Axon pruning: An essential step underlying the developmental plasticity of neuronal connections

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 361, Issue 1473, 2006, Pages 1531-1544

  Low, Lawrence K ^a   Cheng, Hwai Jong ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Axon degeneration; Axon pruning; Axon retraction; Wallerian degeneration

Indexed keywords

CYTOPLASM; DISEASE TREATMENT; NERVOUS SYSTEM; NERVOUS SYSTEM DISORDER; PLASTICITY; PROTEIN;

WALLERIA;

EID: 33749017645     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2006.1883     Document Type: Review

References (132)

1. Adams, B., Lee, M., Fahnestock, M. & Racine, R. J. 1997 Long-term potentiation trains induce mossy fiber sprouting. Brain Res. 775, 193-197. (doi:10.1016/S0006-8993(97)01061-5)
2. Aggoun-Zouaoui, D. & Innocenti, G. M. 1994 Juvenile visual callosal axons in kittens display origin- and fate-related morphology and distribution of arbors. Eur. J. Neurosci. 6, 1846-1863. (doi:10.1111/j.1460-9568.1994.tb00577. x)
3. Amaral, D. G. & Dent, J. A. 1981 Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J. Comp. Neurol. 195, 51-86. (doi:10.1002/cne.901950106)
4. Araki, T., Sasaki, Y. & Milbrandt, J. 2004 Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305, 1010-1013. (doi:10.1126/science.1098014)
5. Awasaki, T. & Ito, K. 2004 Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr. Biol. 14, 668-677. (doi:10.1016/j.cub.2004.04.001)
6. Awasaki, T., Saito, M., Sone, M., Suzuki, E., Sakai, R., Ito, K. & Hama, C. 2000 The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 26, 119-131. (doi:10.1016/S0896-6273(00)81143-5)
7. Bagri, A., Cheng, H. J., Yaron, A., Pleasure, S. J. & Tessier-Lavigne, M. 2003 Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 113, 285-299. (doi:10.1016/S0092-8674(03)00267-8)
8. Barres, B. A. 1999 A new role for glia: generation of neurons! Cell 97, 667-670. (doi:10.1016/S0092-8674(00)80777-1)
9. Bateman, J., Shu, H. & Van Vactor, D. 2000 The guanine nucleotide exchange factor trio mediates axonal development in the Drosophila embryo. Neuron 26, 93-106. (doi:10.1016/S0896-6273(00)81141-1)
10. Bernstein, M. & Lichtman, J. W. 1999 Axonal atrophy: the retraction reaction. Curr. Opin. Neurobiol. 9, 364-370. (doi:10.1016/S0959-4388(99)80053-1)
11. Billuart, P., Winter, C. G., Maresh, A., Zhao, X. & Luo, L. 2001 Regulating axon branch stability: the role of p190 RhoGAP in repressing a retraction signaling pathway. Cell 107, 195-207. (doi:10.1016/S0092-8674(01) 00522-0)
12. Bishop, D. L., Misgeld, T., Walsh, M. K., Gan, W. B. & Lichtman, J. W. 2004 Axon branch removal at developing synapses by axosome shedding. Neuron 44, 651-661. (doi:10.1016/j.neuron.2004.10.026)
13. Bixby, J. L. 1981 Ultrastructural observations on synapse elimination in neonatal rabbit skeletal muscle. J. Neurocytol. 10, 81-100. (doi:10.1007/ BF01181746)
14. Bonhoeffer, T. & Yuste, R. 2002 Spine motility. Phenomenology, mechanisms, and function. Neuron 35, 1019-1027. (doi:10.1016/S0896-6273(02) 00906-6)
15. Buffelli, M., Burgess, R. W., Feng, G., Lobe, C. G., Lichtman, J. W. & Sanes, J. R. 2003 Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424, 430-434. (doi:10.1038/ nature01844)
16. Burek, M. J. & Oppenheim, R. W. 1996 Programmed cell death in the developing nervous system. Brain Pathol. 6, 427-446.
17. Campenot, R. B. 1982a Development of sympathetic neurons in compartmentalized cultures. II. Local control of neurite survival by nerve growth factor. Dev. Biol. 93, 13-21. (doi:10.1016/0012-1606(82)90233-0)
18. Campenot, R. B. 1982b Development of sympathetic neurons in compartmentalized cultures. I. Local control of neurite growth by nerve growth factor. Dev. Biol. 93, 1-12. (doi:10.1016/0012-1606(82)90232-9)
19. Cavanagh, J. B. 1964 The significance of the 'dying back' process in experimental and human neurological disease. Int. Rev. Exp. Pathol. 3, 219-267.
20. Cheng, H. J., Bagri, A., Yaron, A., Stein, E., Pleasure, S. J. & Tessier-Lavigne, M. 2001 Plexin-A3 mediates semaphorin signaling and regulates the development of hippocampal axonal projections. Neuron 32, 249-263. (doi:10.1016/S0896-6273(01)00478-0)
21. Cheng, H. J., Nakamoto, M., Bergemann, A. D. & Flanagan, J. G. 1995 Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 82, 371-381. (doi:10.1016/0092-8674(95)90426-3)
22. Coleman, M. P. & Perry, V. H. 2002 Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci. 25, 532-537. (doi:10.1016/S0166-2236(02)02255-5)
23. Colman, H., Nabekura, J. & Lichtman, J. W. 1997 Alterations in synaptic strength preceding axon withdrawal. Science 275, 356-361. (doi:10.1126/science.275.5298.356)
24. Coleman, M. P., Conforti, L., Buckmaster, E. A., Tarlton, A., Ewing, R. M., Brown, M. C., Lyon, M. F. & Perry, V. H. 1998 An 85-kb tandem triplication in the slow Wallerian degeneration (Wlds) mouse. Proc. Natl Acad. Sci. USA 95, 9985-9990. (doi:10.1073/pnas.95.17.9985)
25. Conforti, L., Tarlton, A., Mack, T. G., Mi, W., Buckmaster, E. A., Wagner, D., Perry, V. H. & Coleman, M. P. 2000 A Ufd2/D4Cole1e chimeric protein and overexpression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. Proc. Natl Acad. Sci. USA 97, 11 377-11 382. (doi:10.1073/pnas.97.21. 11377)
26. Cowan, W. M., Fawcett, J. W., O'Leary, D. D. & Stanfield, B. B. 1984 Regressive events in neurogenesis. Science 225, 1258-1265.
27. Deckwerth, T. L. & Johnson Jr, E. M. 1994 Neurites can remain viable after destruction of the neuronal soma by programmed cell death (apoptosis). Dev. Biol. 165, 63-72. (doi:10.1006/dbio.1994.1234)
28. De Felipe, J. & Jones, E. G. 1991 Cajal's degeneration and regeneration of the nervous system. New York, NY: Oxford University Press.
29. Dehay, C., Horsburgh, G., Berland, M., Killackey, H. & Kennedy, H. 1989 Maturation and connectivity of the visual cortex in monkey is altered by prenatal removal of retinal input. Nature 337, 265-267. (doi:10.1038/337265a0)
30. Dubois-Dauphin, M., Frankowski, H., Tsujimoto, Y., Huarte, J. & Martinou, J. C. 1994 Neonatal motoneurons overexpressing the bcl-2 protooncogene in transgenic mice are protected from axotomy-induced cell death. Proc. Natl Acad. Sci. USA 91, 3309-3313. (doi:10.1073/pnas.91.8.3309)
31. Eaton, B. A. & Davis, G. W. 2003 Synapse disassembly. Genes Dev. 17, 2075-2082. (doi:10.1101/gad.1113703)
32. Eaton, B. A. & Davis, G. W. 2005 LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron 47, 695-708. (doi:10.1016/j.neuron.2005.08.010)
33. Eaton, B. A., Fetter, R. D. & Davis, G. W. 2002 Dynactin is necessary for synapse stabilization. Neuron 34, 729-741. (doi:10.1016/S0896-6273(02) 00721-3)
34. Eckenhoff, M. F. & Pysh, J. J. 1979 Double-walled coated vesicle formation: evidence for massive and transient conjugate internalization of plasma membranes during cerebellar development. J. Neurocytol. 8, 623-638. (doi:10.1007/BF01208513)
35. Ethell, I. M. & Pasquale, E. B. 2005 Molecular mechanisms of dendritic spine development and remodeling. Prog. Neurobiol. 75, 161-205. (doi:10.1016/j.pneurobio.2005.02.003)
36. Ferri, A., Sanes, J. R., Coleman, M. P., Cunningham, J. M. & Kato, A. C. 2003 Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Curr. Biol. 13, 669-673. (doi:10.1016/S0960-9822(03)00206-9)
37. Finn, J. T., Weil, M., Archer, F., Siman, R., Srinivasan, A. & Raff, M. C. 2000 Evidence that Wallerian degeneration and localized axon degeneration induced by local neurotrophin deprivation do not involve caspases. J. Neurosci. 20, 1333-1341.
38. Frost, D. O., Moy, Y. P. & Smith, D. C. 1990 Effects of alternating monocular occlusion on the development of visual callosal connections. Exp. Brain Res. 83, 200-209. (doi:10.1007/BF00232209)
39. Gan, W. B. & Lichtman, J. W. 1998 Synaptic segregation at the developing neuromuscular junction. Science 282, 1508-1511. (doi:10.1126/science. 282.5393.1508)
40. Gillingwater, T. H. & Ribchester, R. R. 2001 Compartmental neurodegeneration and synaptic plasticity in the Wld(s) mutant mouse. J. Physiol. 534, 627-639. (doi:10.1111/j.1469-7793.2001.00627.x)
41. Goda, Y. & Davis, G. W. 2003 Mechanisms of synapse assembly and disassembly. Neuron 40, 243-264. (doi:10.1016/S0896-6273(03)00608-1)
42. Govek, E. E., Newey, S. E. & Van Aelst, L. 2005 The role of the Rho GTPases in neuronal development. Genes Dev. 19, 1-49. (doi:10.1101/gad.1256405)
43. Griffin, J. W., George, E. B. & Chaudhry, V. 1996 Wallerian degeneration in peripheral nerve disease. Baillieres Clin. Neurol. 5, 65-75.
44. Hashimoto, K. & Kano, M. 2003 Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38, 785-796. (doi:10.1016/S0896-6273(03)00298-8)
45. Hebbar, S. & Fernandes, J. J. 2004 Pruning of motor neuron branches establishes the DLM innervation pattern in Drosophila. J. Neurobiol. 60, 499-516. (doi:10.1002/neu.20031)
46. Horner, P. J. & Gage, F. H. 2000 Regenerating the damaged central nervous system. Nature 407, 963-970. (doi:10.1038/35039559)
47. Houzel, J. C., Milleret, C. & Innocenti, G. 1994 Morphology of callosal axons interconnecting areas 17 and 18 of the cat. Eur. J. Neurosci. 6, 898-917. (doi:10.1111/j.1460-9568.1994.tb00585.x)
48. Innocenti, G. M. 1981 Growth and reshaping of axons in the establishment of visual callosal connections. Science 212, 824-827.
49. Innocenti, G. M. 1995 Exuberant development of connections, and its possible permissive role in cortical evolution. Trends Neurosci. 18, 397-402. (doi:10.1016/0166-2236(95)93936-R)
50. Innocenti, G. M. & Clarke, S. 1984 The organization of immature callosal connections. J. Comp. Neurol. 230, 287-309. (doi:10.1002/cne.902300212)
51. Ito, M. 1984 The modifiable neuronal network of the cerebellum. Jpn. J. Physiol. 34, 781-792.
52. Kage, E., Hayashi, Y., Takeuchi, H., Hirotsu, T., Kunitomo, H., Inoue, T., Arai, H., Iino, Y. & Kubo, T. 2005 MBR-1, a novel helix-turn-helix transcription factor, is required for pruning excessive neurites in Caenorhabditis elegans. Curr. Biol. 15, 1554-1559. (doi:10.1016/j.cub.2005.07. 057)
53. Kerschensteiner, M., Schwab, M. E., Lichtman, J. W. & Misgeld, T. 2005 In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat. Med. 11, 572-577. (doi:10.1038/nm1229)
54. Koirala, S. & Ko, C. P. 2004 Pruning an axon piece by piece: a new mode of synapse elimination. Neuron 44, 578-580.
55. Koralek, K. A. & Killackey, H. P. 1990 Callosal projections in rat somatosensory cortex are altered by early removal of afferent input. Proc. Natl Acad. Sci. USA 87, 1396-1400. (doi:10.1073/pnas.87.4.1396)
56. Kuo, C. T., Jan, L. Y. & Jan, Y. N. 2005 Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteosome, and ecdysone signaling. Proc. Natl Acad. Sci. USA 102, 15 230-15 235. (doi:10.1073/pnas.0507393102)
57. Lee, T., Marticke, S., Sung, C., Robinow, S. & Luo, L. 2000a Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 28, 807-818. (doi:10.1016/S0896- 6273(00)00155-0)
58. Lee, T., Winter, C., Marticke, S. S., Lee, A. & Luo, L. 2000b Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25, 307-316. (doi:10.1016/S0896-6273(00)80896-X)
59. Lendvai, B., Stern, E. A., Chen, B. & Svoboda, K. 2000 Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404, 876-881. (doi:10.1038/35009107)
60. Levi-Montalcini, R. 1987 The nerve growth factor 35 years later. Science 237, 1154-1162.
61. Lichtman, J. W. & Balice-Gordon, R. J. 1990 Understanding synaptic competition in theory and in practice. J. Neurobiol. 21, 99-106. (doi:10.1002/neu.480210107)
62. Lichtman, J. W. & Colman, H. 2000 Synapse elimination and indelible memory. Neuron 25, 269-278. (doi:10.1016/S0896-6273(00)80893-4)
63. Liu, X. B., Low, L. K., Jones, E. G. & Cheng, H. J. 2005 Stereotyped axon pruning via plexin signaling is associated with synaptic complex elimination in the hippocampus. J. Neurosci. 25, 9124-9134. (doi:10.1523/ JNEUROSCI.2648-05.2005)
64. Lohof, A. M., Delhaye-Bouchaud, N. & Mariani, J. 1996 Synapse elimination in the central nervous system: functional significance and cellular mechanisms. Rev. Neurosci. 7, 85-101.
65. Lund, R. D., Mitchell, D. E. & Henry, G. H. 1978 Squint-induced modification of callosal connection in cats. Brain Res. 144, 169-172. (doi:10.1016/0006-8993(78)90445-6)
66. Lunn, E. R., Perry, V. H., Brown, M. C., Rosen, H. & Gordon, S. 1989 Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur. J. Neurosci. 1, 27-33. (doi:10.1111/j.1460-9568.1989.tb00771.x)
67. Luo, L. 2000 Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1, 173-180. (doi:10.1038/35044547)
68. Luo, L. & O'Leary, D. D. 2005 Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28, 127-156. (doi:10.1146/annurev. neuro.28.061604.135632)
69. Mack, T. G. et al. 2001 Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 4, 1199-1206. (doi:10.1038/nn770)
70. Mallat, M., Marin-Teva, J. L. & Cheret, C. 2005 Phagocytosis in the developing CNS: more than clearing the corpses. Curr. Opin. Neurobiol. 15, 101-107. (doi:10.1016/j.conb.2005.01.006)
71. Mariani, J. 1983 Elimination of synapses during the development of the central nervous system. Prog. Brain Res. 58, 383-392.
72. Marin, E. C., Watts, R. J., Tanaka, N. K., Ito, K. & Luo, L. 2005 Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132, 725-737. (doi:10.1242/dev.01614)
73. Marty, S. & Peschanski, M. 1994 Fine structural alteration in target-deprived axonal terminals in the rat thalamus. Neuroscience 62, 1121-1132. (doi:10.1016/0306-4522(94)90348-4)
74. Marty, S., Weinitz, J. M. & Peschanski, M. 1994 Target dependence of adult neurons: pattern of terminal arborizations. J. Neurosci. 14, 5257-5266.
75. 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.
76. McBurney, M. W., Yang, X., Jardine, K., Hixon, M., Boekelheide, K., Webb, J. R., Lansdorp, P. M. & Lemieux, M. 2003 The mammalian SIR2alpha protein has a role in embryogenesis and gametogenesis. Mol. Cell Biol. 23, 38-54. (doi:10.1128/MCB.23.1.38-54.2003)
77. McLaughlin, T., Hindges, R. & O'Leary, D. D. 2003 Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr. Opin. Neurobiol. 13, 57-69. (doi:10.1016/S0959-4388(03)00014-X)
78. Meier, P., Finch, A. & Evan, G. 2000 Apoptosis in development. Nature 407, 796-801. (doi:10.1038/35037734)
79. Nakamoto, M., Cheng, H. J., Friedman, G. C., McLaughlin, T., Hansen, M. J., Yoon, C. H., O'Leary, D. D. & Flanagan, J. G. 1996 Topographically specific effects of ELF-1 on retinal axon guidance in vitro and retinal axon mapping in vivo. Cell 86, 755-766. (doi:10.1016/S0092-8674(00)80150-6)
80. Nakamura, H. & O'Leary, D. D. 1989 Inaccuracies in initial growth and arborization of chick retinotectal axons followed by course corrections and axon remodeling to develop topographic order. J. Neurosci. 9, 3776-3795.
81. Neumann, S., Bradke, F., Tessier-Lavigne, M. & Basbaum, A. I. 2002 Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34, 885-893. (doi:10.1016/S0896-6273(02) 00702-X)
82. Ng, J., Nardine, T., Harms, M., Tzu, J., Goldstein, A., Sun, Y., Dietzl, G., Dickson, B. J. & Luo, L. 2002 Rac GTPases control axon growth, guidance and branching. Nature 416, 442-447. (doi:10.1038/416442a)
83. Nguyen, Q. T. & Lichtman, J. W. 1996 Mechanism of synapse disassembly at the developing neuromuscular junction. Curr. Opin. Neurobiol. 6, 104-112. (doi:10.1016/S0959-4388(96)80015-8)
84. O'Leary, D. D. 1987 Remodelling of early axonal projections through the selective elimination of neurons and long axon collaterals. Ciba Found. Symp. 126, 113-142.
85. O'Leary, D. D. & Stanfield, B. B. 1989 Selective elimination of axons extended by developing cortical neurons is dependent on regional locale: experiments utilizing fetal cortical transplants. J. Neurosci. 9, 2230-2246.
86. O'Leary, D. D., Bicknese, A. R., De Carlos, J. A., Heffner, C. D., Koester, S. E., Kutka, L. J. & Terashima, T. 1990 Target selection by cortical axons: alternative mechanisms to establish axonal connections in the developing brain. Cold Spring Harb. Symp. Quant. Biol. 55, 453-468.
87. Oppenheim, R. W. 1981 Studies in developmental neurobiology: essays in honor of Viktor Hamburger. In The neurotrophic theory and naturally occurring motoneuron death (ed. W. M. Cowan). New York, NY: Oxford University Press.
88. Oppenheim, R. W. 1989 The neurotrophic theory and naturally occurring motoneuron death. Trends Neurosci. 12, 252-255. (doi:10.1016/0166-2236(89)90021- 0)
89. Pearson, H. E., Stoffler, D. J. & Sonstein, W. J. 1992 Response of retinal terminals to loss of postsynaptic target neurons in the dorsal lateral geniculate nucleus of the adult cat. J. Comp. Neurol. 315, 333-343. (doi:10.1002/cne.903150308)
90. Pielage, J., Fetter, R. D. & Davis, G. W. 2005 Presynaptic spectrin is essential for synapse stabilization. Curr. Biol. 15, 918-928. (doi:10.1016/j.cub.2005.04.030)
91. 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. (doi:10.1371/journal.pbio.0030272)
92. Purves, D. & Lichtman, J. W. 1980 Elimination of synapses in the developing nervous system. Science 210, 153-157.
93. Raff, M. C., Whitmore, A. V. & Finn, J. T. 2002 Axonal self-destruction and neurodegeneration. Science 296, 868-871. (doi:10.1126/science.1068613)
94. Reddy, L. V., Koirala, S., Sugiura, Y., Herrera, A. A. & Ko, C. P. 2003 Glial cells maintain synaptic structure and function and promote development of the neuromuscular junction in vivo. Neuron 40, 563-580. (doi:10.1016/S0896-6273(03)00682-2)
95. Reinoso, B. S. & O'Leary, D. D. M. 1989 Extension, branching and regression of visual corticospinal axons in rat. Soc. Neurosci. Abstr. 15, 1337.
96. Riley, D. A. 1981 Ultrastructural evidence for axon retraction during the spontaneous elimination of polyneuronal innervation of the rat soleus muscle. J. Neurocytol. 10, 425-440. (doi:10.1007/BF01262414)
97. Rosenthal, J. L. & Taraskevich, P. S. 1977 Reduction of multiaxonal innervation at the neuromuscular junction of the rat during development. J. Physiol. 270, 299-310.
98. Rossi, F., Borsello, T., Vaudano, E. & Strata, P. 1993 Regressive modifications of climbing fibres following Purkinje cell degeneration in the cerebellar cortex of the adult rat. Neuroscience 53, 759-778. (doi:10.1016/0306-4522(93)90622-M)
99. Sagot, Y., Dubois-Dauphin, M., Tan, S. A., de Bilbao, F., Aebischer, P., Martinou, J. C. & Kato, A. C. 1995 Bcl-2 overexpression prevents motoneuron cell body loss but not axonal degeneration in a mouse model of a neurodegenerative disease. J. Neurosci. 15, 7727-7733.
100. Sahay, A., Molliver, M. E., Ginty, D. D. & Kolodkin, A. L. 2003 Semaphorin 3F is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events. J. Neurosci. 23, 6671-6680.
101. Sajadi, A., Schneider, B. L. & Aebischer, P. 2004 Wlds-mediated protection of dopaminergic fibers in an animal model of Parkinson disease. Curr. Biol. 14, 326-330. (doi:10.1016/S0960-9822(04)00050-8)
102. Sanes, J. R. & Lichtman, J. W. 1999 Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 22, 389-442. (doi:10.1146/annurev. neuro.22.1.389)
103. Schmalbruch, H., al-Amood, W. S. & Lewis, D. M. 1991a Morphology of long-term denervated rat soleus muscle and the effect of chronic electrical stimulation. J. Physiol. 441, 233-241.
104. Schmalbruch, H., Jensen, H. J., Bjaerg, M., Kamieniecka, Z. & Kurland, L. 1991b A new mouse mutant with progressive motor neuronopathy. J. Neuropathol. Exp. Neurol. 50, 192-204.
105. Segal, M. 2002 Changing views of Cajal's neuron: the case of the dendritic spine. Prog. Brain Res. 136, 101-107.
106. Shatz, C. J. 1977 Anatomy of interhemispheric connections in the visual system of Boston Siamese and ordinary cats. J. Comp. Neurol. 173, 497-518. (doi:10.1002/cne.901730307)
107. Singh, K. K. & Miller, F. D. 2005 Activity regulates positive and negative neurotrophin-derived signals to determine axon competition. Neuron 45, 837-845. (doi:10.1016/j.neuron.2005.01.049)
108. Stanfield, B. B. & O'Leary, D. D. 1985a Fetal occipital cortical neurones transplanted to the rostral cortex can extend and maintain a pyramidal tract axon. Nature 313, 135-137. (doi:10.1038/313135a0)
109. Stanfield, B. B. & O'Leary, D. D. 1985b The transient corticospinal projection from the occipital cortex during the postnatal development of the rat. J. Comp. Neurol. 238, 236-248. (doi:10.1002/cne.902380210)
110. Stanfield, B. B., O'Leary, D. D. & Fricks, C. 1982 Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones. Nature 298, 371-373. (doi:10.1038/298371a0)
111. Tessier-Lavigne, M. 2002 Wiring the brain: the logic and molecular mechanisms of axon guidance and regeneration. Harvey Lect. 98, 103-143.
112. Trachtenberg, J. T., Chen, B. E., Knott, G. W., Feng, G., Sanes, J. R., Welker, E. & Svoboda, K. 2002 Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420, 788-794. (doi:10.1038/nature01273)
113. Ullian, E. M., Christopherson, K. S. & Barres, B. A. 2004 Role for glia in synaptogenesis. Glia 47, 209-216. (doi:10.1002/glia.20082)
114. Voges, D., Zwickl, P. & Baumeister, W. 1999 The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68, 1015-1068. (doi:10.1146/annurev.biochem.68.1.1015)
115. Waller, A. 1850 Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations on the alterations produced thereby in the structure of their primitive fibers. Phil. Trans. R. Soc. B 140, 423-429.
116. Walsh, M. K. & Lichtman, J. W. 2003 In vivo time-lapse imaging of synaptic takeover associated with naturally occurring synapse elimination. Neuron 37, 67-73. (doi:10.1016/S0896-6273(02)01142-X)
117. Wang, J., Zhai, Q., Chen, Y., Lin, E., Gu, W., McBurney, M. W. & He, Z. 2005 A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol. 170, 349-355.
118. Watts, R. J., Hoopfer, E. D. & Luo, L. 2003 Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38, 871-885. (doi:10.1016/S0896-6273(03) 00295-2)
119. Watts, R. J., Schuldiner, O., Perrino, J., Larsen, C. & Luo, L. 2004 Glia engulf degenerating axons during developmental axon pruning. Curr. Biol. 14, 678-684. (doi:10.1016/j.cub.2004.03.035)
120. Weimann, J. M., Zhang, Y. A., Levin, M. E., Devine, W. P., Brulet, P. & McConnell, S. K. 1999 Cortical neurons require Otx1 for the refinement of exuberant axonal projections to subcortical targets. Neuron 24, 819-831. (doi:10.1016/S0896-6273(00)81030-2)
121. Williams, D. W. & Truman, J. W. 2004 Mechanisms of dendritic elaboration of sensory neurons in Drosophila: insights from in vivo time lapse. J. Neurosci. 24, 1541-1550. (doi:10.1523/JNEUROSCI.4521-03.2004)
122. Williams, D. W. & Truman, J. W. 2005a Remodeling dendrites during insect metamorphosis. J. Neurobiol. 64, 24-33. (doi:10.1002/neu.20151)
123. Williams, D. W. & Truman, J. W. 2005b Cellular mechanisms of dendrite pruning in Drosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons. Development 132, 3631-3642. (doi:10.1242/dev.01928)
124. Yanik, M. F., Cinar, H., Cinar, H. N., Chisholm, A. D., Jin, Y. & Ben-Yakar, A. 2004 Neurosurgery: functional regeneration after laser axotomy. Nature 432, 822. (doi:10.1038/432822a)
125. Yates, P. A., Roskies, A. L., McLaughlin, T. & O'Leary, D. D. 2001 Topographic-specific axon branching controlled by ephrin-As is the critical event in retinotectal map development. J. Neurosci. 21, 8548-8563.
126. Yates, P. A., Holub, A. D., McLaughlin, T., Sejnowski, T. J. & O'Leary, D. D. 2004 Computational modeling of retinotopic map development to define contributions of EphA-ephrinA gradients, axon-axon interactions, and patterned activity. J. Neurobiol. 59, 95-113. (doi:10.1002/neu.10341)
127. Yuan, J., Lipinski, M. & Degterev, A. 2003 Diversity in the mechanisms of neuronal cell death. Neuron 40, 401-413. (doi:10.1016/S0896- 6273(03)00601-9)
128. Yuste, R. & Bonhoeffer, T. 2001 Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 24, 1071-1089. (doi:10.1146/annurev.neuro.24.1.1071)
129. Zhai, Q., Wang, J., Kim, A., Liu, Q., Watts, R., Hoopfer, E., Mitchison, T., Luo, L. & He, Z. 2003 Involvement of the ubiquitin-proteasome system in the early stages of wallerian degeneration. Neuron 39, 217-225. (doi:10.1016/S0896-6273(03)00429-X)
130. Zheng, X., Wang, J., Haerry, T. E., Wu, A. Y., Martin, J., O'Connor, M. B., Lee, C. H. & Lee, T. 2003 TGF-beta signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell 112, 303-315. (doi:10.1016/S0092-8674(03)00072-2)
131. Zufferey, P. D., Jin, F., Nakamura, H., Tettoni, L. & Innocenti, G. M. 1999 The role of pattern vision in the development of cortico-cortical connections. Eur. J. Neurosci. 11, 2669-2688. (doi:10.1046/j.1460-9568.1999. 00683.x)
132. Zuo, Y., Lin, A., Chang, P. & Gan, W. B. 2005 Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46, 181-189. (doi:10.1016/j.neuron.2005.04.001)