Neurotrophic factors promote and enhance locomotor recovery in untrained spinalized cats

Journal of Neurophysiology

Volumn 98, Issue 4, 2007, Pages 1988-1996

  Boyce, Vanessa S ^a   Tumolo, Maureen ^a   Fischer, Itzhak ^a   Murray, Marion ^a   Lemay, Michel A ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLOSPORIN A; NEUROTROPHIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL BASED GENE THERAPY; CELL TRANSPLANTATION; CHRONICITY; CONTROLLED STUDY; CONVALESCENCE; FEMALE; FIBROBLAST; INTERMETHOD COMPARISON; KINEMATICS; KINESIOTHERAPY; LOCOMOTION; MOTOR PERFORMANCE; NERVE FIBER GROWTH; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; TIME; TRAINING; TREADMILL EXERCISE; VELOCITY; WEIGHT BEARING;

ANIMALS; BIOMECHANICS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CATS; DATA INTERPRETATION, STATISTICAL; DECEREBRATE STATE; EXERCISE THERAPY; FEMALE; FIBROBLASTS; FUNCTIONAL LATERALITY; HINDLIMB; IMMUNOHISTOCHEMISTRY; LOCOMOTION; NERVE GROWTH FACTORS; NEURONAL PLASTICITY; NEUROTROPHIN 3; SPINAL CORD;

EID: 35348921741     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00391.2007     Document Type: Article

References (50)

1. Arvanian VL, Mendell LM. Acute modulation of synaptic transmission to motoneurons by BDNF in the neonatal rat spinal cord. Eur J Neurosci 14: 1800-1808, 2001.
2. Arvanov VL, Seebach BS, Mendell LM. NT-3 evokes an LTP-like facilitation of AMPA/kainate receptor-mediated synaptic transmission in the neonatal rat spinal cord. J Neurophysiol 84: 752-758, 2000.
3. Barbeau H, Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 412: 84-95, 1987.
4. Belanger M, Drew T, Provencher J, Rossignol S. A comparison of treadmill locomotion in adult cats before and after spinal transection. J Neurophysiol 76: 471-491, 1996.
5. Bem T, Gorska T, Majczynski H, Zmyslowski W. Different patterns of fore-hindlimb coordination during overground locomotion in cats with ventral and lateral spinal lesions. Exp Brain Res 104: 70-80, 1995.
6. Boyce VS, Bhowmik M, Tumolo MA, Tobias CA, Fischer I, Murray M, Lemay MA. Locomotor recovery in spinalized cats using sensorimotor training and transplants of fibroblasts genetically modified to produce BDNF and NT-3 neurotrophins. Soc Neurosci 852.6: 2002.
7. Boyce VS, Tumolo MA, Murray M, Fischer I, Lemay MA. Neurotrophic factors restore locomotor ability in chronic spinal cats without locomotor training. Soc Neurosci 224.10: 2005.
8. Cai LL, Fong AJ, Otoshi CK, Liang Y, Burdick JW, Roy RR, Edgerton VR. Implications of assist-as-needed robotic step training after a complete spinal cord injury on intrinsic strategies of motor learning. J Neurosci 26: 10564-10568, 2006.
9. Cha J, Heng C, Reinkensmeyer DJ, Roy RR, Edgerton VR, De Leon RD. Locomotor ability in spinal rats is dependent on the amount of activity imposed on the hindlimbs during treadmill training. J Neurotrauma 24: 1000-1012, 2007.
10. Conner JM, Lauterborn JC, Yan Q, Gall CM, Varon S. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J Neurosci 17: 2295-2313, 1997.
11. Cote MP, Menard A, Gossard JP. Spinal cats on the treadmill: changes in load pathways. J Neurosci 23: 2789-2796, 2003.
12. de Leon RD, Acosta CN. Effect of robotic-assisted treadmill training and chronic quipazine treatment on hindlimb stepping in spinally transected rats. J Neurotrauma 23: 1147-1163, 2006.
13. de Leon RD, Hodgson JA, Roy RR, Edgerton VR. Full weight-bearing hindlimb standing following stand training in the adult spinal cat. J Neurophysiol 80: 83-91, 1998a.
14. de Leon RD, Hodgson JA, Roy RR, Edgerton VR. Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J Neurophysiol 79: 1329-1340, 1998b.
15. DiStefano PS, Friedman B, Radziejewski C, Alexander C, Boland P, Schick CM, Lindsay RM, Wiegand SJ. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron 8: 983-993, 1992.
16. Drew T, Jiang W, Widajewicz W. Contributions of the motor cortex to the control of the hindlimbs during locomotion in the cat. Brain Res Brain Res Rev 40: 178-191, 2002.
17. Edgerton VR, Leon RD, Harkema SJ, Hodgson JA, London N, Reinkensmeyer DJ, Roy RR, Talmadge RJ, Tillakaratne NJ, Timoszyk W, Tobin A. Retraining the injured spinal cord. J Physiol 533: 15-22, 2001.
18. Eidelberg E, Story JL, Meyer BL, Nystel J. Stepping by chronic spinal cats. Exp Brain Res 40: 241-246, 1980.
19. English AW. Interlimb coordination during stepping in the cat: an electromyographic analysis. J Neurophysiol 42: 229-243, 1979.
20. Franks JN, Boothe HW, Taylor L, Geller S, Carroll GL, Cracas V, Boothe DM. Evaluation of transdermal fentanyl patches for analgesia in cats undergoing onychectomy. J Am Vet Med Assoc 217: 1013-1020, 2000.
21. Gomez-Pinilla F, Ying Z, Opazo P, Roy RR, Edgerton VR. Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. Eur J Neurosci 13: 1078-1084, 2001.
22. Gomez-Pinilla F, Ying Z, Roy RR, Molteni R, Edgerton VR. Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol 88: 2187-2195, 2002.
23. Goslow GEJ, Reinking RM, Stuart DG. The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morphol 141: 1-41, 1973.
24. Grill R, Murai K, Blesch A, Gage FH, Tuszynski MH. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci 17: 5560-5572, 1997.
25. Hayashi Y, Shumsky JS, Connors T, Otsuka T, Fischer I, Tessler A, Murray M. Immunosuppression with either cyclosporine a or FK506 supports survival of transplanted fibroblasts and promotes growth of host axons into the transplant after spinal cord injury. J Neurotrauma 22: 1267-1281, 2005.
26. Helgren ME, Cliffer KD, Torrento K, Cavnor C, Curtis R, DiStefano PS, Wiegand SJ, Lindsay RM. Neurotrophin-3 administration attenuates deficits of pyridoxine-induced large-fiber sensory neuropathy. J Neurosci 17: 372-382, 1997.
27. Himes BT, Liu Y, Solowska JM, Snyder EY, Fischer I, Tessler A. Transplants of cells genetically modified to express neurotrophin-3 rescue axotomized Clarke's nucleus neurons after spinal cord hemisection in adult rats. J Neurosci Res 65: 549-564, 2001.
28. Hongo T, Jankowska E, Lundberg A. The rubrospinal tract. I. Effects on alpha-motoneurones innervating hindlimb muscles in cats. Exp Brain Res 7: 344-364, 1969.
29. Howland DR, Bregman BS, Tessler A, Goldberger ME. Transplants enhance locomotion in neonatal kittens whose spinal cords are transected: a behavioral and anatomical study. Exp Neurol 135: 123-145, 1995.
30. Hutchinson KJ, Gomez-Pinilla F, Crowe MJ, Ying Z, Basso DM. Three exercise paradigms differentially improve sensory recovery after spinal cord contusion in rats. Brain 127: 1403-1414, 2004.
31. Jakeman LB, Wei P, Guan Z, Stokes BT. Brain-derived neurotrophic factor stimulates hindlimb stepping and sprouting of cholinergic fibers after spinal cord injury. Exp Neurol 154: 170-184, 1998.
32. Jin Y, Tessler A, Fischer I, Houle JD. Fibroblasts genetically modified to produce BDNF support regrowth of chronically injured serotonergic axons. Neurorehabil Neural Repair 14: 311-317, 2000.
33. Kunkel-Bagden E, Dai HN, Bregman BS. Recovery of function after spinal cord hemisection in newborn and adult rats: differential effects on reflex and locomotor function. Exp Neurol 116: 40-51, 1992.
34. Leblond H, L'Esperance M, Orsal D, Rossignol S. Treadmill locomotion in the intact and spinal mouse. J Neurosci 23: 11411-11419, 2003.
35. Liu Y, Himes BT, Moul J, Huang W, Chow SY, Tessler A, Fischer I. Application of recombinant adenovirus for in vivo gene delivery to spinal cord. Brain Res 768: 19-29, 1997.
36. Liu Y, Himes BT, Tryon B, Moul J, Chow SY, Jin H, Murray M, Tessler A, Fischer I. Intraspinal grafting of fibroblasts genetically modified by recombinant adenoviruses. Neuroreport 9: 1075-1079, 1998.
37. Liu Y, Kim D, Himes BT, Chow SY, Schallert T, Murray M, Tessler A, Fischer I. Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J Neurosci 19: 4370-4387, 1999.
38. Lovely RG, Gregor RJ, Roy RR, Edgerton VR. Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat. Exp Neurol 92: 421-435, 1986.
39. Lu B. BDNF and activity-dependent synaptic modulation. Learn Mem 10: 86-98, 2003.
40. Lu P, Jones LL, Tuszynski MH. BDNF-expressing marrow stromal cells support extensive axonal growth at sites of spinal cord injury. Exp Neurol 191: 344-360, 2005.
41. Mitsui T, Fischer I, Shumsky JS, Murray M. Transplants of fibroblasts expressing BDNF and NT-3 promote recovery of bladder and hindlimb function following spinal contusion injury in rats. Exp Neurol 194: 410-431, 2005.
42. Nothias JM, Mitsui T, Shumsky JS, Fischer I, Antonacci MD, Murray M. Combined effects of neurotrophin secreting transplants, exercise, and serotonergic drug challenge improve function in spinal rats. Neurorehabil Neural Repair 19: 296-312, 2005.
43. Schwab ME, Bartholdi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 76: 319-370, 1996.
44. Smith JL, Smith LA, Zernicke RF, Hoy M. Locomotion in exercised and nonexercised cats cordotomized at two or twelve weeks of age. Exp Neurol 76: 393-413, 1982.
45. Tessler A. Intraspinal transplants. Ann Neurol 29: 115-123, 1991.
46. Tillakaratne NJ, de Leon RD, Hoang TX, Roy RR, Edgerton VR, Tobin AJ. Use-dependent modulation of inhibitory capacity in the feline lumbar spinal cord. J Neurosci 22: 3130-3143, 2002.
47. von Bartheld CS, Byers MR, Williams R, Bothwell M. Anterograde transport of neurotrophins and axodendritic transfer in the developing visual system. Nature 379: 830-833, 1996.
48. Ying Z, Roy RR, Edgerton VR, Gomez-Pinilla F. Exercise restores levels of neurotrophins and synaptic plasticity following spinal cord injury. Exp Neurol 193: 411-419, 2005.
49. Zar JH. Circular distributions: descriptive statistics. In: Biostatistical Analysis, edited by Ryu T and Snavely SL. Upper Saddle River, NJ: Prentice Hall, 1999a, p. 592-615.
50. Zar JH. Circular distributions: hypothesis testing. In: Biostatistical Analysis, edited by Ryu T and Snavely SL. Upper Saddle River, NJ: Prentice Hall, 1999b, p. 616-663.