Chapter 27 Neural Plasticity After Nerve Injury and Regeneration

International Review of Neurobiology

Volumn 87, Issue C, 2009, Pages 483-505

  Navarro, Xavier ^a,b  

^a INSTITUT DE NEUROCIÈNCIES   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; POTASSIUM CHANNEL KV1.1; VOLTAGE GATED SODIUM CHANNEL;

BRAIN REGION; BRAIN STEM; CENTRAL NERVOUS SYSTEM FUNCTION; CHANNEL GATING; EXCITATORY POSTSYNAPTIC POTENTIAL; MOTOR CONTROL; MOTOR CORTEX; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE FIBER TRANSECTION; NERVE PROJECTION; NERVE REGENERATION; NEUROPATHIC PAIN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REINNERVATION; REVIEW; SOMATOSENSORY CORTEX; SPINAL CORD; SPINAL REFLEX; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; THALAMUS; ANIMAL; BIOLOGICAL MODEL; BRAIN; CELL MEMBRANE POTENTIAL; CELL SURVIVAL; HUMAN; INJURY; METABOLISM; NERVE CELL; NERVE TRACT; PERIPHERAL NERVE; PHYSIOLOGY; REFLEX;

ANIMALS; BRAIN; CELL SURVIVAL; HUMANS; ION CHANNELS; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; MOTOR CORTEX; NERVE REGENERATION; NEURAL PATHWAYS; NEURONAL PLASTICITY; NEURONS; PERIPHERAL NERVES; REFLEX; SOMATOSENSORY CORTEX; SPINAL CORD;

EID: 70349785979     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0074-7742(09)87027-X     Document Type: Review

References (129)

1. Abdulla F.A., and Smith P.A. Axotomy- and autotomy-induced changes in the excitability of rat dorsal root ganglion neurons. J. Neurophysiol. 85 (2001) 630-643
2. Abernethy D.A., Rud A., and Thomas P.K. Neurotrophic influence of the distal stump of transected peripheral nerve on axonal regeneration: Absence of topographic specificity in adult nerve. J. Anat. 180 (1992) 395-400
3. Aldskogius H., Liu L., and Svensson M. Glial responses to synaptic damage and plasticity. J. Neurosci. Res. 58 (1999) 33-41
4. Bjorkman A., Rosén B., and Lundborg G. Enhanced function in nerve-injured hands after contralateral deafferentation. Neuroreport 16 (2005) 517-519
5. Bodine-Fowler S.C., Meyer R.S., Moscovitz A., Abrams R., and Botte J. Inaccurate projection of rat soleus motoneurons: A comparison of nerve repair techniques. Muscle Nerve 20 (1997) 29-37
6. Borke R.C., Curtis M., and Ginsberg C. Choline acetyltransferase and calcitonin gene-related peptide immunoreactivity in motoneurons after different types of nerve injury. J. Neurocytol. 22 (1993) 141-153
7. Bosse F., Hasenpusch-Theil K., Kury P., and Muller H.W. Gene expression profiling reveals that peripheral nerve regeneration is a consequence of both novel injury-dependent and reactivated developmental processes. J. Neurochem. 96 (2006) 1441-1457
8. Boyd J.G., and Gordon T. Neurotrophic factors and their receptors in axonal regeneration and functional recovery after peripheral nerve injury. Mol. Neurobiol. 27 (2003) 277-324
9. Brannstrom T., Havton L., and Kellerth J.O. Changes in size and dendritic arborization patterns of adult cat spinal alpha-motoneurons following permanent axotomy. J. Comp. Neurol. 318 (1992) 439-451
10. Brannstrom T., Havton L., and Kellerth J.O. Restorative effects of reinnervation on the size and dendritic arborization patterns of axotomized cat spinal alpha-motoneurons. J. Comp. Neurol. 318 (1992) 452-461
11. Brasil-Neto J.P., Cohen L.G., Pascual-Leone A., Jabir F.K., Wall R.T., and Hallett M. Rapid reversible modulation of human motor outputs after transient deafferentation of the forearm: A study with transcranial magnetic stimulation. Neurology 42 (1992) 1302-1306
12. Brown M.C., Holland R.L., and Ironton R. Nodal and terminal sprouting from motor nerves in fast and slow muscles in the mouse. J. Physiol. 306 (1980) 493-510
13. Brushart T.M. Motor axons preferentially reinnervate motor pathways. J. Neurosci. 13 (1993) 2730-2738
14. Calderó J., Casanovas A., Sorribas A., and Esquerda J.E. Calcitonin gene-related peptide in rat spinal cord motoneurons: Subcellular distribution and changes induced by axotomy. Neuroscience 48 (1992) 449-461
15. Cameron A.A., Vansant G., Wu W., Carlo D.J., and Ill C.R. Identification of reciprocally regulated gene modules in regenerating dorsal root ganglion neurons and activated peripheral or central nervous system glia. J. Cell. Biochem. 88 (2003) 970-985
16. Castro-Lopes J.M., Tavara I., and Coimbra A. GABA decreases in the spinal cord dorsal horn after peripheral neurectomy. Brain Res. 620 (1993) 287-291
17. Chen D.H. Qualitative and quantitative study of synaptic displacement in chromatolyzed spinal motoneurons of the cat. J. Comp. Neurol. 177 (1978) 635-664
18. Chen R., Corwell B., Yaseen Z., Hallet M., and Cohen L. Mechanisms of cortical reorganization in lower-limb amputees. J. Neurosci. 18 (1998) 3443-3450
19. Chen R., Cohen L.G., and Hallett M. Nervous system reorganization following injury. Neuroscience 111 (2002) 761-773
20. Churchill J.D., Arnold L.L., and Garraghty P.E. Somatotopic reorganization in the brainstem and thalamus following peripheral nerve injury in adult primates. Brain Res. 910 (2001) 142-152
21. Churchill J.D., Tharp J.A., Wellman C.L., Sengelaub D.R., and Garraghty P.E. Morphological correlates of injury-induced reorganization in primate somatosensory cortex. BMC Neurosci. 5 (2004) 43
22. Cohen L.G., Bandinelli S., Findley T.W., and Hallett M. Motor reorganization after upper limb amputation in man. Brain 114 (1991) 615-627
23. Cope T.C., Bonasera J., and Nichols T.R. Reinnervated muscles fail to produce stretch reflexes. J. Neurophysiol. 71 (1994) 817-820
24. Costigan M., Befort K., Karchewski L., Griffin R.S., D'Urso D., Allchorne A., Sitarski J., Mannion J.W., Pratt R.E., and Woolf C.J. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci. 3 (2002) 16
25. Dhillon G.S., Kruger T.B., Sandhu J.S., and Horch K.W. Effects of short-term training on sensory and motor function in severed nerves of long-term human amputees. J. Neurophysiol. 93 (2005) 2625-2633
26. Donoghue J.P., Suner S., and Sanes J.N. Dynamic organization of primary motor cortex output to target muscles in adult rats. II. Rapid reorganization following motor nerve lesions. Exp. Brain. Res. 79 (1990) 492-503
27. Field-Fote E.C. Electrical stimulation modifies spinal and cortical neural circuitry. Exerc. Sports Sci. Rev. 32 (2004) 155-160
28. Flor H., Elbert T., Muhlnickel W., Pantev C., Wienbruch C., and Taub E. Cortical reorganization and phantom phenomena in congenital and traumatic upper-extremity amputees. Exp. Brain Res. 119 (1998) 205-212
29. Florence S.L., Garraghty P.E., Wall J.T., and Kaas J.H. Sensory afferent projections and area 3b somatotopy following median nerve cut and repair in macaque monkeys. Cereb. Cortex 4 (1994) 391-407
30. Florence S.L., Taub H.B., and Kaas J.H. Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys. Science 282 (1998) 1117-1121
31. Florence S.L., Hackett T.A., and Strata F. Thalamic and cortical contributions to neural plasticity after limb amputation. J. Neurophysiol. 83 (2000) 3154-3159
32. Florence S.L., Boydston L.A., Hackett T.A., Lachoff H.T., Strata F., and Niblock M.M. Sensory enrichment after peripheral nerve injury restores cortical, not thalamic, receptive field organization. Eur. J. Neurosci. 13 (2001) 1755-1766
33. Fu S.Y., and Gordon T. The cellular and molecular basis of peripheral nerve regeneration. Mol. Neurobiol. 14 (1997) 67-116
34. Garraghty P.E., and Kaas J.H. Large-scale functional reorganization in adult monkey cortex after peripheral nerve injury. Proc. Natl. Acad. Sci. USA 88 (1991) 6976-6980
35. Garraghty P.E., and Muja N. NMDA receptors and plasticity in adult primate somatosensory cortex. J. Comp. Neurol. 367 (1996) 19-26
36. Giraux P., Sirigu A., Schneider F., and Dubernard J.M. Cortical reorganization in motor cortex after graft of both hands. Nat. Neurosci. 4 (2001) 691-692
37. Groves M.J., Christopherson T., Giometto B., and Scaravilli F. Axotomy-induced apoptosis in adult rat primary sensory neurons. J. Neurocytol. 26 (1997) 615-624
38. Hanz S., and Fainzilber M. Retrograde signalling in injured nerve: The axon reaction revisited. J. Neurochem. 99 (2006) 13-19
39. Havton L.A., and Kellerth J.O. Plasticity of lumbosacral monosynaptic reflexes after a ventral root transection injury in the adult cat. Exp. Brain Res. 155 (2004) 111-114
40. Hickmott P.W., and Steen P.A. Large-scale changes in dendritic structure during reorganization of adult somatosensory cortex. Nat. Neurosci. 8 (2005) 140-142
41. Holmberg P., and Kellerth J.O. Do synaptic rearrangements underlie compensatory reflex enhancement in spinal motoneurons after partial cell loss?. Synapse 38 (2000) 384-391
42. Hu J., Mata M., Hao S., Zhang G., and Fink D.J. Central sprouting of uninjured small fiber afferents in the adult rat spinal cord following spinal nerve ligation. Eur. J. Neurosci. 20 (2004) 1705-1712
43. Hughes D.I., Scott D.T., Todd A.J., and Riddell J.S. Lack of evidence for sprouting of Abeta afferents into the superficial laminas of the spinal cord dorsal horn after nerve section. J. Neurosci. 23 (2003) 9491-9499
44. Ishikawa K., Tanaka M., Black J.A., and Waxman S.G. Changes in expression of voltage-gated potassium channels in dorsal root ganglion neurons following axotomy. Muscle Nerve 22 (1999) 502-507
45. Iwahashi Y., Furuyama T., Inagaki S., Morita Y., and Takagi H. Distinct regulation of sodium channel types I, II and III following nerve transection. Brain Res. Mol. Brain Res. 22 (1994) 341-345
46. Jackson P.C., and Diamond J. Temporal and spatial constraints on the collateral sprouting of low-threshold mechanosensory nerves in the skin of rats. J. Comp. Neurol. 226 (1984) 336-345
47. Kaas J.H. Plasticity of sensory and motor maps in adult mammals. Annu. Rev. Neurosci. 14 (1991) 137-167
48. Kaas J.H. Is most of neural plasticity in the thalamus cortical?. Proc. Natl. Acad. Sci. USA 96 (1999) 7622-7623
49. Kaas J.H., and Collins C.E. Anatomic and functional reorganization of somatosensory cortex in mature primates after peripheral nerve and spinal cord injury. Adv. Neurol. 93 (2003) 87-95
50. Kline D.G., and Hudson A.R. Nerve Injuries: Operative Results for Major Nerve Injuries, Entrapments, and Tumors (1995), Saunders, Philadelphia
51. Koerber H.R., Mirnics K., and Lawson J.J. Synaptic plasticity in the adult spinal dorsal horn: The appearance of new functional connections following peripheral nerve regeneration. Exp. Neurol. 200 (2006) 468-479
52. Koliatsos V.E., Price W.L., Pardo C.A., and Price D.L. Ventral root avulsion: an experimental model of death of adult motor neurons. J. Comp. Neurol. 342 (1994) 35-44
53. Kreutzberg G.W. Reaction of the neuronal cell body to axonal damage. In: Waxman S.G., Kocsis J.D., and Stys P.K. (Eds). The Axon: Structure, Function and Pathophysiology (1995), Oxford University Press, Oxford 355-374
54. Krupa D.J., Ghazanfar A.A., and Nicolelis M.A. Immediate thalamic sensory plasticity depends on corticothalamic feedback. Proc. Natl. Acad. Sci. USA 96 (1999) 8200-8205
55. Kubo T., Yamashita T., Yamaguchi A., Hosokawa K., and Tohyama M. Analysis of genes induced in peripheral nerve after axotomy using cDNA microarrays. J. Neurochem. 82 (2002) 1129-1136
56. Kuno M., Miyata Y., and Muñoz-Martinez E.J. Differential reaction of fast and slow alpha-motoneurones to axotomy. J. Physiol. 240 (1974) 725-739
57. Lieberman A.R. The axon reaction: A review of the principal features of perikarial responses to axon injury. Int. Rev. Neurobiol. 14 (1971) 49-124
58. Lundborg G. A 25-year perspective of peripheral nerve surgery: Evolving neuroscientific concepts and clinical significance. J. Hand Surg. 25A (2000) 391-414
59. Lundborg G. Brain plasticity and hand surgery: An overview. J. Hand Surg. 25B (2000) 242-252
60. Lundborg G. Nerve Injury and Repair: Regeneration, Reconstruction, and Cortical Remodeling. 2nd ed. (2004), Elsevier, Philadelphia
61. Madison R.D., Archibald S.J., and Brushart T.M.E. Reinnervation accuracy of the rat femoral nerve by motor and sensory neurons. J. Neurosci. 16 (1996) 5698-5703
62. Mano Y., Chuma T., and Watanabe I. Cortical reorganization in training. J. Electromyogr. Kinesiol. 13 (2003) 57-62
63. Martin L.J., Kaiser A., and Price A.C. Motor neuron degeneration after sciatic nerve avulsion in adult rat evolves with oxidative stress and is apoptosis. J. Neurobiol. 40 (1999) 185-201
64. McGregor G.P., Gibson S.J., Sabate I.M., Blank M.A., Christofides N.D., Wall P.D., Polak J.M., and Bloom S.R. Effect of peripheral nerve section and nerve crush on spinal cord neuropeptides in the rat; increased VIP and PHI in the dorsal horn. Neuroscience 13 (1984) 207-216
65. Melzack R., Coderre T.J., Katz J., and Vaccarino A.L. Central neuroplasticity and pathological pain. Ann. NY Acad. Sci. 933 (2001) 157-174
66. Mendell L. Modifiability of spinal synapses. Physiol. Rev. 64 (1984) 260-324
67. Mendell L.M., and Munson J.B. Retrograde effects on synaptic transmission at the Ia/motoneuron connection. J. Physiol. (Paris) 93 (1999) 297-304
68. Merzenich M.M., Kaas J.H., Wall R.J., Nelson M., Sur D., and Felleman D. Topographic reorganization of somatosensory cortical areas 3B and 1 in adult monkeys following restricted deafferentation. Neuroscience 8 (1983) 33-55
69. Merzenich M.M., Kaas J.H., Wall R.J., Sur M., Nelson R.J., and Felleman D.J. Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 10 (1983) 639-665
70. Molander C., and Aldskogius H. Directional specificity of regenerating primary sensory neurons after peripheral nerve crush or transection and epineurial suture. A sequential double-labelling study in the rat. Restor. Neurol. Neurosci. 4 (1992) 339-344
71. Molander C., Wang H.F., Rivero-Melián C., and Grant G. Early decline and late restoration of spinal cord binding and transganglionic transport of isolectin B4 from Griffonia simplicifolia I after peripheral nerve transection or crush. Restor. Neurol. Neurosci. 10 (1996) 123-133
72. Moore K.A., Kohno T., Karchewski L.A., Scholz J., Baba H., and Woolf C.J. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J. Neurosci. 22 (2002) 6724-6731
73. Myers W.A., Churchill J.D., Muja N., and Garraghty P.E. Role of NMDA receptors in adult primate cortical somatosensory plasticity. J. Comp. Neurol. 418 (2000) 373-382
74. Navarro X., Vivó M., and Valero-Cabré A. Neural plasticity after peripheral nerve injury and regeneration. Progr. Neurobiol. 82 (2007) 163-201
75. Nicolelis M.A., Lin R.C., Woodward D.J., and Chapin J.K. Induction of immediate spatiotemporal changes in thalamic networks by peripheral block of ascending cutaneous information. Nature 361 (1993) 533-536
76. Patko T., Vassias I., Vidal P.P., and De Waele C. Modulation of the voltage-gated sodium- and calcium-dependent potassium channels in rat vestibular and facial nuclei after unilateral labyrinthectomy and facial nerve transection: An in situ hybridization study. Neuroscience 117 (2003) 265-280
77. Pearson P.P., Arnold P.B., Oladehin A., Li C.X., and Waters R.S. Large-scale cortical reorganization following forelimb deafferentation in rat does not involve plasticity of intracortical connections. Exp. Brain Res. 138 (2001) 8-25
78. Pearson P.P., Li C.X., Chappell T.D., and Waters R.S. Delayed reorganization of the shoulder representation in forepaw barrel subfield (FBS) in first somatosensory cortex (SI) following forelimb deafferentation in adult rats. Exp. Brain Res. 153 (2003) 100-112
79. Purves D. Functional and structural changes in mammalian sympathetic neurones following interruption of their axons. J. Physiol. 252 (1975) 429-463
80. Qi H.X., Stepniewska I., and Kaas J.H. Reorganization of primary motor cortex in adult macaque monkeys with long-standing amputations. J. Neurophysiol. 84 (2000) 2133-2147
81. Ramachandran V.S., and Hirstein W. The perception of phantom limbs. The D. O. Hebb lecture. Brain 121 (1998) 1603-1630
82. Röricht S., Machetanz J., Irlbacher K., Niehaus L., Biemer E., and Meyer B.U. Reorganization of human motor cortex after hand replantation. Ann. Neurol. 50 (2001) 240-249
83. Rose P.K., MacDermid V., and Neuber-Hess M. Structural plasticity of motoneuron dendrites caused by axotomy. In: Cope T.C. (Ed). Motor Neurobiology of the Spinal Cord (2001), CRC Press, Boca Raton, FL 251-270
84. Rosén B., and Lundborg G. Early use of artificial sensibility to improve sensory recovery after repair of the median and ulnar nerve. Scand. J. Plast. Reconstr. Surg. Hand Surg. 37 (2003) 54-57
85. Rosén B., Bjorkman A., and Lundborg G. Improved sensory relearning after nerve repair induced by selective temporary anaesthesia: A new concept in hand rehabilitation. J. Hand Surg. [Br.] 31 (2006) 126-132
86. Rosenkranz K., and Rothwell J.C. Differences between the effects of three plasticity inducing protocols on the organization of the human motor cortex. Eur. J. Neurosci. 23 (2006) 822-829
87. Rossini P.M., Martino G., Narici L., Pasquarelli A., Peresson M., Pizzela V., Tecchio F., Torrioli G., and Romani G.L. Short term brain plasticity in humans: Transient finger representation changes in sensory cortex somatotopy following ischemic anesthesia. Brain Res. 642 (1994) 169-177
88. Sanes J.N., Suner S., Lando J.F., and Donoghue J.P. Rapid reorganization of adult rat motor cortex somatic representation patterns after motor nerve injury. Proc. Natl. Acad. Sci. USA 85 (1988) 2003-2007
89. Sanes J.N., Suner S., and Donoghue J.P. Dynamic organization of primary motor cortex output to target muscles in adult rats. I. Long-term patterns of reorganization following motor or mixed peripheral nerve lesions. Exp. Brain. Res. 79 (1990) 479-491
90. Sanna P.P., Celio M., Bloom F., and Rende M. Presumptive Renshaw cells contain decreased calbindin during recovery from sciatic nerve lesions. Proc. Natl. Acad. Sci. USA 90 (1993) 3048-3052
91. Schady W., Braune S., Watson S., Torebjork H.E., and Schmidt R. Responsiveness of the somatosensory system after nerve injury and amputation in the human hand. Ann. Neurol. 36 (1994) 68-75
92. Scott J.J., and Panesar G. Small-signal sensitivity of muscle spindles reinnervated after long-term denervation. Brain Res. 671 (1995) 325-328
93. Seburn K.L., and Cope T.C. Short-term afferent axotomy increases both strength and depression at Ia-motoneuron synapses in rat. J. Neurosci. 18 (1998) 1142-1147
94. Sengelaub D.R., Muja N., Mills A.C., Myers W.A., Churchill J.D., and Garraghty P.E. Denervation-induced sprouting of intact peripheral afferents into the cuneate nucleus of adult rats. Brain Res. 769 (1997) 256-262
95. Shehab S.A., Spike R.C., and Todd A.J. Evidence against cholera toxin B subunit as a reliable tracer for sprouting of primary afferents following peripheral nerve injury. Brain Res. 964 (2003) 218-227
96. Shieh S.J., Chiu H.Y., and Hsu H.Y. Long-term effects of sensory reeducation following digital replantation and revascularization. Microsurgery 18 (1998) 334-336
97. Shortland P., and Woolf C.J. Chronic peripheral nerve section results in a rearrangement of the central axonal arborizations of axotomized A-beta primary afferent neurons in the rat spinal cord. J. Comp, Neurol. 330 (1993) 65-82
98. Sumner B.E.H., and Sunderland S. Quantitative electron microscopy on the injured hypoglossal nucleus in the rat. J. Neurocytol. 2 (1973) 315-328
99. Sunderland S. Nerve Injuries and Their Repair. A Critical Appraisal (1991), Churchill Livingstone, Edinburgh
100. Terenghi G. Peripheral nerve regeneration and neurotrophic factors. J. Anat. 194 (1999) 1-14
101. Titmus M.J., and Faber D.S. Axotomy-induced alterations in the electrophysiological characteristics of neurons. Prog. Neurobiol. 35 (1990) 1-51
102. Valero-Cabré A., and Navarro X. H reflex restitution and facilitation after different types of peripheral nerve injury and repair. Brain Res. 919 (2001) 302-312
103. Valero-Cabré A., and Navarro X. Functional impact of axonal misdirection after peripheral nerve injuries followed by graft or tube repair. J. Neurotrauma 19 (2002) 1475-1485
104. Valero-Cabré A., and Navarro X. Changes in crossed spinal reflexes after peripheral nerve injury and repair. J. Neurophysiol. 87 (2002) 1763-1771
105. Valero-Cabré A., Tsironis K., Skouras E., Perego G., Navarro X., and Neiss W.F. Superior muscle reinnervation after autologous nerve graft or poly-l-lactide-ε{lunate}-caprolactone (PLC) tube implantation in comparison to silicone tube repair. J. Neurosci. Res. 63 (2001) 214-223
106. Valero-Cabré A., Tsironis K., Skouras E., Navarro X., and Neiss W.F. Peripheral and spinal motor reorganization after nerve injury and repair. J. Neurotrauma 21 (2004) 95-108
107. Vanden-Noven S., Wallace N., Muccio D., Turtz A., and Pinter M.J. Adult spinal motoneurons remain viable despite prolonged absence of functional synaptic contact with muscle. Exp. Neurol. 123 (1993) 147-156
108. Verdú E., and Navarro X. Comparison of immunohistochemical and functional reinervation of skin and muscle after peripheral nerve injury. Exp. Neurol. 146 (1997) 187-198
109. Verdú E., and Navarro X. The role of Schwann cell in nerve regeneration. In: Castellano B., González B., and Nieto-Sampedro M. (Eds). Understanding Glial Cells (1998), Kluwer Academic, Boston 319-359
110. Villar M.J., Wiesenfeld-Hallin Z., Xu X.J., Theodorsson E., Emson P.C., and Hökfelt T. Further studies on galanin-, substance P-, and CGRP-like immunoreactivities in primary sensory neurons and spinal cord: Effects of dorsal rhizotomies and sciatic nerve lesions. Exp. Neurol. 112 (1991) 29-39
111. Vivó M., Puigdemasa A., Casals L., Asensio E., Udina E., and Navarro X. Immediate electrical stimulation enhances regeneration and reinnervation and modulates spinal plastic changes after sciatic nerve injury and repair. Exp. Neurol. 211 (2008) 180-193
112. Wakisaka S., Kajander K.C., and Bennett G.J. Increased neuropeptide (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci. Lett. 124 (1991) 200-203
113. Wall J.T., and Cusick C.G. Cutaneous responsiveness in primary somatosensory (S-I) hindpaw cortex before and after partial hindpaw deafferentation in adult rats. J. Neurosci. 4 (1984) 1499-1515
114. Wall J.T., Felleman D.J., and Kaas J.H. Recovery of normal topography in the somatosensory cortex of monkeys after nerve crush and regeneration. Science 221 (1983) 771-773
115. Wall J.T., Kaas J.H., Sur M., Nelson R.J., Fellman D.J., and Merzenich M.M. Functional reorganization in somatosensory cortical areas 3b and 1 of adult monkeys after median nerve repair: Possible relationships to sensory recovery in humans. J. Neurosci. 6 (1986) 218-233
116. Wall J.T., Xu J., and Wang X. Human brain plasticity: an emerging view of the multiple substrates and mechanisms that cause cortical changes and related sensory dysfunctions after injuries of sensory inputs from the body. Brain Res. Rev. 39 (2002) 181-215
117. Waxman S.G., Cummins T.R., Dib-Hajj S.D., and Black J.A. Voltage-gated sodium channels and the molecular pathogenesis of pain: A review. J. Rehabil. Res. Dev. 37 (2000) 517-528
118. Wood J.N., Boorman J.P., Okuse K., and Baker M.D. Voltage-gated sodium channels and pain pathways. J. Neurobiol. 61 (2004) 55-71
119. Woods T.M., Cusick C.G., Pons T.P., Taub E., and Jones E.G. Progressive transneuronal changes in the brainstem and thalamus after long-term dorsal rhizotomies in adult macaque monkeys. J. Neurosci. 20 (2000) 3884-3899
120. Woolf C.J., and Salter M.W. Neuronal plasticity: Increasing the gain in pain. Science 288 (2000) 1765-1768
121. Woolf C.J., Shortland P., Reynolds M., Ridings J., Doubell T., and Coggeshall R.E. Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J. Comp. Neurol. 360 (1995) 121-131
122. Wu C.W.H., and Kaas J.H. Reorganization in primary motor cortex of primates with long-standing therapeutic amputations. J. Neurosci. 19 (1999) 7679-7697
123. Xu J., and Wall J.T. Rapid changes in brainstem maps of adult primates after peripheral injury. Brain Res. 774 (1997) 211-215
124. Xu J., and Wall J.T. Functional organization of tactile inputs from the hand in the cuneate nucleus and its relationship to organization in the somatosensory cortex. J. Comp. Neurol. 411 (1999) 369-389
125. Yang Y., Xie Y., Chai H., Fan M., Liu S., Liu H., Bruce I., and Wu W. Microarray analysis of gene expression patterns in adult spinal motoneurons after different types of axonal injuries. Brain Res. 1075 (2006) 1-12
126. Ygge J. Neuronal loss in lumbar dorsal root ganglia after proximal compared to distal sciatic nerve resection: A quantitative study in the rat. Brain Res. 478 (1989) 193-195
127. Zhang J.M., Donnelly D.F., Song X.J., and Lamotte R.H. Axotomy increases the excitability of dorsal root ganglion cells with unmyelinated axons. J. Neurophysiol. 78 (1997) 2790-2794
128. Zhao P., Waxman S.G., and Hains B.C. Sodium channel expression in the ventral posterolateral nucleus of the thalamus after peripheral nerve injury. Mol. Pain 2 (2006) 27
129. Zigmond R.E. LIF, NGF, and the cell body response to axotomy. Neuroscientist 3 (1997) 176-185