Rodent models for treatment of spinal cord injury: Research trends and progress toward useful repair

Current Opinion in Neurology

Volumn 17, Issue 2, 2004, Pages 121-131

  Rosenzweig, Ephron S ^a   McDonald, John W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mouse; Rat; Regeneration

Indexed keywords

ACIDIC FIBROBLAST GROWTH FACTOR; AGMATINE; AMPA RECEPTOR ANTAGONIST; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CHANNEL BLOCKING AGENT; CALPASTATIN; CASPASE INHIBITOR; CELL ADHESION MOLECULE; CHONDROITIN ABC LYASE; DEXTROMETHORPHAN; ENOXAPARIN; FIBRONECTIN; IMMUNOGLOBULIN FC FRAGMENT; INTERLEUKIN 6; MEDROXYPROGESTERONE ACETATE; MELATONIN; METHYLPREDNISOLONE; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NERVE GROWTH FACTOR; NEUROTROPHIN 3; PENTOXIFYLLINE; PROGESTERONE; PROSTAGLANDIN E1; PROTEIN KINASE INHIBITOR; RESVERATROL; TISSUE PLASMINOGEN ACTIVATOR; UNINDEXED DRUG; VASCULOTROPIN;

BLADDER FUNCTION; CONTUSION; LOCOMOTION; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PAIN; REVIEW; SPINAL CORD COMPRESSION; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; SPINE STABILIZATION; TREATMENT INDICATION;

ADULT; ANIMALS; CHILD, PRESCHOOL; DISEASE MODELS, ANIMAL; HUMANS; LOCOMOTION; MICE; MICE, SCID; NERVE REGENERATION; PAIN THRESHOLD; RATS; SPINAL CORD INJURIES; TREATMENT OUTCOME; URINARY BLADDER, NEUROGENIC;

EID: 1842453803     PISSN: 13507540     EISSN: None     Source Type: Journal    
DOI: 10.1097/00019052-200404000-00007     Document Type: Review

References (258)

1. Richardson PM, McGuinness UM, Aguayo AJ. Axons from CNS neurons regenerate into PNS grafts. Nature 1980; 284:264-265.
2. David S, Aguayo AJ. Axonal elongation into peripheral nervous system 'bridges' after central nervous system injury in adult rats. Science 1981; 214:931-933.
3. David S, Lacroix S. Molecular approaches to spinal cord repair. Annu Rev Neurosci 2003; 26:411-440. A complete review of the inhibitory molecules found in myelin and possible methods for interfering with that inhibition. The paper also briefly discusses CSPGs and the glial scar.
4. Grimpe B, Silver J. The extracellular matrix in axon regeneration. Prog Brain Res 2002; 137:333-349.
5. Filbin MT. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 2003; 4:703-713. A comprehensive review of myelin-associated molecules that are inhibitory to neurite growth, as well as the signalling cascades involved. The paper discusses both direct blocking of the inhibitory pathways and altering the state of the neuron by elevating cAMP levels.
6. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull 1999; 49:377-391.
7. Schwab ME. Repairing the injured spinal cord. Science 2002; 295:1029-1031.
8. Schwab ME. Increasing plasticity and functional recovery of the lesioned spinal cord. Prog Brain Res 2002; 137:351-359.
9. Bregman BS. Regeneration in the spinal cord. Curr Opin Neurobiol 1998; 8:800-807.
10. McDonald JW, Howard MJ. Repairing the damaged spinal cord: a summary of our early success with embryonic stem cell transplantation and remyelination. Prog Brain Res 2002; 137:299-309.
11. McDonald JW, Becker D. Spinal cord injury: promising interventions and realistic goals. Am J Phys Med Rehabil 2003; 82 (10 Suppl.):S38-S49. A brief review that addresses both laboratory and clinical research. It also discusses general approaches for the transition from basic science to clinical application.
12. Bunge MB. Bridging the transected or contused adult rat spinal cord with Schwann cell and olfactory ensheathing glia transplants. Prog Brain Res 2002; 137:275-282.
13. Jacobs WB, Fehlings MG. The molecular basis of neural regeneration. Neurosurgery 2003; 53:943-948; discussion 948-950.
14. Blesch A, Lu P, Tuszynski MH. Neurotrophic factors, gene therapy, and neural stem cells for spinal cord repair. Brain Res Bull 2002; 57:833-838.
15. Tuszynski MH, Conner J, Blesch A, et al. New strategies in neural repair. Prog Brain Res 2002; 138:401-409.
16. Plunet W, Kwon BK, Tetzlaff W. Promoting axonal regeneration in the central nervous system by enhancing the cell body response to axotomy. J Neurosci Res 2002; 68:1-6.
17. Houle JD, Tessler A. Repair of chronic spinal cord injury. Exp Neurol 2003; 182:247-260. An elegant, comprehensive discussion of the complexities of chronic SCI, and a thorough review of the attempted treatments of chronic SCI. It also includes a brief review of successful treatments begun during the semi-chronic stages of SCI.
18. Novikova LN, Novikov LN, Kellerth JO. Biopolymers and biodegradable smart implants for tissue regeneration after spinal cord injury. Curr Opin Neurol 2003; 16:711-715. A brief review that effectively covers the variety of synthetic biodegradable or biocompatible matrices used as implants to aid spinal cord regeneration.
19. Okano H, Ogawa Y, Nakamura M, et al. Transplantation of neural stem cells into the spinal cord after injury. Semin Cell Dev Biol 2003; 14:191-198. A clearly written discussion of the potential uses for neural stem cells in the treatment of SCI. It discusses both successful transplantation studies and possible factors responsible for the failure of other such studies. The authors suggest that the cytokine response immediately after SCI may force astrocytic differentiation of stem cells.
20. Horner PJ, Gage FH. Regenerating the damaged central nervous system. Nature 2000; 407:963-970.
21. Bregman BS, Broude E, McAtee M, Kelley MS. Transplants and neurotrophic factors prevent atrophy of mature CNS neurons after spinal cord injury. Exp Neurol 1998; 149:13-27.
22. Au E, Roskams AJ. Olfactory ensheathing cells of the lamina propria in vivo and in vitro. Glia 2003; 41:224-236. This study explores the properties of an alternative source of OECs.
23. Keyvan-Fouladi N, Li Y, Raisman G. How do transplanted olfactory ensheathing cells restore function? Brain Res Brain Res Rev 2002; 40:325-327.
24. Santos-Benito FF, Ramon-Cueto A. Olfactory ensheathing glia transplantation: a therapy to promote repair in the mammalian central nervous system. Anat Rec 2003; 271B:77-85. A review of the rationale and progress of OEG transplants into rat CNS lesion models.
25. Jones LL, Sajed D, Tuszynski MH. Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J Neurosci 2003; 23:9276-9288.
26. ••]. Despite the modest regeneration observed in these rats, their motor function was largely unimproved. The authors also noted a detrimental effect of the grafting procedure on both motor and sensorimotor performance, regardless of treatment group.
27. Tobias CA, Shumsky JS, Shibata M, et al. Delayed grafting of BDNF and NT-3 producing fibroblasts into the injured spinal cord stimulates sprouting, partially rescues axotomized red nucleus neurons from loss and atrophy, and provides limited regeneration. Exp Neurol 2003; 184:97-113. The authors waited 6 weeks after SCI to transplant neurotrophin-producing fibroblasts. Although there were modest regenerative effects, they were diminished compared with similar treatments after shorter delays.
28. Tuszynski MH, Grill R, Jones LL, et al. NT-3 gene delivery elicits growth of chronically injured corticospinal axons and modestly improves functional deficits after chronic scar resection. Exp Neurol 2003; 181:47-56. Neurotrophin 3-making fibroblasts, transplanted 3 months after SCI, were able to elicit & modest functional improvement. The authors noted, however, that the difference in the Basso-Beattie-Bresnahan locomotor scale could have been the result of selective protection from additional functional decline caused by the grafting procedure.
29. Liu Y, Himes BT, Murray M, et al. Grafts of BDNF-producing fibroblasts rescue axotomized rubrospinal neurons and prevent their atrophy. Exp Neurol 2002; 178:150-164.
30. Franklin RJ. Remyelination by transplanted olfactory ensheathing cells. Anat Rec 2003; 271B:71-76. A brief review covering the use of OECs in both CNS injury and models of primary demyelination.
31. Lu P, Jones LL, Snyder EY, Tuszynski MH. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol 2003; 181:115-129.
32. Murray M, Kim D, Liu Y, et al. Transplantation of genetically modified cells contributes to repair and recovery from spinal injury. Brain Res Brain Res Rev 2002; 40:292-300.
33. Ruitenberg MJ, Plant GW, Christensen CL, et al. Viral vector-mediated gene expression in olfactory ensheathing glia implants in the lesioned rat spinal cord. Gene Ther 2002; 9:135-146.
34. Ruitenberg MJ, Plant GW, Hamers FP, et al. Ex vivo adenoviral vector-mediated neurotrophin gene transfer to olfactory ensheathing glia: effects on rubrospinal tract regeneration, lesion size, and functional recovery after implantation in the injured rat spinal cord. J Neurosci 2003; 23:7045-7058.
35. Ruitenberg MJ, Eggers R, Boer GJ, Verhaagen J. Adeno-associated viral vectors as agents for gene delivery: application in disorders and trauma of the central nervous system. Methods 2002; 28:182-194. A review of the use of adeno-associated viral vectors to make CNS cells overexpress target gene products, followed by detailed descriptions of the relevant protocols.
36. Zhou L, Baumgartner BJ, Hill-Felberg SJ, et al. Neurotrophin-3 expressed in situ induces axonal plasticity in the adult injured spinal cord. J Neurosci 2003; 23:1424-1431. The authors used an adenovirus vector to cause spinal motorneurons to overexpress neurotrophin 3.
37. Zhou L, Shine HD. Neurotrophic factors expressed in both cortex and spinal cord induce axonal plasticity after spinal cord injury. J Neurosci Res 2003; 74:221-226. An elegant use of two adenoviral vectors in combination. Spinal motorneurons were induced to express neurotrophin 3, whereas cells in the sensorimotor cortex were induced to express BDNF or glia-derived neurotrophic factor. The 14-day delay before the onset of treatment makes this paper even more interesting.
38. Blits B, Oudega M, Boer GJ, et al. Adeno-associated viral vector-mediated neurotrophin gene transfer in the injured adult rat spinal cord improves hind-limb function. Neuroscience 2003; 118:271-281. Adeno-associated viral vectors encoding BDNF or neurotrophin 3 were injected caudal to a Schwann cell bridge. Cells grew from the lumbar spinal cord towards the graft, but no outgrowth from the graft to the lumbar cord was observed.
39. Pfeifer A, Brandon EP, Kootstra N, et al. Delivery of the Cre recombinase by a self-deleting lentiviral vector: efficient gene targeting in vivo. Proc Natl Acad Sci U S A 2001; 98:11450-11455.
40. McGee AW, Strittmatter SM. The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends Neurosci 2003; 26:193-198. A detailed review of Nogo, the Nogo receptor, and the signalling pathway involved.
41. Caroni P, Schwab ME. Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J Cell Biol 1988; 106:1281-1288.
42. Caroni P, Schwab ME. Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1988; 1:85-96.
43. Pearse DD, Pereira FC, Marcillo AE, et al. Elevation of cAMP enhances regeneration and improves behavioral recovery in Schwann cell-grafted animals after spinal cord injury. Soc Neurosci Abstracts 2003; 775:10.
44. Qiu J, Cai D, Dai H, et al. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 2002; 34:895-903.
45. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 2002; 34:885-893.
46. Cai D, Shen Y, De Bellard M, et al. Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 1999; 22:89-101.
47. Cai D, Deng K, Mellado W, et al. Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 2002; 35:711-719.
48. Jones LL, Margolis RU, Tuszynski MH. The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp Neurol 2003; 182:399-411. A detailed description of expression changes in four CSPGs after SCI.
49. Grimpe B, Dong S, Doller C, et al. The critical role of basement membrane-independent laminin gamma 1 chain during axon regeneration in the CNS. J Neurosci 2002; 22:3144-3160.
50. Tang X, Davies JE, Davies SJ. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J Neurosci Res 2003; 71:427-444. A detailed description of the changes in expression levels of five CSPGs and tenascin-C after SCI.
51. Yick LW, Cheung PT, So KF, Wu W. Axonal regeneration of Clarke's neurons beyond the spinal cord injury scar after treatment with chondroitinase ABC. Exp Neurol 2003; 182:160-168.
52. Bradbury EJ, Moon LD, Popat RJ, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002; 416:636-640.
53. Chau CH, Shum DK, Li H, et al. Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J 2004; 18:194-196. Acute use of chondroitinase ABC to aid regrowth into the caudal cord through Schwann-cell-seeded guidance channels.
54. Conti A, Cardali S, Genovese T, et al. Role of inflammation in the secondary injury following experimental spinal cord trauma. J Neurosurg Sci 2003; 47:89-94.
55. Gonzalez R, Glaser J, Liu MT, et al. Reducing inflammation decreases secondary degeneration and functional deficit after spinal cord injury. Exp Neurol 2003; 184:456-463.
56. Popovich PG, Jones TB. Manipulating neuroinflammatory reactions in the injured spinal cord: back to basics. Trends Pharmacol Sci 2003; 24:13-17. An opinion on the role of inflammation and immune function in SCI. The authors acknowledge that immune function could be beneficial, but urge against any clinical therapies designed to boost immune response until we know more about the processes governing leukocyte response after SCI.
57. Hauben E, Schwartz M. Therapeutic vaccination for spinal cord injury: helping the body to cure itself. Trends Pharmacol Sci 2003; 24:7-12. An opinion on the role of inflammation and immune function in SCI. The authors suggest that a carefully directed immune response will help prevent much of the secondary cell death associated with SCI.
58. Inman D, Guth L, Steward O. Genetic influences on secondary degeneration and wound healing following spinal cord injury in various strains of mice. J Comp Neurol 2002; 451:225-235.
59. Kaptanoglu E, Beskonakli E, Okutan O, et al. Effect of magnesium sulphate in experimental spinal cord injury: evaluation with ultrastructural findings and early clinical results. J Clin Neurosci 2003; 10:329-334.
60. Mills CD, Johnson KM, Hulsebosch CE. Role of group II and group III metabotropic glutamate receptors in spinal cord injury. Exp Neurol 2002; 173:153-167.
61. Mills CD, Johnson KM, Hulsebosch CE. Group I metabotropic glutamate receptors in spinal cord injury: roles in neuroprotection and the development of chronic central pain. J Neurotrauma 2002; 19:23-42.
62. Beattie MS, Hermann GE, Rogers RC, Bresnahan JC. Cell death in models of spinal cord injury. Prog Brain Res 2002; 137:37-47.
63. Waldmeier PC. Prospects for antiapoptotic drug therapy of neurodegenerative diseases. Prog Neuropsychopharmacol Biol Psychiatry 2003; 27:303-321. An in-depth review of the role of apoptosis in multiple diseases and conditions, including SCI. Human applicability is the focus of this work.
64. Tator CH, Fehlings MG. Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J Neurosurg 1991; 75:15-26.
65. Carlson GD, Gorden C. Current developments in spinal cord injury research. Spine J 2002; 2:116-128.
66. Dong H, Fazzaro A, Xiang C, et al. Enhanced oligodendrocyte survival after spinal cord injury in Bax-deficient mice and mice with delayed Wallerian degeneration. J Neurosci 2003; 23:8682-8691.
67. Steward O, Zheng B, Tessier-Lavigne M. False resurrections: distinguishing regenerated from spared axons in the injured central nervous system. J Comp Neurol 2003; 459:1-8. An enlightening discussion of the potential sparing of axons during partial and complete spinal cord transections. Criteria are proposed by which regenerating axons may be identified.
68. Rivlin AS, Tator CH. Effect of duration of acute spinal cord compression in a new acute cord injury model in the rat. Surg Neurol 1978; 10:38-43.
69. Fehlings MG, Tator CH. The relationships among the severity of spinal cord injury, residual neurological function, axon counts, and counts of retrogradely labeled neurons after experimental spinal cord injury. Exp Neurol 1995; 132:220-228.
70. Holtz A, Nystrom B, Gerdin B. Spinal cord blood flow measured by 14C-iodoantipyrine autoradiography during and after graded spinal cord compression in rats. Surg Neurol 1989; 31:350-360.
71. Martin D, Schoenen J, Delree P, et al. Experimental acute traumatic injury of the adult rat spinal cord by a subdural inflatable balloon: methodology, behavioral analysis, and histopathology. J Neurosci Res 1992; 32:539-550.
72. Young W. Spinal cord contusion models. Prog Brain Res 2002; 137:231-255.
73. Gruner JA. A monitored contusion model of spinal cord injury in the rat. J Neurotrauma 1992; 9:123-126; discussion 126-128.
74. Somerson SK, Stokes BT. Functional analysis of an electromechanical spinal cord injury device. Exp Neurol 1987; 96:82-96.
75. Behrmann DL, Bresnahan JC, Beattie MS, Shah BR. Spinal cord injury produced by consistent mechanical displacement of the cord in rats: behavioral and histologic analysis. J Neurotrauma 1992; 9:197-217.
76. Beattie MS. Anatomic and behavioral outcome after spinal cord injury produced by a displacement controlled impact device. J Neurotrauma 1992; 9:157-159; discussion 159-160.
77. Scheff SW, Rabchevsky AG, Fugaccia I, et al. Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J Neurotrauma 2003; 20:179-193. An introduction of the Infinite Horizons impactor. It also includes a brief review of the history of the contusion model of SCI.
78. Jakeman LB, Guan Z, Wei P, et al. Traumatic spinal cord injury produced by controlled contusion in mouse. J Neurotrauma 2000; 17:299-319.
79. Ma M, Basso DM, Walters P, et al. Behavioral and histological outcomes following graded spinal cord contusion injury in the C57BI/6 mouse. Exp Neurol 2001; 169:239-254.
80. Metz GA, Curt A, van de Meent H, et al. Validation of the weight-drop contusion model in rats: a comparative study of human spinal cord injury. J Neurotrauma 2000; 17:1-17.
81. Verdu E, Garcia-Alias G, Fores J, et al. Olfactory ensheathing cells transplanted in lesioned spinal cord prevent loss of spinal cord parenchyma and promote functional recovery. Glia 2003; 42:275-286.
82. Garcia-Alias G, Verdu E, Fores J, et al. Functional and electrophysiological characterization of photochemical graded spinal cord injury in the rat. J Neurotrauma 2003; 20:501-510.
83. Verdu E, Garcia-Alias G, Fores J, et al. Morphological characterization of photochemical graded spinal cord injury in the rat. J Neurotrauma 2003; 20:483-499.
84. von Euler M, Janson AM, Larsen JO, et al. Spontaneous axonal regeneration in rodent spinal cord after ischemic injury. J Neuropathol Exp Neurol 2002; 61:64-75.
85. Bao F, Liu D. Peroxynitrite generated in the rat spinal cord induces apoptotic cell death and activates caspase-3. Neuroscience 2003; 116:59-70.
86. Bao F, DeWitt DS, Prough DS, Liu D. Peroxynitrite generated in the rat spinal cord induces oxidation and nitration of proteins: reduction by Mn (III) tetrakis (4-benzoic acid) porphyrin. J Neurosci Res 2003; 71:220-227.
87. Brewer KL, McMillan D, Nolan T, Shum K. Cortical changes in cholecystokinin mRNA are related to spontaneous pain behaviors following excitotoxic spinal cord injury in the rat. Brain Res Mol Brain Res 2003; 118:171-174.
88. Brodbelt AR, Stoodley MA, Watling AM, et al. Fluid flow in an animal model of post-traumatic syringomyelia. Eur Spine J 2003; 12:300-306.
89. Caudle RM, Perez FM, King C, et al. N-methyl-D-aspartate receptor subunit expression and phosphorylation following excitotoxic spinal cord injury in rats. Neurosci Lett 2003; 349:37-40.
90. Nottingham SA, Springer JE. Temporal and spatial distribution of activated caspase-3 after subdural kainic acid infusions in rat spinal cord. J Comp Neurol 2003; 464:463-471.
91. Wu WP, Hao JX, Xu XJ, et al. The very-high-efficacy 5-HT(1A) receptor agonist, F 13640, preempts the development of allodynia-like behaviors in rats with spinal cord injury. Eur J Pharmacol 2003; 478:131-137.
92. Yu CG, Fairbanks CA, Wilcox GL, Yezierski RP. Effects of agmatine, interleukin-10, and cyclosporin on spontaneous pain behavior after excitotoxic spinal cord injury in rats. J Pain 2003; 4:129-140.
93. Krassioukov AV, Ackery A, Schwartz G, et al. An in vitro model of neurotrauma in organotypic spinal cord cultures from adult mice. Brain Res Brain Res Protocol 2002; 10:60-68.
94. Saruhashi Y, Matsusue Y, Hukuda S. Effects of serotonin 1A agonist on acute spinal cord injury. Spinal Cord 2002; 40:519-523.
95. Luo J, Borgens R, Shi R. Polyethylene glycol immediately repairs neuronal membranes and inhibits free radical production after acute spinal cord injury. J Neurochem 2002; 83:471-480.
96. Isbir CS, Ak K, Kurtkaya O, et al. Ischemic preconditioning and nicotinamide in spinal cord protection in an experimental model of transient aortic occlusion. Eur J Cardiothorac Surg 2003; 23:1028-1033.
97. Morino T, Ogata T, Horiuchi H, et al. Delayed neuronal damage related to microglia proliferation after mild spinal cord compression injury. Neurosci Res 2003; 46:309-318.
98. Kwon BK, Oxland TR, Tetzlaff W. Animal models used in spinal cord regeneration research. Spine 2002; 27:1504-1510.
99. Gomez VM, Averill S, King V, et al. Transplantation of olfactory ensheathing cells fails to promote significant axonal regeneration from dorsal roots into the rat cervical cord. J Neurocytol 2003; 32:53-70.
100. Pascual JI, Gudino-Cabrera G, Insausti R, Nieto-Sampedro M. Spinal implants of olfactory ensheathing cells promote axon regeneration and bladder activity after bilateral lumbosacral dorsal rhizotomy in the adult rat. J Urol 2002; 167:1522-1526.
101. Ramer MS, Bishop T, Dockery P, et al. Neurotrophin-3-mediated regeneration and recovery of proprioception following dorsal rhizotomy. Mol Cell Neurosci 2002; 19:239-249.
102. Huang MC, Chen KC, Chuang TY, et al. Cervical root repair in adult rats after transection: recovery of forelimb motor function. Exp Neurol 2003; 180:101-109.
103. Bracken MB, Shepard MJ, Collins WF, et al. A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal-cord injury. Results of the Second National Acute Spinal Cord Injury Study. N Engl J Med 1990; 322:1405-1411.
104. Plant GW, Christensen CL, Oudega M, Bunge MB. Delayed transplantation of olfactory ensheathing glia promotes sparing/regeneration of supraspinal axons in the contused adult rat spinal cord. J Neurotrauma 2003; 20:1-16. This study demonstrates that delaying OEC transplants by 7 days post-injury improves their effect on both anatomy and hindlimb function.
105. Keyvan-Fouladi N, Raisman G, Li Y. Functional repair of the corticospinal tract by delayed transplantation of olfactory ensheathing cells in adult rats. J Neurosci 2003; 23:9428-9434. After a lesion of the corticospinal tract, the authors waited 8 weeks to transplant OECs. Rats receiving transplants recovered skilled use of their forepaws.
106. Ogawa Y, Sawamoto K, Miyata T, et al. Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J Neurosci Res 2002; 69:925-933.
107. McDonald JW, Liu XZ, Qu Y, et al. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 1999; 5:1410-1412.
108. Coumans JV, Lin TT, Dai HN, et al. Axonal regeneration and functional recovery after complete spinal cord transection in rats by delayed treatment with transplants and neurotrophins. J Neurosci 2001; 21:9334-9344.
109. ••], this suggests that re-injury can induce a state more favorable for regeneration.
110. Mueller CA, Schluesener HJ, Conrad S, et al. Spinal cord injury induces lesional expression of the proinflammatory and antiangiogenic cytokine EMAP II. J Neurotrauma 2003; 20:1007-1015.
111. Pan W, Zhang L, Liao J, et al. Selective increase in TNF alpha permeation across the blood-spinal cord barrier after SCI. J Neuroimmunol 2003; 134:111-117.
112. Pan W, Csernus B, Kastin AJ. Upregulation of p55 and p75 receptors mediating TNF-alpha transport across the injured blood-spinal cord barrier. J Mol Neurosci 2003; 21:173-184.
113. Di Giovanni S, Knoblach SM, Brandoli C, et al. Gene profiling in spinal cord injury shows role of cell cycle in neuronal death. Ann Neurol 2003; 53:454-468.
114. Dubreuil CI, Winton MJ, McKerracher L. Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system. J Cell Biol 2003; 162:233-243.
115. Goussev S, Hsu JY, Lin Y, et al. Differential temporal expression of matrix metalloproteinases after spinal cord injury: relationship to revascularization and wound healing. J Neurosurg 2003; 99 (2 Suppl.):188-197.
116. Wells JE, Rice TK, Nuttall RK, et al. An adverse role for matrix metalloproteinase 12 after spinal cord injury in mice. J Neurosci 2003; 23:10107-10115.
117. Jung K, Min do S, Sim KB, et al. Upregulation of phospholipase D1 in the spinal cords of rats with clip compression injury. Neurosci Lett 2003; 336:126-130.
118. Kim DH, Heo SD, Ahn MJ, et al. Activation of embryonic intermediate filaments contributes to glial scar formation after spinal cord injury in rats. J Vet Sci 2003; 4:109-112.
119. Krautstrunk M, Scholtes F, Martin D, et al. Increased expression of the putative axon growth-repulsive extracellular matrix molecule, keratan sulphate proteoglycan, following traumatic injury of the adult rat spinal cord. Acta Neuropathol (Berl) 2002; 104:592-600.
120. Liu CL, Jin AM, Tong BH. Detection of gene expression pattern in the early stage after spinal cord injury by gene chip. Chin J Traumatol 2003; 6:18-22.
121. Liu D, Liu J, Sun D, et al. Spinal cord injury increases iron levels: catalytic production of hydroxyl radicals. Free Radic Biol Med 2003; 34:64-71.
122. Peters CM, Rogers SD, Pomonis JD, et al. Endothelin receptor expression in the normal and injured spinal cord: potential involvement in injury-induced ischemia and gliosis. Exp Neurol 2003; 180:1-13.
123. Ray SK, Matzelle DD, Sribnick EA, et al. Calpain inhibitor prevented apoptosis and maintained transcription of proteolipid protein and myelin basic protein genes in rat spinal cord injury. J Chem Neuroanat 2003; 26:119-124.
124. Wingrave JM, Schaecher KE, Sribnick EA, et al. Early induction of secondary injury factors causing activation of calpain and mitochondria- mediated neuronal apoptosis following spinal cord injury in rats. J Neurosci Res 2003; 73:95-104.
125. Seitz A, Kragol M, Aglow E, et al. Apolipoprotein E expression after spinal cord injury in the mouse. J Neurosci Res 2003; 71:417-426.
126. Shibuya S, Miyamoto O, Itano T, et al. Temporal progressive antigen expression in radial glia after contusive spinal cord injury in adult rats. Glia 2003; 42:172-183.
127. Sroga JM, Jones TB, Kigerl KA, et al. Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J Comp Neurol 2003; 462:223-240.
128. Storer PD, Houle JD. βII-tubulin and GAP 43 mRNA expression in chronically injured neurons of the red nucleus after a second spinal cord injury. Exp Neurol 2003; 183:537-547. An interesting demonstration that a second SCI, caused by a delayed transplant operation, is sufficient to elicit a stronger upregulation of some regeneration-associated genes than is observed after the initial injury.
129. Tjoa T, Strausbaugh HJ, Maida N, et al. The use of flow cytometry to assess neutrophil infiltration in the injured murine spinal cord. J Neurosci Methods 2003; 129:49-59.
130. Willson CA, Miranda JD, Foster RD, et al. Transection of the adult rat spinal cord upregulates EphB3 receptor and ligand expression. Cell Transplant 2003; 12:279-290.
131. Moreau-Fauvarque C, Kumanogoh A, Camand E, et al. The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and upregulated after CNS lesion. J Neurosci 2003; 23:9229-9239.
132. Colak A, Soy O, Uzun H, et al. Neuroprotective effects of GYKI 52466 on experimental spinal cord injury in rats. J Neurosurg 2003; 98 (3 Suppl.):275-281.
133. Faulkner JR, Herrmann JE, Woo MJ, et al. Reactive astrocytes protect tissue and preserve function after spinal cord stab injury. Soc Neurosci Abstracts 2003; 744:1.
134. Herrmann JE, Faulkner JR, Woo MJ, et al. Reactive astrocytes protect tissue and preserve function after crush spinal cord injury. Soc Neurosci Abstracts 2003; 744:2.
135. Cakir E, Baykal S, Karahan SC, et al. Acute phase effects of ATP-MgCI2 on experimental spinal cord injury. Neurosurg Rev 2003; 26:67-70.
136. Seki T, Hida K, Tada M, et al. Role of the bcl-2 gene after contusive spinal cord injury in mice. Neurosurgery 2003; 53:192-198; discussion 198.
137. Novikova LN, Novikov LN, Kellerth JO. Differential effects of neurotrophins on neuronal survival and axonal regeneration after spinal cord injury in adult rats. J Comp Neurol 2002; 452:255-263.
138. Gondim FA, Rodrigues CL, Lopes AC Jr, et al. Effect of preinjury large bowel emptying on the inhibition of upper gastrointestinal motility after spinal cord injury in rats. Dig Dis Sci 2003; 48:1713-1718.
139. Unlu A, Hariharan N, Iskandar BJ. Spinal cord regeneration induced by a voltage-gated calcium channel agonist. Neurol Res 2002; 24:639-642.
140. Zhang SX, Bondada V, Geddes JW. Evaluation of conditions for calpain inhibition in the rat spinal cord: effective postinjury inhibition with intraspinal MDL28170 microinjection. J Neurotrauma 2003; 20:59-67.
141. Takagi T, Takayasu M, Mizuno M, et al. Caspase activation in neuronal and glial apoptosis following spinal cord injury in mice. Neurol Med Chir (Tokyo) 2003; 43:20-29; discussion 29-30.
142. Roonprapunt C, Huang W, Grill R, et al. Soluble cell adhesion molecule L1-Fc promotes locomotor recovery in rats after spinal cord injury. J Neurotrauma 2003; 20:871-882.
143. Rabchevsky AG, Sullivan PG, Fugaccia I, Scheff SW. Creatine diet supplement for spinal cord injury: influences on functional recovery and tissue sparing in rats. J Neurotrauma 2003; 20:659-669.
144. Ibarra A, Correa D, Willms K, et al. Effects of cyclosporin-A on immune response, tissue protection and motor function of rats subjected to spinal cord injury. Brain Res 2003; 979:165-178.
145. Topsakal C, Erol FS, Ozveren MF, et al. Effects of methylprednisolone and dextromethorphan on lipid peroxidation in an experimental model of spinal cord injury. Neurosurg Rev 2002; 25:258-266.
146. Topsakal C, Kilic N, Erol FS, et al. Medroxyprogesterone acetate, enoxaparin and pentoxyfylline cause alterations in lipid peroxidation, paraoxonase (PON1) activities and homocysteine levels in the acute oxidative stress in an experimental model of spinal cord injury. Acta Neurochir (Wien) 2002; 144:1021-1031; discussion 1031.
147. Jiang S, Wang J, Khan MI, et al. Enteric glia promote regeneration of transected dorsal root axons into spinal cord of adult rats. Exp Neurol 2003; 181:79-83.
148. Kaptanoglu E, Solaroglu I, Okutan O, et al. Erythropoietin exerts neuroprotection after acute spinal cord injury in rats: effect on lipid peroxidation and early ultrastructural findings. Neurosurg Rev 2003; Epub ahead of print.
149. de Barros Filho TE, de Oliveira RP, Tsanaclis AM, et al. An experimental model for the transplantation of fetal central nervous system cells to the injured spinal cord in rats. Rev Hosp Clin Fac Med Sao Paulo 2002; 57:257-264.
150. King VR, Henseler M, Brown RA, Priestley JV. Mats made from fibronectin support oriented growth of axons in the damaged spinal cord of the adult rat. Exp Neurol 2003; 182:383-398.
151. Tai MH, Cheng H, Wu JP, et al. Gene transfer of glial cell line-derived neurotrophic factor promotes functional recovery following spinal cord contusion. Exp Neurol 2003; 183:508-515.
152. Iannotti C, Li H, Yan P, et al. Glial cell line-derived neurotrophic factor-enriched bridging transplants promote propriospinal axonal regeneration and enhance myelination after spinal cord injury. Exp Neurol 2003; 183:379-393.
153. Menet V, Prieto M, Privat A, Gimenez y Ribotta M. Axonal plasticity and functional recovery after spinal cord injury in mice deficient in both glial fibrillary acidic protein and vimentin genes. Proc Natl Acad Sci U S A 2003; 100:8999-9004.
154. Saporta S, Kim JJ, Willing AE, et al. Human umbilical cord blood stem cells infusion in spinal cord injury: engraftment and beneficial influence on behavior. J Hematother Stem Cell Res 2003; 12:271-278.
155. Huang L, Mehta MP, Nanda A, Zhang JH. The role of multiple hyperbaric oxygenation in expanding therapeutic windows after acute spinal cord injury in rats. J Neurosurg 2003; 99 (2 Suppl.):198-205.
156. Lacroix S, Chang L, Rose-John S, Tuszynski MH. Delivery of hyper-interleukin-6 to the injured spinal cord increases neutrophil and macrophage infiltration and inhibits axonal growth. J Comp Neurol 2002; 454:213-228.
157. Fuller DD, Johnson SM, Olson EB Jr, Mitchell GS. Synaptic pathways to phrenic motoneurons are enhanced by chronic intermittent hypoxia after cervical spinal cord injury. J Neurosci 2003; 23:2993-3000.
158. Schultke E, Kendall E, Kamencic H, et al. Quercetin promotes functional recovery following acute spinal cord injury. J Neurotrauma 2003; 20:583-591.
159. Sicotte M, Tsatas O, Jeong SY, et al. Immunization with myelin or recombinant Nogo-66/MAG in alum promotes axon regeneration and sprouting after corticospinal tract lesions in the spinal cord. Mol Cell Neurosci 2003; 23:251-263.
160. Topsakal C, Kilic N, Ozveren F, et al. Effects of prostaglandin E1, melatonin, and oxytetracycline on lipid peroxidation, antioxidant defense system, paraoxonase (PON1) activities, and homocysteine levels in an animal model of spinal cord injury. Spine 2003; 28:1643-1652.
161. Wells JE, Hurlbert RJ, Fehlings MG, Yong VW. Neuroprotection by minocycline facilitates significant recovery from spinal cord injury in mice. Brain 2003; 126:1628-1637.
162. Yan P, Liu N, Kim GM, et al. Expression of the type 1 and type 2 receptors for tumor necrosis factor after traumatic spinal cord injury in adult rats. Exp Neurol 2003; 183:286-297.
163. Yang YB, Piao YJ. Effects of resveratrol on secondary damages after acute spinal cord injury in rats. Acta Pharmacol Sin 2003; 24:703-710.
164. Li L, Xu Q, Wu Y, et al. Combined therapy of methylprednisolone and brain-derived neurotrophic factor promotes axonal regeneration and functional recovery after spinal cord injury in rats. Chin Med J (Engl) 2003; 116:414-418.
165. Lee SM, Yune TY, Kim SJ, et al. Minocycline reduces cell death and
166. Vroemen M, Aigner L, Winkler J, Weidner N. Adult neural progenitor cell grafts survive after acute spinal cord injury and integrate along axonal pathways. Eur J Neurosci 2003; 18:743-751.
167. Bai H, Suzuki Y, Noda T, et al. Dissemination and proliferation of neural stem cells on the spinal cord by injection into the fourth ventricle of the rat: a method for cell transplantation. J Neurosci Methods 2003; 124:181-187.
168. Marsh DR, Wong ST, Meakin SO, et al. Neutralizing intraspinal nerve growth factor with a trkA-IgG fusion protein blocks the development of autonomic dysreflexia in a clip-compression model of spinal cord injury. J Neurotrauma 2002; 19:1531-1541.
169. Yune TY, Chang MJ, Kim SJ, et al. Increased production of tumor necrosis factor-alpha induces apoptosis after traumatic spinal cord injury in rats. J Neurotrauma 2003; 20:207-219.
170. Kaptanoglu E, Beskonakli E, Solaroglu I, et al. Magnesium sulfate treatment in experimental spinal cord injury: emphasis on vascular changes and early clinical results. Neurosurg Rev 2003; 26:283-287.
171. Li S, Strittmatter SM. Delayed systemic Nogo-66 receptor antagonist promotes recovery from spinal cord injury. J Neurosci 2003; 23:4219-4227. A delayed, non-invasive antagonism of the Nogo pathway improved both anatomical and functional outcome. A laudable attempt to find a clinically practical treatment.
172. Kim JE, Li S, GrandPre T, et al. Axon regeneration in young adult mice lacking Nogo-A/B. Neuron 2003; 38:187-199.
173. Simonen M, Pedersen V, Weinmann O, et al. Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 2003; 38:201-211.
174. Zheng B, Ho C, Li S, et al. Lack of enhanced spinal regeneration in Nogo-deficient mice. Neuron 2003; 38:213-224.
175. Merkler D, Oertle T, Buss A, et al. Rapid induction of autoantibodies against Nogo-A and MOG in the absence of an encephalitogenic T cell response: implication for immunotherapeutic approaches in neurological diseases. FASEB J 2003; 17:2275-2277.
176. DeLucia TA, Conners JJ, Brown TJ, et al. Use of a cell line to investigate olfactory ensheathing cell-enhanced axonal regeneration. Anat Rec 2003; 271B:61-70.
177. Resnick DK, Cechvala CF, Yan Y, et al. Adult olfactory ensheathing cell transplantation for acute spinal cord injury. J Neurotrauma 2003; 20:279-285.
178. Li Y, Decherchi P, Raisman G. Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. J Neurosci 2003; 23:727-731.
179. Horiuchi H, Ogata T, Morino T, et al. Continuous intrathecal infusion of SB203580, a selective inhibitor of p38 mitogen-activated protein kinase, reduces the damage of hind-limb function after thoracic spinal cord injury in rat. Neurosci Res 2003; 47:209-217.
180. Beattie MS, Harrington AW, Lee R, et al. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 2002; 36:375-386.
181. Lee YS, Hsiao I, Lin VW. Peripheral nerve grafts and aFGF restore partial hindlimb function in adult paraplegic rats. J Neurotrauma 2002; 19:1203-1216.
182. Labombarda F, Gonzalez SL, Deniselle MC, et al. Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25-Dx expression in the rat spinal cord. J Neurochem 2003; 87:902-913.
183. Naruo S, Okajima K, Taoka Y, et al. Prostaglandin E1 reduces compression trauma-induced spinal cord injury in rats mainly by inhibiting neutrophil activation. J Neurotrauma 2003; 20:221-228.
184. Sung JK, Miao L, Calvert JW, et al. A possible role of RhoA/Rho-kinase in experimental spinal cord injury in rat. Brain Res 2003; 959:29-38.
185. Fournier AE, Takizawa BT, Strittmatter SM. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci 2003; 23:1416-1423.
186. Jacob JE, Gris P, Fehlings MG, et al. Autonomic dysreflexia after spinal cord transection or compression in 129Sv, C57BL, and Wallerian degeneration slow mutant mice. Exp Neurol 2003; 183:136-146.
187. Liu F, Luo ZJ, You SW, et al. Significance of fixation of the vertebral column for spinal cord injury experiments. Spine 2003; 28:1666-1671.
188. Sugawara T, Lewen A, Gasche Y, et al. Overexpression of SOD1 protects vulnerable motor neurons after spinal cord injury by attenuating mitochondrial cytochrome c release. FASEB J 2002; 16:1997-1999.
189. Hauben E, Mizrahi T, Agranov E, Schwartz M. Sexual dimorphism in the spontaneous recovery from spinal cord injury: a gender gap in beneficial autoimmunity? Eur J Neurosci 2002; 16:1731-1740.
190. Kipnis J, Mizrahi T, Hauben E, et al. Neuroprotective autoimmunity: naturally occurring CD4+CD25+ regulatory T cells suppress the ability to withstand injury to the central nervous system. Proc Natl Acad Sci U S A 2002; 99:15620-15625.
191. Abe Y, Nakamura H, Yoshino O, et al. Decreased neural damage after spinal cord injury in tPA-deficient mice. J Neurotrauma 2003; 20:43-57.
192. Multon S, Franzen R, Poirrier AL, et al. The effect of treadmill training on motor recovery after a partial spinal cord compression-injury in the adult rat. J Neurotrauma 2003; 20:699-706.
193. Widenfalk J, Lipson A, Jubran M, et al. Vascular endothelial growth factor improves functional outcome and decreases secondary degeneration in experimental spinal cord contusion injury. Neuroscience 2003; 120:951-960.
194. Benton RL, Whittemore SR. VEGF165 therapy exacerbates secondary damage following spinal cord injury. Neurochem Res 2003; 28:1693-1703.
195. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995; 12:1-21.
196. Storer PD, Dolbeare D, Houle JD. Treatment of chronically injured spinal cord with neurotrophic factors stimulates βll-tubulin and GAP-43 expression in rubrospinal tract neurons. J Neurosci Res 2003; 74:502-511.
197. Hains BC, Johnson KM, Eaton MJ, et al. Serotonergic neural precursor cell grafts attenuate bilateral hyperexcitability of dorsal horn neurons after spinal hemisection in rat. Neuroscience 2003; 116:1097-1110.
198. Liu Y, Kim D, Himes BT, et al. Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J Neurosci 1999; 19:4370-4387.
199. Jin Y, Fischer I, Tessler A, Houle JD. Transplants of fibroblasts genetically modified to express BDNF promote axonal regeneration from supraspinal neurons following chronic spinal cord injury. Exp Neurol 2002; 177:265-275.
200. Hauben E, Gothilf A, Cohen A, et al. Vaccination with dendritic cells pulsed with peptides of myelin basic protein promotes functional recovery from spinal cord injury. J Neurosci 2003; 23:8808-8819. Using a form of treatment that has generated some controversy, the authors enhanced the immune response after SCI. Treatment begun within 12 days resulted in improved functional and anatomical outcomes, whereas treatment delayed for 28 days had no effect
201. Bomstein Y, Marder JB, Vitner K, et al. Features of skin-coincubated macrophages that promote recovery from spinal cord injury. J Neuroimmunol 2003; 142:10-16.
202. Mitsui T, Kakizaki H, Tanaka H, et al. Immortalized neural stem cells transplanted into the injured spinal cord promote recovery of voiding function in the rat. J Urol 2003; 170:1421-1425.
203. Cao QL, Howard RM, Dennison JB, Whittemore SR. Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp Neurol 2002; 177:349-359. An important demonstration of the difficulties inherent in the transplantation of partially differentiated cells into the injured spinal cord.
204. Gilmore SA, Phillips N, Liu KM, Houle JD. Radiation-induced modulation of the microglial population in the normal and injured mature spinal cord. Exp Neurol 2003; 182:169-179. The authors were able to decrease the numbers of microglia in a given area of spinal cord without changing the number of astrocytes in the same area. They are now investigating the possibility that this treatment will enhance regeneration through a peripheral nerve graft.
205. Inman DM, Steward O. Ascending sensory, but not other long-tract axons, regenerate into the connective tissue matrix that forms at the site of a spinal cord injury in mice. J Comp Neurol 2003; 462:431-449.
206. Inman DM, Steward O. Physical size does not determine the unique histopathological response seen in the injured mouse spinal cord. J Neurotrauma 2003; 20:33-42.
207. Tsien JZ, Chen DF, Gerber D, et al. Subregion- and cell type-restricted gene knockout in mouse brain. Cell 1996; 87:1317-1326.
208. Seki T, Hida K, Tada M, et al. Graded contusion model of the mouse spinal cord using a pneumatic impact device. Neurosurgery 2002; 50:1075-1081; discussion 1081-1072.
209. Basso DM, Fisher LC. The Basso mouse scale for locomotion (BMS) is a more sensitive indicator of recovery than the BBB scale in mice with spinal cord injury. Soc Neurosci Abstracts 2003; 76:13.
210. Bruce JC, Oatway MA, Weaver LC. Chronic pain after clip-compression injury of the rat spinal cord. Exp Neurol 2002; 178:33-48.
211. Gerke MB, Duggan AW, Xu L, Siddall PJ. Thalamic neuronal activity in rats with mechanical allodynia following contusive spinal cord injury. Neuroscience 2003; 117:715-722.
212. Gwak YS, Nam TS, Paik KS, et al. Attenuation of mechanical hyperalgesia following spinal cord injury by administration of antibodies to nerve growth factor in the rat. Neurosci Lett 2003; 336:117-120.
213. Hains BC, Willis WD, Hulsebosch CE. Serotonin receptors 5-HT1A and 5-HT3 reduce hyperexcitability of dorsal horn neurons after chronic spinal cord hemisection injury in rat. Exp Brain Res 2003; 149:174-186.
214. Hains BC, Black JA, Waxman SG. Primary cortical motor neurons undergo apoptosis after axotomizing spinal cord injury. J Comp Neurol 2003; 462:328-341.
215. Hains BC, Klein JP, Saab CY, et al. Upregulation of sodium channel Nav1. 3 and functional involvement in neuronal hyperexcitability associated with central neuropathic pain after spinal cord injury. J Neurosci 2003; 23:8881-8892.
216. Hoheisel U, Scheifer C, Trudrung P, et al. Pathophysiological activity in rat dorsal horn neurones in segments rostral to a chronic spinal cord injury. Brain Res 2003; 974:134-145.
217. Horiuchi H, Ogata T, Morino T, et al. Serotonergic signaling inhibits hyperalgesia induced by spinal cord damage. Brain Res 2003; 963:312-320.
218. Ondarza AB, Ye Z, Hulsebosch CE. Direct evidence of primary afferent sprouting in distant segments following spinal cord injury in the rat: colocalization of GAP-43 and CGRP. Exp Neurol 2003; 184:373-380.
219. Kim J, Jung JI, Na HS, et al. Effects of morphine on mechanical allodynia in a rat model of central neuropathic pain. Neuroreport 2003; 14:1017-1020.
220. Miyazato M, Sugaya K, Nishijima S, et al. Inhibitory effect of intrathecal glycine on the micturition reflex in normal and spinal cord injury rats. Exp Neurol 2003; 183:232-240.
221. Seki S, Sasaki K, Fraser MO, et al. Immunoneutralization of nerve growth factor in lumbosacral spinal cord reduces bladder hyperreflexia in spinal cord injured rats. J Urol 2002; 168:2269-2274.
222. Somogyi GT, Zernova GV, Yoshiyama M, et al. Change in muscarinic modulation of transmitter release in the rat urinary bladder after spinal cord injury. Neurochem Int 2003; 43:73-77.
223. Yu X, Xu L, Zhang XD, Cui FZ. Effect of spinal cord injury on urinary bladder spinal neural pathway: a retrograde transneuronal tracing study with pseudorabies virus. Urology 2003; 62:755-759.
224. Golder FJ, Fuller DD, Davenport PW, et al. Respiratory motor recovery after unilateral spinal cord injury: Eliminating crossed phrenic activity decreases tidal volume and increases contralateral respiratory motor output. J Neurosci 2003; 23:2494-2501.
225. Teng YD, Bingaman M, Taveira-DaSilva AM, et al. Serotonin 1A receptor agonists reverse respiratory abnormalities in spinal cord-injured rats. J Neurosci 2003; 23:4182-4189.
226. Nantwi KD, Goshgarian HG. Actions of specific adenosine receptor A1 and A2 agonists and antagonists in recovery of phrenic motor output following upper cervical spinal cord injury in adult rats. Clin Exp Pharmacol Physiol 2002; 29:915-923.
227. Krassioukov AV, Johns DG, Schramm LP. Sensitivity of sympathetically correlated spinal interneurons, renal sympathetic nerve activity, and arterial pressure to somatic and visceral stimuli after chronic spinal injury. J Neurotrauma 2002; 19:1521-1529.
228. Huang HF, Li MT, Wang S, et al. Spinal cord contusion impairs sperm motility in the rat without disrupting spermatogenesis. J Androl 2003; 24:371-380.
229. Huang HF, Li MT, Wang S, et al. Alteration of cyclic adenosine 3′,5′-monophosphate signaling in rat testicular cells after spinal cord injury. J Spinal Cord Med 2003; 26:69-78.
230. Li Y, Bennett DJ. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 2003; 90:857-869.
231. Rodenbaugh DW, Collins HL, Nowacek DG, DiCarlo SE. Increased susceptibility to ventricular arrhythmias is associated with changes in Ca2+ regulatory proteins in paraplegic rats. Am J Physiol Heart Circ Physiol 2003; 285:H2605-H2613.
232. Rodenbaugh DW, Collins HL, DiCarlo SE. Increased susceptibility to ventricular arrhythmias in hypertensive paraplegic rats. Clin Exp Hypertens 2003; 25:349-358.
233. Watanabe M, Fukuda Y. Survival and axonal regeneration of retinal ganglion cells in adult cats. Prog Retin Eye Res 2002; 21:529-553.
234. Isenmann S, Kretz A, Cellerino A. Molecular determinants of retinal ganglion cell development, survival, and regeneration. Prog Retin Eye Res 2003; 22:483-543.
235. Goldberg JL, Espinosa JS, Xu Y, et al. Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 2002; 33:689-702.
236. Ellezam B, Bertrand J, Dergham P, McKerracher L. Vaccination stimulates retinal ganglion cell regeneration in the adult optic nerve. Neurobiol Dis 2003; 12:1-10.
237. Franklin RJ. Remyelination of the demyelinated CNS: the case for and against transplantation of central, peripheral and olfactory glia. Brain Res Bull 2002; 57:827-832.
238. Rossignol S, Bouyer L, Barthelemy D, et al. Recovery of locomotion in the cat following spinal cord lesions. Brain Res Brain Res Rev 2002; 40:257-266.
239. Rossignol S, Chau C, Giroux N, et al. The cat model of spinal injury. Prog Brain Res 2002; 137:151-168.
240. Mushahwar VK, Gillard DM, Gauthier MJ, Prochazka A. Intraspinal micro stimulation generates locomotor-like and feedback-controlled movements. IEEE Trans Neural Syst Rehabil Eng 2002; 10:68-81.
241. Levi AD, Dancausse H, Li X, et al. Peripheral nerve grafts promoting central nervous system regeneration after spinal cord injury in the primate. J Neurosurg 2002; 96 (2 Suppl.): 197-205. Therapeutic intervention, with modest success, in the primate.
242. Garcia-Miguel MJ, Lain AH, Ramon-Cueto A, Cavada C. Lower limb motor function test and postlesional care and evolution of paraplegic macaque monkeys. Soc Neurosci Abstracts 2003; 275:4.
243. Nicolelis MA. Brain-machine interfaces to restore motor function and probe neural circuits. Nat Rev Neurosci 2003; 4:417-422.
244. Prochazka A, Mushahwar VK, McCreery DB. Neural prostheses. J Physiol 2001; 533:99-109.
245. Jezernik S, Craggs M, Grill WM, et al. Electrical stimulation for the treatment of bladder dysfunction: current status and future possibilities. Neurol Res 2002; 24:413-430.
246. Grill WM, McDonald JW, Peckham PH, et al. At the interface: convergence of neural regeneration and neural prostheses for restoration of function. J Rehabil Res Dev 2001; 38:633-639.
247. Mussa-Ivaldi FA, Miller LE. Brain-machine interfaces: computational demands and clinical needs meet basic neuroscience. Trends Neurosci 2003; 26(6):329-334.
248. Popovic MB. Control of neural prostheses for grasping and reaching. Med Eng Phys 2003; 25:41-50.
249. Peckham PH, Kilgore KL, Keith MW, et al. An advanced neuroprosthesis for restoration of hand and upper arm control using an implantable controller. J Hand Surg (Am) 2002; 27:265-276.
250. Peckham PH, Keith MW, Kilgore KL, et al. Efficacy of an implanted neuroprosthesis for restoring hand grasp in tetraplegia: a multicenter study. Arch Phys Med Rehabil 2001; 82:1380-1388.
251. Gustafson KJ, Creasey GH, Grill WM. A catheter based method to activate urethral sensory nerve fibers. J Urol 2003; 170:126-129.
252. Mushahwar VK, Collins DF, Prochazka A. Spinal cord microstimulation generates functional limb movements in chronically implanted cats. Exp Neurol 2000; 163:422-429.
253. Taylor DM, Tillery SI, Schwartz AB. Direct cortical control of 3D neuroprosthetic devices. Science 2002; 296:1829-1832.
254. Taylor DM, Tillery SI, Schwartz AB. Information conveyed through brain-control: cursor versus robot. IEEE Trans Neural Syst Rehabil Eng 2003; 11:195-199.
255. Reina GA, Moran DW, Schwartz AB. On the relationship between joint angular velocity and motor cortical discharge during reaching. J Neurophysiol 2001; 85:2576-2589.
256. Carmena JM, Lebedev MA, Crist RE, et al. Learning to control a brain-machine interface for reaching and grasping by primates. PLoS Biol 2003; 1:1-16.
257. Mojarradi M, Binkley D, Blalock B, et al. A miniaturized neuroprosthesis suitable for implantation into the brain. IEEE Trans Neural Syst Rehabil Eng 2003; 11:38-42.
258. Shenoy KV, Meeker D, Cao S, et al. Neural prosthetic control signals from plan activity. Neuroreport 2003; 14:591-596.