-Bouchaud N, Mariani J. Representation of vibrissae inputs through the climbing fiber pathway in lobule VII of the adult rat cerebellar vermis. Brain Res 1989; 488: 241-252.
133. Thompson W. Activity and synapse elimination at the neuromuscular junction. Cell Mol Neurobiol 1985; 5: 167-182.
134. Thompson W. Synapse elimination in neonatal rat muscle is sensitive to pattern of muscle use. Nature 1983; 302: 614-616.
135. Thompson W, Kuffler DP, Jansen JKS. The effect of prolonged, reversible block of nerve impulses on the elimination of polyneuronal innervation of new-born rat skeletal muscle fibers. Neuroscience 1979; 4: 271-281.
136. Triller A, Sotelo C. Development of climbing fiber-Purkinje cell synapse in the rat. Morphological evidence for a transient stage of multi-innervation. Abstracts, 1st Meeting of the International Society of Developmental Neuroscience, 1980; p 177.
137. Waysand G, Mariani J. Topology of synaptogenesis: Macroscopic disorder and micro-organization. Comments in Dev Neurobiol 1989; 1: 1-10.
138. Woodward DJ, Hoffer BJ, Altman J. Physiological and pharmacological properties of Purkinje cells in rat cerebellum degranulated by postnatal X-irradiation. J Neurobiol 1974; 5: 283-304.