Brief electrical stimulation accelerates axon regeneration in the peripheral nervous system and promotes sensory axon regeneration in the central nervous system

Motor Control

Volumn 13, Issue 4, 2009, Pages 412-441

  Gordon, Tessa ^a   Udina, Esther ^a   Verge, Valerie M K ^b   Posse De Chaves, Elena I ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Muscle function; Neuromuscular disease; Neurophysiology; Neuroscience

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENZYME INHIBITOR; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; NEUROMODULIN; NEUROTROPHIC FACTOR; ROLIPRAM; SQ 22356; UNCLASSIFIED DRUG;

CENTRAL NERVOUS SYSTEM; ELECTROSTIMULATION; FEMORAL NERVE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOTONEURON; MUSCLE DENERVATION; MUSCLE REINNERVATION; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NERVE INJURY; NERVE TRANSECTION; NONHUMAN; PERIPHERAL NERVE INJURY; PERIPHERAL NERVOUS SYSTEM; PROTEIN EXPRESSION; REVIEW; SCHWANN CELL; TIBIAL NERVE;

EID: 70349782014     PISSN: 10871640     EISSN: 15432696     Source Type: Journal    
DOI: 10.1123/mcj.13.4.412     Document Type: Review

References (151)

1. Aglah, C., Gordon, T., & Posse De Chaves, E.I. (2008). cAMP promotes neurite outgrowth and extension through protein kinase A but independently of Erk activation in cultured rat motoneurons. Neuropharmacology, 55, 8-17.
2. Aitken, J.T., Sharman, M., & Young, J.Z. (1947). Maturation of peripheral nerve fibres with various peripheral connections. Journal of Anatomy, 81, 1-22.
3. Al-Majed, A.A., Brushart, T.M., & Gordon, T. (2000). Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons. The European Journal of Neuroscience, 12, 4381-4390.
4. Al-Majed, A.A., Neumann, C.M., Brushart, T.M., & Gordon, T. (2000). Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. The Journal of Neuroscience, 20, 2602-2608.
5. Al-Majed, A.A., Tam, S.L., & Gordon, T. (2004). Electrical stimulation accelerates and enhances expression of regeneration-associated genes in regenerating rat femoral motoneurons. Cellular and Molecular Neurobiology, 24, 379-402.
6. Bandtlow, C.E. (2003). Regeneration in the central nervous system. Experimental Gerontology, 38, 79-86.
7. Berdan, R.C., Easaw, J.C., & Wang, R. (1993). Alterations in membrane potential after axotomy at different distances from the soma of an identified neuron and the effect of depolarization on neurite outgrowth and calcium channel expression. Journal of Neurophysiology, 69, 151-164.
8. Bisby, M.A. (1980). Changes in the composition of labeled protein transported in motor axons during their regeneration. Journal of Neurobiology, 11, 435-445.
9. Bisby, M.A., & Keen, P. (1984). A Conditioning Lesion Increases Regeneration Rate of Rat Sciatic-Nerve Axons Containing Substance-P. Journal of Physiology-London, 354, 56.
10. Bisby, M.A., & Pollock, B. (1983). Increased regeneration rate in peripheral-nerve axons following double lesions - Enhancement of the conditioning lesion phenomenon. Journal of Neurobiology, 14, 467-472.
11. Bisby, M.A., & Tetzlaff, W. (1992). Changes in cytoskeletal protein synthesis following axon injury and during axon regeneration. Molecular Neurobiology, 6, 107-123.
12. Blenk, K.H., Janig, W., Michaelis, M., & Vogel, C. (1996). Prolonged injury discharge in unmyelinated nerve fibres following transection of the sural nerve in rats. Neuroscience Letters, 215, 185-188. (Pubitemid 26323457)
13. Boyd, J.G., & Gordon, T. (2001). The neurotrophin receptors, trkB and p75, differentially regulate motor axonal regeneration. Journal of Neurobiology, 49, 314-325.
14. Boyd, J.G., & Gordon, T. (2002). A dose-dependent facilitation and inhibition of peripheral nerve regeneration by brain-derived neurotrophic factor. The European Journal of Neuroscience, 15, 613-626. (Pubitemid 35471930)
15. Boyd, J.G., & Gordon, T. (2003a). Glial cell line-derived neurotrophic factor and brainderived neurotrophic factor sustain the axonal regeneration of chronically axotomized motoneurons in vivo. Experimental Neurology, 183, 610-619. (Pubitemid 37205103)
16. Boyd, J.G., & Gordon, T. (2003b). Neurotrophic factors and their receptors in axonal regeneration and functional recovery after peripheral nerve injury. Molecular Neurobiology, 27, 277-324.
17. Brushart, T.M. (1988). Preferential reinnervation of motor nerves by regenerating motor axons. The Journal of Neuroscience, 8, 1026-1031. (Pubitemid 18085168)
18. Brushart, T.M. (1993). Motor axons preferentially reinnervate motor pathways. The Journal of Neuroscience, 13, 2730-2738.
19. Brushart, T.M., Gerber, J., Kessens, P., Chen, Y.G., & Royall, R.M. (1998). Contributions of pathway and neuron to preferential motor reinnervation. The Journal of Neuroscience, 18, 8674-8681. (Pubitemid 28491733)
20. Brushart, T.M., Hoffman, P.N., Royall, R.M., Murinson, B.B., Witzel, C., & Gordon, T. (2002). Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron. The Journal of Neuroscience, 22, 6631-6638. (Pubitemid 35386419)
21. Brushart, T.M., Jari, R., Verge, V., Rohde, C., & Gordon, T. (2005). Electrical stimulation restores the specificity of sensory axon regeneration. Experimental Neurology, 194, 221-229. (Pubitemid 40719757)
22. Brushart, T.M., & Mesulam, M.M. (1980). Transganglionic demonstration of central sensory projections from skin and muscle with HRP-lectin conjugates. Neuroscience Letters, 17, 1-6.
23. Bulsara, K.R., Iskandar, B.J., Villavicencio, A.T., & Skene, J.H. (2002). A new millenium for spinal cord regeneration: growth-associated genes. Spine, 27, 1946-1949.
24. Bunge, M.B., & Pearse, D.D. (2003). Transplantation strategies to promote repair of the injured spinal cord. Journal of Rehabilitation Research and Development, 40, 55-62.
25. Busch, S.A., & Silver, J. (2007). The role of extracellular matrix in CNS regeneration. Current Opinion in Neurobiology, 17, 120-127.
26. Cai, D., Qiu, J., Cao, Z., McAtee, M., Bregman, B.S., & Filbin, M.T. (2001). Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. The Journal of Neuroscience, 21, 4731-4739. (Pubitemid 32565631)
27. Cajal, S.R. (1928). Degeneration and Regeneration of the Nervous System (May, R.M. (trans.)). New York, Oxford: Oxford University Press.
28. Cao, Z., Qiu, J., Domeniconi, M., Hou, J., Bryson, J.B., Mellado, W., et al. (2007). The inhibition site on myelin-associated glycoprotein is within Ig-domain 5 and is distinct from the sialic acid binding site. The Journal of Neuroscience, 27, 9146-9154. (Pubitemid 47312053)
29. Carlsen, R.C. (1982). Comparison of adenylate cyclase activity in segments of rat sciatic nerve with a condition/test or test lesion. Experimental Neurology, 77, 254-265.
30. Caroni, P. (1997). Intrinsic neuronal determinants that promote axonal sprouting and elongation. BioEssays, 19, 767-775. (Pubitemid 27383752)
31. Chong, M.S., Fitzgerald, M., Winter, J., Hutsai, M., Emson, P.C., Wiese, U., et al. (1992). Gap-43 Messenger-RNA in Rat Spinal-Cord and Dorsal-Root Ganglia Neurons - Developmental-Changes and Reexpression Following Peripheral-Nerve Injury. The European Journal of Neuroscience, 4, 883-895.
32. Chong, M.S., Reynolds, M.L., Irwin, N., Coggeshall, R.E., Emson, P.C., Benowitz, L.I., et al. (1994). Gap-43 Expression in Primary Sensory Neurons Following Central Axotomy. The Journal of Neuroscience, 14, 4375-4384. (Pubitemid 24200559)
33. Chung, J.M., Leem, J.W., & Kim, S.H. (1992). Somatic afferent fibers which continuously discharge after being isolated from their receptors. Brain Research, 599, 29-33.
34. DeBellard, M.E., Tang, S., Mukhopadhyay, G., Shen, Y.J., & Filbin, M.T. (1996). Myelinassociated glycoprotein inhibits axonal regeneration from a variety of neurons via interaction with a sialoglycoprotein. Molecular and Cellular Neurosciences, 7, 89-101. (Pubitemid 26147289)
35. Diamond, J., Coughlin, M., Macintyre, L., Holmes, M., & Visheau, B. (1987). Evidence that endogenous beta nerve growth factor is responsible for the collateral sprouting, but not the regeneration, of nociceptive axons in adult rats. Proceedings of the National Academy of Sciences of the United States of America, 84, 6596-6600.
36. Eberhardt, K.A., Irintchev, A., Al-Majed, A.A., Simova, O., Brushart, T.M., Gordon, T., et al. (2006). BDNF/TrkB signaling regulates HNK-1 carbohydrate expression in regenerating motor nerves and promotes functional recovery after peripheral nerve repair. Experimental Neurology, 198, 500-510.
37. Elder, G.A., Friedrich, V.L., Jr., & Lazzarini, R.A. (2001). Schwann cells and oligodendrocytes read distinct signals in establishing myelin sheath thickness. Journal of Neuroscience Research, 65, 493-499.
38. English, A.W., Meador, W., & Carrasco, D.I. (2005). Neurotrophin-4/5 is required for the early growth of regenerating axons in peripheral nerves. The European Journal of Neuroscience, 21, 2624-2634. (Pubitemid 40835106)
39. English, A.W., Schwartz, G., Meador, W., Sabatier, M.J., & Mulligan, A. (2007). Electrical stimulation promotes peripheral axon regeneration by enhanced neuronal neurotrophin signaling. Developmental Neurobiology, 67, 158-172. (Pubitemid 46256799)
40. Fawcett, J.W. (2006). Overcoming inhibition in the damaged spinal cord. Journal of Neurotrauma, 23, 371-383. (Pubitemid 43739277)
41. Fenrich, K., & Gordon, T. (2004). Canadian Association of Neuroscience review: axonal regeneration in the peripheral and central nervous systems-current issues and advances. The Canadian Journal of Neurological Sciences, 31, 142-156. (Pubitemid 38724806)
42. Ferraro, G.B., Alabed, Y.Z., & Fournier, A.E. (2004). Molecular targets to promote central nervous system regeneration. Current Neurovascular Research, 1, 61-75.
43. Filbin, M.T. (2003). Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nature Reviews. Neuroscience, 4, 703-713. (Pubitemid 37280150)
44. Filbin, M.T. (2006). Recapitulate development to promote axonal regeneration: good or bad approach? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 361, 1565-1574.
45. Fitch, M.T., & Silver, J. (2008). CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Experimental Neurology, 209, 294-301.
46. Ford, L.E., Huxley, A.F., & Simmons, R.M. (1977). Tension responses to sudden length change in stimulated frog muscle fibres near slack length. The Journal of Physiology, 269, 441-515.
47. Forman, D.S., & Berenberg, R.A. (1978). Regeneration of motor axons in the rat sciatic nerve studied by labeling with axonally transported radioactive proteins. Brain Research, 156, 213-225.
48. Fouad, K., & Pearson, K. (2004). Restoring walking after spinal cord injury. Progress in Neurobiology, 73, 107-126. (Pubitemid 38759892)
49. Franz, C.K., Rutishauser, U., & Rafuse, V.F. (2008). Intrinsic neuronal properties control selective targeting of regenerating motoneurons. Brain, 131, 1492-1505. (Pubitemid 351806451)
50. Fry, E.J., Ho, C., & David, S. (2007). A role for Nogo receptor in macrophage clearance from injured peripheral nerve. Neuron, 53, 649-662. (Pubitemid 46283376)
51. Fu, S.Y., & Gordon, T. (1995a). Contributing factors to poor functional recovery after delayed nerve repair: prolonged axotomy. The Journal of Neuroscience, 15, 3876-3885.
52. Fu, S.Y., & Gordon, T. (1995b). Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. The Journal of Neuroscience, 15, 3886-3895.
53. Fu, S.Y., & Gordon, T. (1997). The cellular and molecular basis of peripheral nerve regeneration. Molecular Neurobiology, 14, 67-116. (Pubitemid 127720197)
54. Furey, M.J., Midha, R., Xu, Q.G., Belkas, J., & Gordon, T. (2007). Prolonged target deprivation reduces the capacity of injured motoneurons to regenerate. Neurosurgery, 60, 723-732. (Pubitemid 46581132)
55. Geremia, N.M., Gordon, T., Brushart, T.M., Al-Majed, A.A., & Verge, V.M. (2007). Electrical stimulation promotes sensory neuron regeneration and growth-associated gene expression. Experimental Neurology, 205, 347-359. (Pubitemid 46766600)
56. Gonzenbach, R.R., & Schwab, M.E. (2008). Disinhibition of neurite growth to repair the injured adult CNS: focusing on Nogo. Cellular and Molecular Life Sciences, 65, 161-176.
57. Gordon, T. (1983). Dependence of peripheral nerves on their target organs. In Burnstock, G., & O'Brien, R., & Vrbova, G. (Eds.), Somatic and autonomic nerve-muscle interactions (1 ed., pp. 289-316). Amsterdam: Elsevier.
58. Gordon, T., Boyd, J.G., & Sulaiman, O.A.R. (2005). Experimental approaches to promote functional recovery after severe peripheral nerve injuries. European Surgery, 37, 193-203.
59. Gordon, T., Brushart, T.M., Amirjani, N., & Chan, K.M. (2007). The potential of electrical stimulation to promote functional recovery after peripheral nerve injury-comparisons between rats and humans. Acta Neurochirurgica. Supplementum, 100, 3-11.
60. Gordon, T., Chan, K.M., Sulaiman, O.A.R., Udina, E., Amirjani, N., & Brushart, T.M. (2009).Accelerating axon growth to overcome limitations in functional recovery after peripheral nerve injury. Neurosurgery, in press.
61. Gordon, T., Gillespie, J., Orozco, R., & Davis, L. (1991). Axotomy-induced changes in rabbit hindlimb nerves and the effects of chronic electrical stimulation. The Journal of Neuroscience, 11, 2157-2169.
62. Gordon, T., Sulaiman, O.A.R., & Boyd, J.G. (2003). Experimental strategies to promote functional recovery after peripheral nerve injuries. Journal of the Peripheral Nervous System, 8, 236-250. (Pubitemid 37553739)
63. Grados-Munro, E.M., & Fournier, A.E. (2003). Myelin-associated inhibitors of axon regeneration. Journal of Neuroscience Research, 74, 479-485.
64. Grimpe, B., Pressman, Y., Lupa, M.D., Horn, K.P., Bunge, M.B., & Silver, J. (2005). The role of proteoglycans in Schwann cell/astrocyte interactions and in regeneration failure at PNS/CNS interfaces. Molecular and Cellular Neurosciences, 28, 18-29. (Pubitemid 39656008)
65. Gutmann, E., Guttmann, L., Medawar, P.B., & Young, J.Z. (1942). The rate of regeneration of nerve. The Journal of Experimental Biology, 19, 14-44.
66. Gutmann, E., & Young, J.Z. (1944). The re-innervation of muscle after various periods of atrophy. Journal of Anatomy, 78, 15-44.
67. Hall, S.M. (1999). The biology of chronically denervated Schwann cells. Ann.N.Y. Acad. Sci., 883, 215-233.
68. Hannila, S.S., & Filbin, M.T. (2007). The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp. Neurol.
69. Hannila, S.S., Siddiq, M.M., & Filbin, M.T. (2007). Therapeutic approaches to promoting axonal regeneration in the adult Mammalian spinal cord. International Review of Neurobiology, 77, 57-105.
70. Harvey, P.J., Grochmal, J., Tetzlaff, W., Gordon, T., & Bennett, D.J. (2005). An investigation into the potential for activity-dependent regeneration of the rubrospinal tract after spinal cord injury. The European Journal of Neuroscience, 22, 3025-3035. (Pubitemid 43001986)
71. Hoke, A., Redett, R., Hameed, H., Jari, R., Zhou, C., Li, Z.B., et al. (2006). Schwann cells express motor and sensory phenotypes that regulate axon regeneration. The Journal of Neuroscience, 26, 9646-9655. (Pubitemid 44427703)
72. Holmquist, B., Kanje, M., Kerns, J.M., & Danielsen, N. (1993). A mathematical model for regeneration rate and initial delay following surgical repair of peripheral nerves. Journal of Neuroscience Methods, 48, 27-33. (Pubitemid 23245425)
73. Hunt, D., Coffin, R.S., & Anderson, P.N. (2002). The Nogo receptor, its ligands and axonal regeneration in the spinal cord; a review. Journal of Neurocytology, 31, 93-120. (Pubitemid 36801786)
74. Kenney, A.M., & Kocsis, J.D. (1998). Peripheral axotomy induces long-term c-Jun aminoterminal kinase-1 activation and activator protein-1 binding activity by c-Jun and junD in adult rat dorsal root ganglia In vivo. The Journal of Neuroscience, 18, 1318-1328.
75. Kilmer, S.L., & Carlsen, R.C. (1984). Forskolin activation of adenylate cyclase in vivo stimulates nerve regeneration. Nature, 307, 455-457. (Pubitemid 14132059)
76. Kline, D.G., & Hudson, A.R. (1995). Nerve Injuries: Operative Results for Major Nerve Injuries, Entrapments and Tumors. Philadelphia: W.B. Saunders.
77. Kobayashi, N.R., Bedard, A.M., Hincke, M.T., & Tetzlaff, W. (1996). Increased expression of BDNF and trkB mRNA in rat facial motoneurons after axotomy. The European Journal of Neuroscience, 8, 1018-1029.
78. Korshunova, I., Caroni, P., Kolkova, K., Berezin, V., Bock, E., & Walmod, P. S. (2008). Characterization of BASP1-mediated neurite outgrowth. The Journal of Neuroscience Research.
79. Lankford, K.L., Waxman, S.G., & Kocsis, J.D. (1998). Mechanisms of enhancement of neurite regeneration in vitro following a conditioning sciatic nerve lesion. The Journal of Comparative Neurology, 391, 11-29.
80. Lehmann, M., Fournier, A., Selles-Navarro, I., Dergham, P., Sebok, A., Leclerc, N., et al. (1999). Inactivation of Rho signaling pathway promotes CNS axon regeneration. The Journal of Neuroscience, 19, 7537-7547. (Pubitemid 29404610)
81. Li, H., Terenghi, G., & Hall, S.M. (1997). Effects of delayed re-innervation on the expression of c-erbB receptors by chronically denervated rat Schwann cells in vivo. Glia, 20, 333-347. (Pubitemid 27335751)
82. Liu, B.P., Fournier, A., GrandPre, T., & Strittmatter, S.M. (2002). Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science, 297, 1190-1193. (Pubitemid 36193355)
83. Lu, P., & Tuszynski, M.H. (2008). Growth factors and combinatorial therapies for CNS regeneration. Experimental Neurology, 209, 313-320. (Pubitemid 351174138)
84. Mackinnon, S.E., Dellon, A.L., & O'Brien, J.P. (1991). Changes in nerve fiber numbers distal to a nerve repair in the rat sciatic nerve model. Muscle & Nerve, 14, 1116-1122.
85. Mason, M.R., Lieberman, A.R., Grenningloh, G., & Anderson, P.N. (2002). Transcriptional upregulation of SCG10 and CAP-23 is correlated with regeneration of the axons of peripheral and central neurons in vivo. Molecular and Cellular Neurosciences, 20, 595-615.
86. McLean, W.G. (1985). Axonal transport of actin and regeneration rate in non-myelinated sensory nerve fibres. Brain Research, 333, 255-260.
87. McPhail, L.T., Fernandes, K.J., Chan, C.C., Vanderluit, J.L., & Tetzlaff, W. (2004). Axonal reinjury reveals the survival and re-expression of regeneration-associated genes in chronically axotomized adult mouse motoneurons. Experimental Neurology, 188, 331-340.
88. McQuarrie, I.G., Grafstein, B., & Gershon, M.D. (1977). Axonal regeneration in the rat sciatic nerve: effect of a conditioning lesion and of dbcAMP. Brain Research, 132, 443-453. (Pubitemid 8166017)
89. McQuarrie, I.G., & Lasek, R.J. (1989). Transport of cytoskeletal elements from parent axons into regenerating daughter axons. The Journal of Neuroscience, 9, 436-446.
90. Mearow, K.M., Kril, Y., Gloster, A., & Diamond, J. (1994). Expression of NGF receptor and GAP-43 mRNA in DRG neurons during collateral sprouting and regeneration of dorsal cutaneous nerves. Journal of Neurobiology, 25, 127-142. (Pubitemid 24029379)
91. Meiri, K.F., Pfenninger, K.H., & Willard, M.B. (1986). Growth-associated protein, GAP- 43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proceedings of the National Academy of Sciences of the United States of America, 83, 3537-3541.
92. Mesulam, M.M., & Brushart, T.M. (1979). Transganglionic and anterograde transport of horseradish peroxidase across dorsal root ganglia: a tetramethylbenzidine method for tracing central sensory connections of muscles and peripheral nerves. Neuroscience, 4, 1107-1117.
93. Miller, F.D., Tetzlaff, W., Bisby, M.A., Fawcett, J.W., & Milner, R.J. (1989). Rapid induction of the major embryonic alpha-tubulin mRNA, T alpha 1, during nerve regeneration in adult rats. The Journal of Neuroscience, 9, 1452-1463. (Pubitemid 19116763)
94. Moon, L., & Bunge, M.B. (2005). From animal models to humans: strategies for promoting CNS axon regeneration and recovery of limb function after spinal cord injury. Journal of Neurologic Physical Therapy; JNPT, 29, 55-69.
95. Mukhopadhyay, G., Doherty, P., Walsh, F.S., Crocker, P.R., & Filbin, M.T. (1994). A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron, 13, 757-767. (Pubitemid 24300179)
96. 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. (Pubitemid 34722279)
97. Neumann, S., Skinner, K., & Basbaum, A.I. (2005). Sustaining intrinsic growth capacity of adult neurons promotes spinal cord regeneration. Proceedings of the National Academy of Sciences of the United States of America, 102, 16848-16852. (Pubitemid 41688865)
98. Neumann, S., & Woolf, C.J. (1999). Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron, 23, 83-91. (Pubitemid 29262466)
99. Nix, W.A., & Hopf, H.C. (1983). Electrical stimulation of regenerating nerve and its effect on motor recovery. Brain Research, 272, 21-25.
100. Noble, J., Munro, C.A., Prasad, V.S., & Midha, R. (1998). Analysis of upper and lower extremity peripheral nerve injuries in a population of patients with multiple injuries. The Journal of Trauma, 45, 116-122.
101. Obouhova, G., Clowry, G.J., & Vrbova, G. (1994). Changes in retrogradely labelled neurones in the red nucleus and cortex after depletion of motoneurones by axotomy in neonatal rats. Developmental Neuroscience, 16, 34-37. (Pubitemid 24330186)
102. Pearse, D.D., Pereira, F.C., Marcillo, A.E., Bates, M.L., Berrocal, Y.A., Filbin, M.T., et al. (2004). cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nature Medicine, 10, 610-616.
103. Pettersson, L. M. E., Gordon, T., Tyreman, N., & Verge, V. M. K. (2006). The role of injury discharge in induction of injury-associated GAP-43 expression in sensory neurons. Social Neuroscience, 31, 323-326.
104. Pockett, S. & Gavin, R. M. (1985). Acceleration of peripheral nerve regeneration after crush injury in rat. Neuroscience Letters, 59, 221-224. (Pubitemid 15239690)
105. Qiu, J., Cai, D., Dai, H., McAtee, M., Hoffman, P.N., Bregman, B.S., et al. (2002). Spinal axon regeneration induced by elevation of cyclic AMP. Neuron, 34, 895-903. (Pubitemid 34722280)
106. Qiu, J., Cai, D., & Filbin, M.T. (2002). A role for cAMP in regeneration during development and after injury. Progress in Brain Research, 137, 381-387. (Pubitemid 35460957)
107. Redett, R., Jari, R., Crawford, T., Chen, Y.G., Rohde, C., & Brushart, T.M. (2005). Peripheral pathways regulate motoneuron collateral dynamics. The Journal of Neuroscience, 25, 9406-9412. (Pubitemid 41464753)
108. Richardson, P.M., & Issa, V.M. (1984). Peripheral injury enhances central regeneration of primary sensory neurones. Nature, 309, 791-793.
109. Richardson, P.M., Issa, V.M., & Aguayo, A.J. (1984). Regeneration of long spinal axons in the rat. Journal of Neurocytology, 13, 165-182.
110. Richardson, P.M., & Verge, V.M. (1986). The induction of a regenerative propensity in sensory neurons following peripheral axonal injury. Journal of Neurocytology, 15, 585-594.
111. Richardson, P.M., & Verge, V.M. (1987). Axonal regeneration in dorsal spinal roots is accelerated by peripheral axonal transection. Brain Research, 411, 406-408.
112. Richmond, F.J.R., Gladdy, R., Crasy, J.L., Kitamura, S., Smits, E., & Thomson, D.B. (1994). Efficacy of seven retrograde tracers, compared in multiple-labelling studies of feline motoneurones. Journal of Neuroscience Methods, 53, 35-46. (Pubitemid 24238749)
113. Schwab, M.E. (2004). Nogo and axon regeneration. Current Opinion in Neurobiology, 14, 118-124.
114. Shen, Y.J., DeBellard, M.E., Salzer, J.L., Roder, J., & Filbin, M.T. (1998). Myelin-associated glycoprotein in myelin and expressed by Schwann cells inhibits axonal regeneration and branching. Molecular and Cellular Neurosciences, 12, 79-91. (Pubitemid 28524292)
115. Silver, J., & Miller, J.H. (2004). Regeneration beyond the glial scar. Nature Reviews. Neuroscience, 5, 146-156.
116. Strittmatter, S.M., Igarashi, M., & Fishman, M.C. (1994). GAP-43 amino terminal peptides modulate growth cone morphology and neurite outgrowth. The Journal of Neuroscience, 14, 5503-5513. (Pubitemid 24279068)
117. Sulaiman, O.A.R., & Gordon, T. (2000). Effects of short- and long-term Schwann cell denervation on peripheral nerve regeneration, myelination, and size. Glia, 32, 234-246.
118. Sulaiman, O.A.R., & Gordon, T. (2002). Transforming growth factor-beta and forskolin attenuate the adverse effects of long-term Schwann cell denervation on peripheral nerve regeneration in vivo. Glia, 37, 206-218.
119. Sulaiman, O.A.R., & Gordon, T. (2003). Cellular and molecular interactions after peripheral and central injury. Biomed Rev, 14, 51-62. (Pubitemid 40806875)
120. Sulaiman, O.A.R., & Gordon, T. (2009). Role of chronic Schwann cell denervation in poor functional recovery after peripheral nerve injuries and strategies to combat it. Neurosurgery, in press.
121. Sulaiman, O.A.R., Midha, R., Munro, C.A., Matsuyama, T., Al-Majed, A.A., & Gordon, T. (2002). Chronic Schwann cell denervation and the presence of a sensory nerve reduce motor axonal regeneration. Experimental Neurology, 176, 342-354 (Pubitemid 35193351)
122. Sulaiman, O.A.R., Midha, R., & Gordon, T. (2009). Pathophysiology of surgical nerve disorders. In Yeomans Textbook of Neurological Surgery (6th ed., pp. in press.).
123. Sulaiman, O.A.R., Voda, J., Gold, B.G., & Gordon, T. (2002). FK506 increases peripheral nerve regeneration after chronic axotomy but not after chronic schwann cell denervation. Experimental Neurology, 175, 127-137. (Pubitemid 34507915)
124. Sunderland, S. (1947a). Rate of regeneration in human peripheral nerves: analysis of interval between injury and onset of recovery. Archives of Neurology and Psychiatry, 58(3), 251-295.
125. Sunderland, S. (1947b). Rate of Regeneration of Motor Fibers in the Ulnar and Sciatic Nerves. Archives of Neurology and Psychiatry, 58, 7-13.
126. Sunderland, S. (1947c). Rate of Regeneration of Sensory Nerve Fibers. Archives of Neurology and Psychiatry, 58, 1-5.
127. Sunderland, S. (1968). Nerve and Nerve Injuries. Baltimore: Williams & Wilkins.
128. Suzuki, G., Ochi, M., Shu, N., Uchio, Y., & Matsuura, Y. (1998). Sensory neurons regenerate more dominantly than motoneurons during the initial stage of the regenerating process after peripheral axotomy. Neuroreport, 9, 3487-3492. (Pubitemid 28566135)
129. Swett, J.E., Wikholm, R.P., Blanks, R.H., Swett, A.L., & Conley, L.C. (1986). Motoneurons of the rat sciatic nerve. Experimental Neurology, 93, 227-252.
130. Tang, S., Woodhall, R.W., Shen, Y.J., DeBellard, M.E., Saffell, J.L., Doherty, P., et al. (1997). Soluble myelin-associated glycoprotein (MAG) found in vivo inhibits axonal regeneration. Molecular and Cellular Neurosciences, 9, 333-346. (Pubitemid 27467486)
131. Tetzlaff, W., & Bisby, M.A. (1990). Cytoskeletal protein synthesis and regulation of nerve regeneration in PNS and CNS neurons of the rat. Restorative Neurology and Neuroscience, 1, 189-196.
132. Tetzlaff, W., Lederis, K.L., Cassar, L., & Bisby, M.A. (1989). Axonal transport and localization of B-50/GAP-43-like immunoreactivity in regnerating sciatic and facial nerves of the rat. The Journal of Neuroscience, 9, 1303-1313. (Pubitemid 19116750)
133. Thomas, C.K., Stein, R.B., Gordon, T., Lee, R.G., & Elleker, M.G. (1987). Patterns of reinnervation and motor unit recruitment in human hand muscles after complete ulnar and median nerve section and resuture. Journal of Neurology, Neurosurgery, and Psychiatry, 50, 259-268. (Pubitemid 17025864)
134. Tyreman, N., Pettersson, L.M.E., Verge, V.M., and Gordon, T. (2008). BDNF-mediated acceleration of motor axonal regeneration by brief low frequency electrical stimulation (ES). Society for Neuroscience, 33, 752-762.
135. Udina, E., Furey, M., Busch, S., Silver, J., Gordon, T., & Fouad, K. (2008). Electrical stimulation of intact peripheral sensory axons in rats promotes outgrowth of their central projections. Experimental Neurology, 210, 238-247.
136. Verge, V.M., Merlio, J.P., Grondin, J., Ernfors, P., Persson, H., Riopelle, R.J., et al. (1992). Colocalization of NGF binding sites, trk mRNA, and low-affinity NGF receptor mRNA in primary sensory neurons: responses to injury and infusion of NGF. The Journal of Neuroscience, 12, 4011-4022.
137. Verge, V.M., Tetzlaff, W., Richardson, P.M., & Bisby, M.A. (1990). Correlation between GAP43 and nerve growth factor receptors in rat sensory neurons. The Journal of Neuroscience, 10, 926-934. (Pubitemid 20104789)
138. Verma, P., Garcia-Alias, G., & Fawcett, J.W. (2008). Spinal Cord Repair: Bridging the Divide. Neurorehabil. Neural Repair.
139. Wall, P.D., & Gutnick, M. (1974). Ongoing activity in peripheral nerves: the physiology and pharmacology of impulses originating from a neuroma. Experimental Neurology, 43, 580-593.
140. Watson, D.F., Hoffman, P.N., Fittro, K.P., & Griffin, J.W. (1989). Neurofilament and tubulin transport slows along the course of mature motor axons. Brain Research, 477, 225-232.
141. Weinberg, H.J., & Spencer, P.S. (1978). The fate of Schwann cells isolated from axonal contact. Journal of Neurocytology, 7, 555-569.
142. Witzel, C., Rohde, C., & Brushart, T.M. (2005). Pathway sampling by regenerating peripheral axons. The Journal of Comparative Neurology, 485, 183-190. (Pubitemid 40471297)
143. Wong, J., & Oblinger, M.M. (1990). A comparison of peripheral and central axotomy effects on neurofilament and tubulin gene expression in rat dorsal root ganglion neurons. The Journal of Neuroscience, 10, 2215-2222.
144. Wu, D., Huang, W., Richardson, P.M., Priestley, J.V., & Liu, M. (2008). TRPC4 in rat dorsal root ganglion neurons is increased after nerve injury and is necessary for neurite outgrowth. The Journal of Biological Chemistry, 283, 416-426.
145. Wu, D., Zhang, Y., Bo, X., Huang, W., Xiao, F., Zhang, X., et al. (2007). Actions of neuropoietic cytokines and cyclic AMP in regenerative conditioning of rat primary sensory neurons. Experimental Neurology, 204, 66-76. (Pubitemid 46343726)
146. Yiu, G., & He, Z. (2003). Signaling mechanisms of the myelin inhibitors of axon regeneration. Current Opinion in Neurobiology, 13, 545-551. (Pubitemid 37441273)
147. Yiu, G., & He, Z. (2006). Glial inhibition of CNS axon regeneration. Nature Reviews. Neuroscience, 7, 617-627. (Pubitemid 44106744)
148. You, S., Petrov, T., Chung, P.H., & Gordon, T. (1997). The expression of the low affinity nerve growth factor receptor in long-term denervated Schwann cells. Glia, 20, 87-100. (Pubitemid 27253202)
149. Zhang, Y., Zhang, X., Wu, D., Verhaagen, J., Richardson, P.M., Yeh, J., et al. (2007). Lentiviral- mediated expression of polysialic acid in spinal cord and conditioning lesion promote regeneration of sensory axons into spinal cord. Molecular Therapy, 15, 1796-1804. (Pubitemid 47434186)
150. Zheng, B., Atwal, J., Ho, C., Case, L., He, X.L., Garcia, K.C., et al. (2005). Genetic deletion of the Nogo receptor does not reduce neurite inhibition in vitro or promote corticospinal tract regeneration in vivo. Proceedings of the National Academy of Sciences of the United States of America, 102, 1205-1210. (Pubitemid 40170750)
151. Zochodne, D.W. (2008). Neurobiology of Peripheral Nerve Regeneration. New York: Cambridge University Press.