Corticospinal regeneration into lumbar grey matter correlates with locomotor recovery after complete spinal corel transection and repair with peripheral nerve grafts, fibroblast growth factor 1, fibrin glue, and spinal fusion

Journal of Neuropathology and Experimental Neurology

Volumn 64, Issue 3, 2005, Pages 230-244

  Tsai, Eve C ^a   Krassioukov, Andrei V ^b   Tator, Charles H ^c  

^a TORONTO WESTERN HOSPITAL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Axonal regeneration; Central pattern generator; Functional recovery; Peripheral nerve grafts; Spinal cord injury

Indexed keywords

CALCITONIN; FIBRIN GLUE; FIBROBLAST GROWTH FACTOR 1;

ANALYSIS OF VARIANCE; ARTICLE; ELECTROPHYSIOLOGY; EVOKED MUSCLE RESPONSE; FLUORESCENCE MICROSCOPY; FUNCTIONAL ASSESSMENT; GRAY MATTER; IMMUNOHISTOCHEMISTRY; LINEAR REGRESSION ANALYSIS; LOCOMOTION; LUMBAR SPINE; NERVE FIBER; NERVE FIBER REGENERATION; NERVE GRAFT; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; RAPHESPINAL TRACT; RAT; RETICULOSPINAL TRACT; RUBROSPINAL TRACT; SEROTONINERGIC SYSTEM; SPINAL CORD TRANSSECTION; SPINE FUSION; TISSUE REPAIR; VESTIBULOSPINAL TRACT;

EID: 15244344434     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnen/64.3.230     Document Type: Article

References (56)

1. Z'Graggen WJ, Metz GA, Kartje GL, et al. Functional recovery and enhanced corticofugal plasticity after unilateral pyramidal tract lesion and blockade of myelin-associated neurite growth inhibitors in adult rats. J Neurosci 1998;18:4744-57
2. Lee YS, Lin CY, Robertson RT, et al. Motor recovery and anatomic evidence of axonal regrowth in spinal cord-repaired adult rats. J Neuropathol Exp Neurol 2004;63:233-45
3. Cheng H, Cao Y, Olson L. Spinal cord repair in adult paraplegic rats: Partial restoration of hind limb function. Science 1996;273:510-13
4. Ramon-Cueto A, Cordero MI, Santos-Benito FF, et al. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000;25:425-35
5. Rapalino O, Lazarov-Spiegler O, Agranov E, et al. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 1998;4:814-21
6. 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;21:9334-44
7. Thallmair M, Metz GA, Z'Graggen WJ, et al. Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat Neurosci 1998;1:124-31
8. Tsai EC, van Bendegem RL, Hwang SW, Tatar CH. A novel method for simultaneous anterograde and retrograde labeling of spinal cord motor tracts in the same animal. J Histochem Cytochem 2001;49:1111-22
9. Basso DM, Beattie MS, Bresnahan JC, et al. MASCIS evaluation of open field locomotor scores: Effects of experience and teamwork on reliability: Multicenter Animal Spinal Cord Injury Study. J Neurotrauma 1996;13:343-59
10. Basso DM, Beattie MS, Bresnahan JC. Graded histologic and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 1996;139:244-56
11. 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
12. Koyanagi I, Tator CH. Effect of a single huge dose of methylprednisolone on blood flow, evoked potentials, and histology after acute spinal cord injury in the rat. Neurol Res 1997;19:289-99
13. Nashmi R, Imamura H, Tator CH, et al. Serial recording of somatosensory and myoelectric motor evoked potentials: Role in assessing functional recovery after graded spinal cord injury in the rat. J Neurotrauma 1997;14:151-59
14. Agrawal SK, Theriault E, Fehlings MG. Role of group I metabotropic glutamate receptors in traumatic spinal cord white matter injury. J Neurotrauma 1998;15:929-41
15. Fitch MT, Doller C, Combs CK, et al. Cellular and molecular mechanisms of glial scarring and progressive cavitation: In vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J Neurosci 1999;19:8182-98
16. Popovich PG, Wei P, Stokes BT. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J Comp Neurol 1997;377:443-64
17. Brook GA, Plate D, Franzen R, et al. Spontaneous longitudinally orientated axonal regeneration is associated with the Schwann cell framework within the lesion site following spinal cord compression injury of the rat. J Neurosci Res 1998;53:51-65
18. Levine JM, Nishiyama A. The NG2 chondroitin sulfate proteoglycan: A multifunctional proteoglycan associated with immature cells. Perspect Dev Neurobiol 1996;3:245-59
19. Merchenthaler I. Neurons with access to the general circulation in the central nervous system of the rat: A retrograde tracing study with fluoro-gold. Neuroscience 1991;44:655-62
20. Chen A, Xu XM, Kleitman N, et al. Methylprednisolone administration improves axonal regeneration into Schwann cell grafts in transected adult rat thoracic spinal cord. Exp Neurol 1996;138:261-76
21. Krenz NR, Weaver LC. CGRP expression increases in the ventral horn rostral to spinal cord transection. Neuroreport 1996;7:2859-62
22. Krenz NR, Weaver LC. Sprouting of primary afferent fibers after spinal cord transection in the rat. Neuroscience 1998;85:443-58
23. Marchetti C, Beato M, Nistri A. Alternating rhythmic activity induced by dorsal root stimulation in the neonatal rat spinal cord in vitro. J Physiol 2001;530(Pt 1):105-12
24. Morgenstern DA, Asher RA, Naidu M, et al. Expression and glycanation of the NG2 proteoglycan in developing, adult, and damaged peripheral nerve. Mol Cell Neurosci 2003;24:787-802
25. McTigue DM, Wei P, Stokes BT. Proliferation of NG2-posirive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J Neurosci 2001;21:3392-400
26. Pallini R. Anatomy of 'regenerating axons.' Science 1998;280:181-82
27. Pataky DM, Borisoff JF, Femandes KJ, et al. Fibroblast growth factor treatment produces differential effects on survival and neurite outgrowth from identified bulbospinal neurons in vitro. Exp Neurol 2000;163:357-72
28. Lee YS, Baratta J, Yu J, et al. AFGF promotes axonal growth in rat spinal cord organotypic slice co-cultures. J Neurotrauma 2002;19:357-67
29. Richardson PM, Issa VM, Aguayo AJ. Regeneration of long spinal axons in the rat. J Neurocytol 1984;13:165-82
30. Richardson PM, McGuinness UM, Aguayo AJ. Peripheral nerve autografts to the rat spinal cord: Studies with axonal tracing methods. Brain Res 1982;237:147-62
31. Richardson PM, McGuinness UM, Aguayo AJ. Axons from CNS neurons regenerate into PNS grafts. Nature 1980;284:264-65
32. Raineteau O, Z'Graggen WJ, Thallmair M, et al. Sprouting and regeneration after pyramidotomy and blockade of the myelin-associated neunte growth inhibitors NI 35/250 in adult rats. Eur J Neurosci 1999;11:1486-90
33. Brosamle C, Huber AB, Fiedler M, et al. Regeneration of lesioned corticospinal tract fibers in the adult rat induced by a recombinant, humanized IN-1 antibody fragment. J Neurosci 2000;20:8061-68
34. Tatar CH. Quantification of retrograde degeneration in corticospinal tract fibers. J Neurosurg 1989;70:655-56
35. Feraboli-Lohnherr D, Barthe JY, Orsal D. Serotonin-induced activation of the network for locomotion in adult spinal rats. J Neurosci Res 1999;55:87-98
36. Antri M, Orsal D, Barthe JY. Locomotor recovery in the chronic spinal rat: Effects of long-term treatment with a 5-HT2 agonist. Eur J Neurosci 2002;16:467-76
37. Ribotta MG, Provencher J, Feraboli-Lohnherr D, et al. Activation of locomotion in adult chronic spinal rats is achieved by transplantation of embryonic raphe cells reinnervating a precise lumbar level. J Neurosci 2000;20:5144-52
38. Gasser UE, Dravid AR. Noradrenergic, serotonergic, and cholinergic sprouting in the hippocampus that follows partial or complete transection of the septohippocampal pathway: Contributions of spared inputs. Exp Neurol 1987;96:352-64
39. Jackisch R, Neufang B, Hertting G, et al. Sympathetic sprouting: time course of changes of noradrenergic, cholinergic, and serotonergic markers in the denervated rat hippocampus. J Neurochem 1995;65:329-37
40. Thota A, Carlson S, Jung R. Recovery of locomotor function after treadmill training of incomplete spinal cord injured rats. Biomed Sci Instrum 2001;37:63-67
41. Smith JL, Edgerton VR, Eldred E, et al. The chronic spinalized cat: A model for neuromuscular plasticity. Birth Defects Orig Artic Ser 1983;73:357-73
42. Lovely RG, Gregor RJ, Roy RR, et al. Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat. Exp Neurol 1986;92:421-35
43. Lovely RG, Gregor RJ, Roy RR, et al. Weight-bearing hindlimb stepping in treadmill-exercised adult spinal cats. Brain Res 1990;514:206-18
44. McDonald JW, Gottlieb DI, Choi DW. Reply to "What is a functional recovery after spinal cord injury?" Nat Med 2000;6:358
45. Privat A, Ribotta MG, Orsal D. What is a functional recovery after spinal cord injury? Nat Med 2000;6:358
46. Eyre JA, Miller S, Clowry GJ, et al. Functional corticospinal projections are established prenatally in the human fetus permitting involvement in the development of spinal motor centers. Brain 2000;123(Pt 1): 51-64
47. Hase T, Kawaguchi S, Hayashi H, et al. Spinal cord repair in neonatal rats: a correlation between axonal regeneration and functional recovery. Eur J Neurosci 2002;15:969-74
48. Kwon BK, Liu J, Messerer C, et al. Survival and regeneration of rubrospinal neurons 1 year after spinal cord injury. Proc Natl Acad Sci USA 2002;99:3246-51
49. Plant GW, Bates ML, Bunge MB. Inhibitory proteoglycan immunoreactivity is higher at the caudal than the rostral Schwann cell graft-transected spinal cord interface. Mol Cell Neurosci 2001;17:471-87
50. Lemons ML, Howland DR, Anderson DK. Chondroitin sulfate proteoglycan immunoreactivity increases following spinal cord injury and transplantation. Exp Neurol 1999;160:51-65
51. Zuo J, Neubauer D, Dyess K, et al. Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp Neurol 1998;154:654-62
52. Senoo E, Tamaki N, Fujimoto E, et al. Effects of prelesioned peripheral nerve graft on nerve regeneration in the rat spinal cord. Neurosurgery 1998;42:1347-56
53. Sims TJ, Durgun MB, Gilmore SA. Transplantation of sciatic nerve segments into normal and glia-depleted spinal cords. Exp Brain Res 1999;125:495-501
54. Nieto-Sampedro M. Neurite outgrowth inhibitors in gliotic tissue. Adv Exp Med Biol 1999;468:207-24
55. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull 1999;49:377-91
56. Bradbury EJ, Moon LD, Popat RJ, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002;416:636-40