Activity-dependent increase in neurotrophic factors is associated with an enhanced modulation of spinal reflexes after spinal cord injury

Journal of Neurotrauma

Volumn 28, Issue 2, 2011, Pages 299-309

  Côté, Marie Pascale ^a   Azzam, Gregory A ^a   Lemay, Michel A ^a   Zhukareva, Victoria ^a   Houlé, John D ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

complete transaction; cycling; exercise; locomotor training; spinal cord injury

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN 3; NEUROTROPHIN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BICYCLE; CONTROLLED STUDY; EXERCISE; FEMALE; HOFFMANN REFLEX; LUMBAR SPINE; NERVE CELL EXCITABILITY; NERVE STIMULATION; NONHUMAN; PROTEIN EXPRESSION; RAT; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; SPINAL REFLEX; TASK PERFORMANCE; THORACIC SPINE; TIBIAL NERVE; TREADMILL; WESTERN BLOTTING;

ANIMALS; DISEASE MODELS, ANIMAL; EXERCISE THERAPY; FEMALE; NERVE GROWTH FACTORS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; REFLEX; SPINAL CORD INJURIES;

EID: 79951718250     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1594     Document Type: Article

References (73)

1. Beaumont, E., Houlé, J.D., Peterson, C.A., and Gardiner, P.F. (2004). Passive exercise and fetal spinal cord transplant both help to restore motoneuronal properties after spinal cord transection in rats. Muscle Nerve 29, 234-242. (Pubitemid 38166845)
2. Beaumont, E., Kaloustian, S., Rousseau, G., and Cormery, B. (2008). Training improves the electrophysiological properties of lumbar neurons and locomotion after thoracic spinal cord injury in rats. Neurosci. Res. 62, 147-154.
3. Bennett,D.J., Li, Y.,Harvey, P.J., and Gorassini,M. (2001). Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. J. Neurophysiol. 86, 1972-1982.
4. Boorman, G., Becker, W.J., Morrice, B.L., and Lee, R.G. (1992). Modulation of the soleus H-reflex during pedalling in normal humans and in patients with spinal spasticity. J. Neurol. Neurosurg. Psychiatry 55, 1150-1156. (Pubitemid 23010094)
5. Boulenguez, P., Liabeuf, S., Bos, R., Bras, H., Jean-Xavier, C., Brocard, C., Stil, A., Darbon, P., Cattaert, D., Delpire, E., Marsala, M., and Vinay, L. (2010). Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat. Med. 16, 302-307.
6. Boyce, V.S., Tumolo, M., Fischer, I., Murray, M., and Lemay, M.A. (2007). Neurotrophic factors promote and enhance locomotor recovery in untrained spinalized cats. J. Neurophysiol. 98, 1988-1996. (Pubitemid 47584388)
7. Bregman, B.S., Coumans, J.-V., Dai, H.N., Kuhn, P.L., Lynskey, J., McAtee, M., and Sandhu, F. (2002). Transplants and neurotrophic factors increase regeneration and recovery of function after spinal cord injury, in: Progress in Brain Research. L. McKerracher, G. Doucet, and S. Rossignol (eds). Elsevier: Montreal, pps. 258-273.
8. Brooke, J.D., McIlroy, W.E., and Collins, D.F. (1992). Movement features and H-reflex modulation. I. Pedalling versus matched controls. Brain Res. 582, 78-84.
9. Cai, L.L., Courtine, G., Fong, A.J., Burdick, J.W., Roy, R.R., and Edgerton, V.R. (2006). Plasticity of functional connectivity in the adult spinal cord. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 361, 1635-1646. (Pubitemid 44450215)
10. Cao, L., Liu, L., Chen, Z.Y., Wang, L.M., Ye, J.L., Qiu, H.Y., Lu, C.L., and He, C. (2004). Olfactory ensheathing cells genetically modified to secrete GDNF to promote spinal cord repair. Brain 127, 535-549. (Pubitemid 38295471)
11. Capaday, C., and Stein, R.B. (1987). Difference in the amplitude of the human soleus H reflex during walking and running. J. Physiol. 392, 513-522. (Pubitemid 18014319)
12. Crenna, P., and Frigo, C. (1987). Excitability of the soleus Hreflex arc during walking and stepping in man. Exp. Brain Res. 66, 49-60. (Pubitemid 17039272)
13. de Leon, R.D., Hodgson, J.A., Roy, R.R., and Edgerton, V.R. (1998). Full weight-bearing hindlimb standing following stand training in the adult spinal cat. J. Neurophysiol. 80, 83-91. (Pubitemid 28326242)
14. de Leon, R.D., Tamaki, H., Hodgson, J.A., Roy, R.R., and Edgerton, V.R. (1999). Hindlimb locomotor and postural training modulates glycinergic inhibition in the spinal cord of the adult spinal cat. J. Neurophysiol. 82, 359-369. (Pubitemid 29330090)
15. Dolbeare, D., and Houlé, J.D. (2003). Restriction of axonal retraction and promotion of axonal regeneration by chronically injured neurons after intraspinal treatment with glial cell linederived neurotrophic factor (GDNF). J. Neurotrauma 20, 1251-1261. (Pubitemid 37467287)
16. Dupont-Versteegden, E.E., Houlé, J.D., Dennis, R.A., Zhang, J., Knox, M., Wagoner, G., and Peterson, C.A. (2004). Exerciseinduced gene expression in soleus muscle is dependent on time after spinal cord injury in rats. Muscle Nerve 29, 73-81. (Pubitemid 38040559)
17. Edgerton, V.R., de Leon, R.D., Tillakaratne, N., Recktenwald, M.R., Hodgson, J.A., and Roy, R.R. (1997). Use-dependent plasticity in spinal stepping and standing. Adv. Neurol. 72, 233-247.
18. Etlin, A., Blivis, D., Ben-Zwi, M., and Lev-Tov, A. (2010). Long and short multifunicular projections of sacral neurons are activated by sensory input to produce locomotor activity in the absence of supraspinal control. J. Neurosci. 30, 10324-10336.
19. Field-Fote, E.C., Brown, K.M., and Lindley, S.D. (2006). Influence of posture and stimulus parameters on post-activation depression of the soleus H-reflex in individuals with chronic spinal cord injury. Neurosci. Lett. 410, 37-41. (Pubitemid 44667249)
20. Fortun, J., Puzis, R., Pearse, D.D., Gage, F.H., and Bunge, M.B. (2009). Muscle injection of AAV-NT3 promotes anatomical reorganization of CST axons and improves behavioral outcome following SCI. J. Neurotrauma 26, 941-953.
21. Gomez-Pinilla, F., Huie, J.R., Ying, Z., Ferguson, A.R., Crown, E.D., Baumbauer, K.M., Edgerton, V.R., and Grau, J.W. (2007). BDNF and learning: Evidence that instrumental training promotes learning within the spinal cord by up-regulating BDNF expression. Neuroscience 148, 893-906. (Pubitemid 47419189)
22. Gomez-Pinilla, F., Ying, Z., Roy, R.R., Hodgson, J., and Edgerton, V.R. (2004). Afferent input modulates neurotrophins and synaptic plasticity in the spinal cord. J. Neurophysiol. 92, 3423-3432. (Pubitemid 39506320)
23. Grey, M.J., Klinge, K., Crone, C., Lorentzen, J., Biering-Sorensen, F., Ravnborg, M., and Nielsen, J.B. (2008). Post-activation depression of soleus stretch reflexes in healthy and spastic humans. Exp. Brain Res. 185, 189-197. (Pubitemid 351208252)
24. Hashimoto, M., Nitta, A., Fukumitsu, H., Nomoto, H., Shen, L., and Furukawa, S. (2005). Inflammation-induced GDNF improves locomotor function after spinal cord injury. Neuroreport 16, 99-102. (Pubitemid 40250377)
25. Hausdorff, J.M. (2005). Gait variability: methods, modeling and meaning. J. Neuroeng. Rehabil. 2, 19.
26. Hornby, T.G., Kahn, J.H., Wu, M., and Schmit, B.D. (2006). Temporal facilitation of spastic stretch reflexes following human spinal cord injury. J. Physiol. 571, 593-604. (Pubitemid 43329549)
27. Hosoido, T., Motoyama, S., Goto, M., Mori, F., Tajima, T., Hirata, H., and Wada, N. (2009). Characteristics of H- and M-waves recorded from rat forelimbs. Neurosci. Lett. 450, 239-241.
28. Houlé, J.D., Morris, K., Skinner, R.D., Garcia-Rill, E., and Peterson, C.A. (1999). Effects of fetal spinal cord tissue transplants and cycling exercise on the soleus muscle in spinalized rats. Muscle Nerve 22, 846-856. (Pubitemid 29330031)
29. Hultborn, H., Illert, M., Nielsen, J., Paul, A., Ballegaard, M., and Wiese, H. (1996). On the mechanism of the post-activation depression of the H-reflex in human subjects. Exp. Brain Res. 108, 450-462. (Pubitemid 26095298)
30. Hunt, C.C. (1955) Monosynaptic reflex response of spinal motoneurons to graded afferent stimulation. J. Gen. Physiol. 38, 813-852.
31. Hutchinson, K.J., Gomez-Pinilla, F., Crowe, M.J., Ying, Z., and Basso, D.M. (2004). Three exercise paradigms differentially improve sensory recovery after spinal cord contusion in rats. Brain 127, 1403-1414. (Pubitemid 38745518)
32. Ichiyama, R.M., Courtine, G., Gerasimenko, Y.P., Yang, G.J., van den Brand, R., Lavrov, I.A., Zhong, H., Roy, R.R., and Edgerton, V.R. (2008). Step training reinforces specific spinal locomotor circuitry in adult spinal rats. J. Neurosci. 28, 7370-7375.
33. Jakeman, L.B., Wei, P., Guan, Z., and Stokes, B.T. (1998). Brainderived neurotrophic factor stimulates hindlimb stepping and sprouting of cholinergic fibers after spinal cord injury. Exp. Neurol. 154, 170-184. (Pubitemid 28553577)
34. Keeler, B.E., Siegfried, R.N., Liu, G., Miller, K.N., Santi, L., and Houlé, J.D. (2009). Changes in gene expression are maintained over short and long periods of cycling exercise (Ex) after spinal cord injury (SCI) Program No. 563.5 Neuroscience Meeting Planner. Chicago: Society for Neuroscience, Online.
35. Kernell, D., and Hultborn, H. (1990). Synaptic effects on recruitment gain: a mechanism of importance for the input-output relations of motoneurone pools? Brain Res. 507, 176-179. (Pubitemid 20033847)
36. Kiser, T.S., Reese, N.B., Maresh, T., Hearn, S., Yates, C., Skinner, R.D., Pait, T.G., and Garcia-Rill, E. (2005). Use of a motorized bicycle exercise trainer to normalize frequency-dependent habituation of the H-reflex in spinal cord injury. J. Spinal Cord Med. 28, 241-245. (Pubitemid 43108136)
37. Knikou, M. (2010). Neural control of locomotion and traininginduced plasticity after spinal and cerebral lesions. Clin. Neurophysiol. 121, 1655-1668.
38. Koerber, H.R., and Mendell, L.M. (1991). Modulation of synaptic transmission at Ia-afferent fiber connections on motoneurons during high-frequency stimulation: role of postsynaptic target. J. Neurophysiol. 65, 590-597.
39. Lee, J.K., Emch, G.S., Johnson, C.S., and Wrathall, J.R. (2005). Effect of spinal cord injury severity on alterations of the Hreflex. Exp. Neurol. 196, 430-440. (Pubitemid 41607832)
40. Lee, J.K., Johnson, C.S., and Wrathall, J.R. (2007). Up-regulation of 5-HT2 receptors is involved in the increased H-reflex amplitude after contusive spinal cord injury. Exp. Neurol. 203, 502-511. (Pubitemid 46157221)
41. Lloyd, D.P. (1957). Monosynaptic reflex response of individual motoneurons as a function of frequency. J. Gen. Physiol. 40, 435-450.
42. Luckman, S.M., Dyball, R.E., and Leng, G. (1994). Induction of c-fos expression in hypothalamic magnocellular neurons requires synaptic activation and not simply increased spike activity. J. Neurosci. 14, 4825-4830. (Pubitemid 24237904)
43. Ma, Y.H., Zhang, Y., Cao, L., Su, J.C., Wang, Z.W., Xu, A.B., and Zhang, S.C. (2010). Effect of neurotrophin-3 genetically modified olfactory ensheathing cells transplantation on spinal cord injury. Cell Transplant 19, 167-177.
44. Mendell, L.M., and Arvanian, V.L. (2002). Diversity of neurotrophin action in the postnatal spinal cord. Brain Res. Brain Res. Rev. 40, 230-239. (Pubitemid 36183172)
45. Mendell, L.M. (1984). Modifiability of spinal synapses. Physiol. Rev. 64, 260-324. (Pubitemid 14139949)
46. Mendell, L.M., Munson, J.B., and Arvanian, V.L. (2001). Neurotrophins and synaptic plasticity in the mammalian spinal cord. J. Physiol. 533, 91-97. (Pubitemid 32499361)
47. Murray, M., and Goldberger, M.E. (1974). Restitution of function and collateral sprouting in the cat spinal cord: the partially hemisected animal. J. Comp. Neurol. 158, 19-36.
48. Nielsen, J.B., Crone, C., and Hultborn, H. (2007). The spinal pathophysiology of spasticity-from a basic science point of view. Acta Physiol. (Oxf.) 189, 171-180. (Pubitemid 46148327)
49. Novikova, L.N., Novikov, L.N., and Kellerth, J.O. (2002). Differential effects of neurotrophins on neuronal survival and axonal regeneration after spinal cord injury in adult rats. J. Comp. Neurol. 452, 255-263.
50. Novikova, L.N., Novikov, L.N., and Kellerth, J.O. (2000). Survival effects of BDNF and NT-3 on axotomized rubrospinal neurons depend on the temporal pattern of neurotrophin administration. Eur. J. Neurosci. 12, 776-780. (Pubitemid 30142781)
51. Ollivier-Lanvin, K., Keeler, B.E., Siegfried, R., Houlé, J.D., and Lemay, M.A. (2010). Proprioceptive neuropathy affects normalization of the H-reflex by exercise after spinal cord injury. Exp. Neurol. 221, 198-205.
52. Pearson, K.G. (2001). Could enhanced reflex function contribute to improving locomotion after spinal cord repair? J. Physiol. 533, 75-81. (Pubitemid 32499359)
53. Petruska, J.C., Ichiyama, R.M., Jindrich, D.L., Crown, E.D., Tansey, K.E., Roy, R.R., Edgerton, V.R., and Mendell, L.M. (2007). Changes in motoneuron properties and synaptic inputs related to step training after spinal cord transection in rats. J. Neurosci. 27, 4460-4471. (Pubitemid 46640712)
54. Phadke, C.P., Flynn, S.M., Thompson, F.J., Behrman, A.L., Trimble, M.H., and Kukulka, C.G. (2009). Comparison of single bout effects of bicycle training versus locomotor training on paired reflex depression of the soleus H-reflex after motor incomplete spinal cord injury. Arch. Phys. Med. Rehabil. 90, 1218-1228.
55. Reese, N.B., Skinner, R.D., Mitchell, D., Yates, C., Barnes, C.N., Kiser, T.S., and Garcia-Rill, E. (2006). Restoration of frequencydependent depression of the H-reflex by passive exercise in spinal rats. Spinal Cord 44, 28-34. (Pubitemid 43060942)
56. Rivera, C., Li, H., Thomas-Crusells, J., Lahtinen, H., Viitanen, T., Nanobashvili, A., Kokaia, Z., Airaksinen, M.S., Voipio, J., Kaila, K., and Saarma, M. (2002). BDNF-induced TrkB activation down-regulates the K+-Cl- cotransporter KCC2 and impairs neuronal Cl- extrusion. J. Cell Biol. 159, 747-752. (Pubitemid 36008357)
57. Rivera, C., Voipio, J., Thomas-Crusells, J., Li, H., Emri, Z., Sipila, S., Payne, J.A., Minichiello, L., Saarma, M., and Kaila, K. (2004). Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J. Neurosci. 24, 4683-4691. (Pubitemid 38656623)
58. Rojas Vega, S., Abel, T., Lindschulten, R., Hollmann, W., Bloch, W., and Strüder, H.K. (2008). Impact of exercise on neuroplasticity-related proteins in spinal cord injured humans. Neuroscience 153, 1064-1070.
59. Rossignol, S., Dubuc, R., and Gossard, J.-P. (2006). Dynamic sensorimotor interactions in locomotion. Physiol. Rev. 86, 89-154.
60. Schindler-Ivens, S., and Shields, R.K. (2000). Low frequency depression of H-reflexes in humans with acute and chronic spinal-cord injury. Exp. Brain Res. 133, 233-241. (Pubitemid 30449909)
61. Seebach, B.S., Arvanov, V., and Mendell, L.M. (1999). Effects of BDNF and NT-3 on development of Ia/motoneuron functional connectivity in neonatal rats. J. Neurophysiol. 81, 2398-2405. (Pubitemid 29262568)
62. Skinner, R.D., Houlé, J.D., Reese, N.B., Berry, C.L., and Garcia- Rill, E. (1996). Effects of exercise and fetal spinal cord implants on the H-reflex in chronically spinalized adult rats. Brain Res. 729, 127-131. (Pubitemid 26276188)
63. Skup, M., Dwornik, A., Macias, M., Sulejczak, D., Wiater, M., and Czarkowska-Bauch, J. (2002). Long-term locomotor training up-regulates TrkB(FL) receptor-like proteins, brainderived neurotrophic factor, and neurotrophin 4 with different topographies of expression in oligodendroglia and neurons in the spinal cord. Exp. Neurol. 176, 289-307. (Pubitemid 35193346)
64. Thompson, F.J., Reier, P.J., Lucas, C.C., and Parmer, R. (1992). Altered patterns of reflex excitability subsequent to contusion injury of the rat spinal cord. J. Neurophysiol. 68, 1473-1486.
65. van den Berg-Emons, R., Bussmann, J.B., Haisma, J.A., Sluis, T.A., van der Woude, L.H., Bergen, M.P., and Stam, H.J. (2008). A prospective study on physical activity levels after spinal cord injury during inpatient rehabilitation and the year after discharge. Arch. Phys. Med. Rehabil. 89, 2094-2101.
66. Xia, R., and Rymer, W.Z. (2005). Reflex reciprocal facilitation of antagonist muscles in spinal cord injury. Spinal Cord 43, 14-21. Yates, C.C., Charlesworth, A., Reese, N.B., Skinner, R.D., and
67. Garcia-Rill, E. (2008b). The effects of passive exercise therapy initiated prior to or after the development of hyperreflexia following spinal transection. Exp. Neurol. 213, 405-409.
68. Yates, C., Charlesworth, A., Allen, S.R., Reese, N.B., Skinner, R.D., and Garcia-Rill, E. (2008a). The onset of hyperreflexia in the rat following complete spinal cord transection. Spinal Cord 46, 798-803.
69. Ye, J.H., and Houlé, J.D. (1997). Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 143, 70-81. (Pubitemid 27049133)
70. Ying, Z., Roy, R.R., Edgerton, V.R., and Gomez-Pinilla, F. (2005). Exercise restores levels of neurotrophins and synaptic plasticity following spinal cord injury. Exp. Neurol. 193, 411-419. (Pubitemid 40626768)
71. Ying, Z., Roy, R.R., Zhong, H., Zdunowski, S., Edgerton, V.R., and Gomez-Pinilla, F. (2008). BDNF-exercise interactions in the recovery of symmetrical stepping after a cervical hemisection in rats. Neuroscience 155, 1070-1078.
72. Zhou, H.L., Yang, H.J., Li, Y.M., Wang, Y., Yan, L., Guo, X.L., Ba, Y.C., Liu, S., and Wang, T.H. (2008). Changes in Glial cell linederived neurotrophic factor expression in the rostral and caudal stumps of the transected adult rat spinal cord. Neurochem. Res. 33, 927-937.
73. Ziegler, M.D., Zhong, H., Roy, R.R., and Edgerton, V.R. (2010). Why variability facilitates spinal learning. J. Neurosci. 30, 10720-10726.