Conduction failure following spinal cord injury: Functional and anatomical changes from acute to chronic stages

Journal of Neuroscience

Volumn 31, Issue 50, 2011, Pages 18543-18555

  James, Nicholas D ^a   Bartus, Katalin ^a   Grist, John ^a   Bennett, David L H ^a   McMahon, Stephen B ^a   Bradbury, Elizabeth J ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTUSION; COOLING; DEMYELINATION; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; FEMALE; FUNCTIONAL STATUS; IMMUNOHISTOCHEMISTRY; LOCOMOTION; NERVE BLOCK; NERVE CONDUCTION DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; REMYELINIZATION; SPINAL CORD INJURY; SPINAL CORD LESION; SPINE;

ACTION POTENTIALS; ANIMALS; AXONS; FEMALE; NEURAL CONDUCTION; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SPINAL CORD INJURIES; TIME FACTORS;

EID: 83455199070     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4306-11.2011     Document Type: Article

References (60)

1. Alilain WJ, Horn KP, Hu H, Dick TE, Silver J (2011) Functional regeneration of respiratory pathways after spinal cord injury. Nature 475:196-200
2. Alto LT, Havton LA, Conner JM, Hollis Ii ER, Blesch A, Tuszynski MH (2009) Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury. Nat Neurosci 12:1106-1113
3. Atkinson PP, Atkinson JL (1996) Spinal shock. Mayo Clin Proc 71:384-389
4. Barakat DJ, Gaglani SM, Neravetla SR, Sanchez AR, Andrade CM, Pressman Y, Puzis R, Garg MS, Bunge MB, Pearse DD (2005) Survival, integration, and axon growth support of glia transplanted into the chronically contused spinal cord. Cell Transplant 14:225-240
5. Basso DM, Beattie MS, Bresnahan JC (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1-21
6. Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, Anderson DK, Faden AI, Hsu CY, Noble LJ, Salzman S, Young W (1997) Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 148:453-463
7. Beaumont E, Onifer SM, Reed WR, Magnuson DS (2006) Magnetically evoked inter-enlargement response: an assessment of ascending propriospinal fibers following spinal cord injury. Exp Neurol 201:428-440
8. Blakemore WF, Murray JA (1981) Quantitative examination of internodal length of remyelinated nerve fibres in the central nervous system. J Neurol Sci 49:273-284
9. Blight AR (1983) Axonal physiology of chronic spinal cord injury in the cat: intracellular recording in vitro. Neuroscience 10:1471-1486
10. Bostock H, Sherratt RM, Sears TA (1978) Overcoming conduction failure in demyelinated nerve fibres by prolonging action potentials. Nature 274:385-387
11. Bradbury EJ, Carter LM (2011) Manipulating the glial scar: chondroitinase ABC as a therapy for spinal cord injury. Brain Res Bull 84:306-316
12. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640
13. Bruce JH, Norenberg MD, Kraydieh S, Puckett W, Marcillo A, Dietrich D (2000) Schwannosis: role of gliosis and proteoglycan in human spinal cord injury. J Neurotrauma 17:781-788
14. Bunge RP, Puckett WR, Becerra JL, Marcillo A, Quencer RM (1993) Observations on the pathology of human spinal cord injury. A review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. Adv Neurol 59:75-89
15. Cafferty WB, Duffy P, Huebner E, Strittmatter SM (2010) MAG and OMgp synergize with Nogo-A to restrict axonal growth and neurological recovery after spinal cord trauma. J Neurosci 30:6825-6837
16. Cao Q, Zhang YP, Iannotti C, DeVries WH, Xu XM, Shields CB, Whittemore SR (2005) Functional and electrophysiological changes after graded traumatic spinal cord injury in adult rat. Exp Neurol 191 [Suppl 1]:S3-S16.
17. Cao Q, He Q, Wang Y, Cheng X, Howard RM, Zhang Y, DeVries WH, Shields CB, Magnuson DS, Xu XM, Kim DH, Whittemore SR (2010) Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. J Neurosci 30:2989-3001
18. Dumont RJ, Okonkwo DO, Verma S, Hurlbert RJ, Boulos PT, Ellegala DB, Dumont AS (2001) Acute spinal cord injury, Part I: Pathophysiologic mechanisms. Clin Neuropharmacol 24:254-264
19. Ellingson BM, Kurpad SN, Schmit BD (2008) Characteristics of mid-to long-latency spinal somatosensory evoked potentials following spinal trauma in the rat. J Neurotrauma 25:1323-1334
20. Fawcett JW, Asher RA (1999) The glial scar and central nervous system repair. Brain Res Bull 49:377-391
21. Fitch MT, Silver J (2008) CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp Neurol 209:294-301
22. Franklin RJ, Blakemore WF (1993) Requirements for Schwann cell migration within CNS environments: a viewpoint. Int J Dev Neurosci 11:641-649
23. Guest JD, Hiester ED, Bunge RP (2005) Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Exp Neurol 192:384-393
24. Hagg T, Oudega M (2006) Degenerative and spontaneous regenerative processes after spinal cord injury. J Neurotrauma 23:264-280
25. Hains BC, Saab CY, Lo AC, Waxman SG (2004) Sodium channel blockade with phenytoin protects spinal cord axons, enhances axonal conduction, and improves functional motor recovery after contusion SCI. Exp Neurol 188:365-377
26. Hellal F, Hurtado A, Ruschel J, Flynn KC, Laskowski CJ, Umlauf M, Kapitein LC, Strikis D, Lemmon V, Bixby J, Hoogenraad CC, Bradke F (2011) Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 331:928-931
27. Hubscher CH, Johnson RD (2006) Chronic spinal cord injury induced changes in the responses of thalamic neurons. Exp Neurol 197:177-188
28. Hunanyan AS, García-Alías G, Alessi V, Levine JM, Fawcett JW, Mendell LM, Arvanian VL (2010) Role of chondroitin sulfate proteoglycans in axonal conduction in mammalian spinal cord. J Neurosci 30:7761-7769
29. Iaci JF, Vecchione AM, Zimber MP, Caggiano AO (2007) Chondroitin sulfate proteoglycans in spinal cord contusion injury and the effects of chondroitinase treatment. J Neurotrauma 24:1743-1759
30. Jones LL, Margolis RU, Tuszynski MH (2003) The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp Neurol 182:399-411
31. Kakulas BA (1999) A review of the neuropathology of human spinal cord injury with emphasis on special features. J Spinal Cord Med 22:119-124
32. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Morshead CM, Fehlings MG (2006) Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J Neurosci 26:3377-3389
33. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O (2005) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25:4694-4705
34. Khan T, Havey RM, Sayers ST, Patwardhan A, King WW (1999) Animal models of spinal cord contusion injuries. Lab Anim Sci 49:161-172
35. Lasiene J, Shupe L, Perlmutter S, Horner P (2008) No evidence for chronic demyelination in spared axons after spinal cord injury in a mouse. J Neurosci 28:3887-3896
36. McDonald WI, Sears TA (1969) Effect of demyelination on conduction in the central nervous system. Nature 221:182-183
37. Metz GA, Whishaw IQ (2002) Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate foreand hindlimb stepping, placing, and co-ordination. J Neurosci Methods 115:169-179
38. Metz GA, Curt A, van de Meent H, Klusman I, Schwab ME, Dietz V (2000) Validation of the weight-drop contusion model in rats: a comparative study of human spinal cord injury. J Neurotrauma 17:1-17
39. Nashmi R, Fehlings MG (2001) Changes in axonal physiology and morphology after chronic compressive injury of the rat thoracic spinal cord. Neuroscience 104:235-251
40. Nashmi R, Imamura H, Tator CH, Fehlings MG (1997) Serial recording of somatosensory and myoelectric motor evoked potentials: role in assessing functional recovery after graded spinal cord injury in the rat. J Neurotrauma 14:151-159
41. + channels after chronic spinal cord injury. Eur J Neurosci 12:491-506
42. Norenberg MD, Smith J, Marcillo A (2004) The pathology of human spinal cord injury: defining the problems. J Neurotrauma 21:429-440
43. Onifer SM, Nunn CD, Decker JA, Payne BN, Wagoner MR, Puckett AH, Massey JM, Armstrong J, Kaddumi EG, Fentress KG, Wells MJ, West RM, Calloway CC, Schnell JT, Whitaker CM, Burke DA, Hubscher CH (2007) Loss and spontaneous recovery of forelimb evoked potentials in both the adult rat cuneate nucleus and somatosensory cortex following contusive cervical spinal cord injury. Exp Neurol 207:238-247
44. Rabchevsky AG, Fugaccia I, Sullivan PG, Scheff SW (2001) Cyclosporin A treatment following spinal cord injury to the rat: behavioral effects and stereological assessment of tissue sparing. J Neurotrauma 18:513-522
45. Rasminsky M (1973) The effects of temperature on conduction in demyelinated single nerve fibers. Arch Neurol 28:287-292
46. Reier PJ, Stensaas LJ, Guth L (1983) The astrocytic scar as an impediment to regeneration in the central nervous system. In: Spinal cord reconstruction (Kao CC, Bunge RP, Reier PJ, eds), pp 163-195. New York: Raven.
47. Salazar DL, Uchida N, Hamers FP, Cummings BJ, Anderson AJ (2010) Human neural stem cells differentiate and promote locomotor recovery in an early chronic spinal cord injury NOD-scid mouse model. PLoS One 5:e12272.
48. Scheff SW, Rabchevsky AG, Fugaccia I, Main JA, Lumpp JE Jr (2003) Experimental modeling of spinal cord injury: characterization of a forcedefined injury device. J Neurotrauma 20:179-193
49. Sharma HS, Westman J, Olsson Y, Alm P (1996) Involvement of nitric oxide in acute spinal cord injury: an immunocytochemical study using light and electron microscopy in the rat. Neurosci Res 24:373-384
50. Shuman SL, Bresnahan JC, Beattie MS (1997) Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J Neurosci Res 50:798-808
51. Smith KJ, Felts PA, John GR (2000) Effects of 4-aminopyridine on demyelinated axons, synapses and muscle tension. Brain 123:171-184
52. Smith PM, Jeffery ND (2005) Spinal shock-comparative aspects and clinical relevance. J Vet Intern Med 19:788-793
53. Springer JE, Rao RR, Lim HR, Cho SI, Moon GJ, Lee HY, Park EJ, Noh JS, Gwag BJ (2010) The functional and neuroprotective actions of Neu2000, a dual-acting pharmacological agent, in the treatment of acute spinal cord injury. J Neurotrauma 27:139-149
54. Tang X, Davies JE, Davies SJ (2003) 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 71:427-444
55. Tator CH, Fehlings MG (1991) Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J Neurosurg 75:15-26
56. Totoiu MO, Keirstead HS (2005) Spinal cord injury is accompanied by chronic progressive demyelination. J Comp Neurol 486:373-383
57. Waxman SG (1989) Demyelination in spinal cord injury. J Neurol Sci 91:1-14
58. Winkler T, Sharma HS, Stålberg E, Badgaiyan RD, Alm P, Westman J (1998) Spinal cord evoked potentials and edema in the pathophysiology of rat spinal cord injury. Involvement of nitric oxide. Amino Acids 14:131-139
59. Zawadzka M, Rivers LE, Fancy SP, Zhao C, Tripathi R, Jamen F, Young K, Goncharevich A, Pohl H, Rizzi M, Rowitch DH, Kessaris N, Suter U, Richardson WD, Franklin RJ (2010) CNS-resident glial progenitor/ stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6:578-590
60. Zorner B, Schwab ME (2010) Anti-Nogo on the go: from animal models to a clinical trial. Ann N Y Acad Sci 1198 [Suppl 1]:E22-E34