Archives of Physical Medicine and Rehabilitation
Volume 88, Issue 12 , Pages 1606-1613 , December 2007

Comparison of Soleus H-Reflex Modulation After Incomplete Spinal Cord Injury in 2 Walking Environments: Treadmill With Body Weight Support and Overground

  • Chetan P. Phadke, PhD

      Affiliations

    • Department of Physical Therapy, University of Florida, Gainesville, FL
    • McKnight Brain Institute, University of Florida, Gainesville, FL
  • ,
  • Samuel S. Wu, PhD

      Affiliations

    • Division of Biostatistics, College of Medicine, University of Florida, Gainesville, FL
    • VA Rehabilitation Outcomes Research Center, Malcolm Randall VAMC, Gainesville, FL
  • ,
  • Floyd J. Thompson, PhD

      Affiliations

    • McKnight Brain Institute, University of Florida, Gainesville, FL
  • ,
  • Andrea L. Behrman, PhD

      Affiliations

    • Department of Physical Therapy, University of Florida, Gainesville, FL
    • VA Brain Rehabilitation Research Center, Malcolm Randall VAMC, Gainesville, FL.
    • Corresponding Author InformationReprint requests to Andrea L. Behrman, PhD, Dept of Physical Therapy, PO Box 100154, University of Florida, Gainesville, FL 32610-0154

References 

  1. Wernig A, Muller S. Laufband locomotion with body weight support improved walking in persons with severe spinal cord injuries. Paraplegia. 1992;30:229–238
  2. Wernig A, Muller S, Nanassy A, Cagol E. Laufband therapy based on ‘rules of spinal locomotion’ is effective in spinal cord injured persons. [published erratum in: Eur J Neurosci 1995;7:1429] Eur J Neurosci. 1995;7:823–829
  3. Behrman AL, Harkema SJ. Locomotor training after human spinal cord injury: a series of case studies. Phys Ther. 2000;80:688–700
  4. Behrman AL, Lawless-Dixon AR, Davis SB, et al. Locomotor training progression and outcomes after incomplete spinal cord injury. Phys Ther. 2005;85:1356–1371
  5. Field-Fote EC, Lindley SD, Sherman AL. Locomotor training approaches for individuals with spinal cord injury: a preliminary report of walking-related outcomes. J Neurol Phys Ther. 2005;29:127–137
  6. Visintin M, Barbeau H. The effects of body weight support on the locomotor pattern of spastic paretic patients. Can J Neurol Sci. 1989;16:315–325
  7. Barbeau H, Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res. 1987;412:84–95
  8. 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. 1998;79:1329–1340
  9. 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. 1986;92:421–435
  10. Lovely RG, Gregor RJ, Roy RR, Edgerton VR. Weight-bearing hindlimb stepping in treadmill-exercised adult spinal cats. Brain Res. 1990;514:206–218
  11. Barbeau H, Wainberg M, Finch L. Description and application of a system for locomotor rehabilitation. Med Biol Eng Comput. 1987;25:341–344
  12. Dietz V. Locomotor training in paraplegic patients. Ann Neurol. 1995;38:965
  13. Behrman AL, Bowden MG, Nair PM. Neuroplasticity after spinal cord injury and training: an emerging paradigm shift in rehabilitation and walking recovery. Phys Ther. 2006;86:1406–1425
  14. Harkema SJ, Hurley SL, Patel UK, Requejo PS, Dobkin BH, Edgerton VR. Human lumbosacral spinal cord interprets loading during stepping. J Neurophysiol. 1997;77:797–811
  15. Thomas SL, Gorassini MA. Increases in corticospinal tract function by treadmill training after incomplete spinal cord injury. J Neurophysiol. 2005;94:2844–2855
  16. Zehr EP. Training-induced adaptive plasticity in human somatosensory reflex pathways. J Appl Physiol. 2006;101:1783–1794
  17. Yang JF, Fung J, Edamura M, Blunt R, Stein RB, Barbeau H. H-reflex modulation during walking in spastic paretic subjects. Can J Neurol Sci. 1991;18:443–452
  18. Fung J, Barbeau H. Effects of conditioning cutaneomuscular stimulation on the soleus H-reflex in normal and spastic paretic subjects during walking and standing. J Neurophysiol. 1994;72:2090–2104
  19. Trimble MH, Kukulka CG, Behrman AL. The effect of treadmill gait training on low-frequency depression of the soleus H-reflex: comparison of a spinal cord injured man to normal subjects. Neurosci Lett. 1998;246:186–188
  20. Capaday C, Stein RB. Amplitude modulation of the soleus H-reflex in the humans during walking and standing. J Neurosci. 1986;6:1308–1313
  21. Hiersemenzel LP, Curt A, Dietz V. From spinal shock to spasticity: neuronal adaptations to a spinal cord injury. Neurology. 2000;54:1574–1582
  22. Knikou M. Plantar cutaneous input modulates differently spinal reflexes in subjects with intact and injured spinal cord. Spinal Cord. 2007;45:69–77
  23. Burke D, Hagbarth KE, Lofstedt L. Muscle spindle activity in man during shortening and lengthening contractions. J Physiol. 1978;277:131–142
  24. Edamura M, Yang JF, Stein RB. Factors that determine the magnitude and time course of human H-reflexes in locomotion. J Neurosci. 1991;11:420–427
  25. Sinkjaer T, Andersen JB, Larsen B. Soleus stretch reflex modulation during gait in humans. J Neurophysiol. 1996;76:1112–1120
  26. Sinkjaer T, Andersen JB, Nielsen JF, Hansen HJ. Soleus long-latency stretch reflexes during walking in healthy and spastic humans. Clin Neurophysiol. 1999;110:951–959
  27. Crone C, Johnsen LL, Biering-Sorensen F, Nielsen JB. Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury. Brain. 2003;126(Pt 2):495–507
  28. Okuma Y, Mizuno Y, Lee RG. Reciprocal Ia inhibition in patients with asymmetric spinal spasticity. Clin Neurophysiol. 2002;113:292–297
  29. Kiser TS, Reese NB, Maresh T, et al. Use of a motorized bicycle exercise trainer to normalize frequency-dependent habituation of the H-reflex in spinal cord injury. J Spinal Cord Med. 2005;28:241–245
  30. Little JW, Halar EM. H-reflex changes following spinal cord injury. Arch Phys Med Rehabil. 1985;66:19–22
  31. Thompson FJ, Parmer R, Reier PJ. Alteration in rate modulation of reflexes to lumbar motoneurons after midthoracic spinal cord injury in the rat (I. Contusion injury). J Neurotrauma. 1998;15:495–508
  32. Thompson FJ, Reier PJ, Uthman B, et al. Neurophysiological assessment of the feasibility and safety of neural tissue transplantation in patients with syringomyelia. J Neurotrauma. 2001;18:931–945
  33. Trimble MH, Behrman AL, Flynn SM, Thigpen MT, Thompson FJ. Acute effects of locomotor training on overground walking speed and H-reflex modulation in individuals with incomplete spinal cord injury. J Spinal Cord Med. 2001;24:74–80
  34. Trimble MH, Kukulka CG, Behrman AL. The effect of treadmill gait training on low-frequency depression of the soleus H-reflex: comparison of a spinal cord injured man to normal subjects. Neurosci Lett. 1998;246:186–188
  35. Maynard FM, Bracken MB, Creasey G, et al. International Standards for Neurological and Functional Classification of Spinal Cord Injury (American Spinal Injury Association). Spinal Cord. 1997;35:266–274
  36. Dobkin BH, Apple D, Barbeau H, et al. Methods for a randomized trial of weight-supported treadmill training versus conventional training for walking during inpatient rehabilitation after incomplete traumatic spinal cord injury. Neurorehabil Neural Repair. 2003;17:153–167
  37. Protas EJ, Holmes SA, Qureshy H, Johnson A, Lee D, Sherwood AM. Supported treadmill ambulation training after spinal cord injury: a pilot study. Arch Phys Med Rehabil. 2001;82:825–831
  38. Finch L, Barbeau H, Arsenault B. Influence of body weight support on normal human gait: development of a gait retraining strategy. Phys Ther. 1991;71:842–855discussion 855-6
  39. Kido A, Tanaka N, Stein RB. Spinal excitation and inhibition decrease as humans age. Can J Physiol Pharmacol. 2004;82:238–248
  40. Schindler-Ivens S, Shields RK. Low frequency depression of H-reflexes in humans with acute and chronic spinal-cord injury. Exp Brain Res. 2000;133:233–241
  41. Van Emmerik RE, McDermott WJ, Haddad JM, Van Wegen EE. Age-related changes in upper body adaptation to walking speed in human locomotion. Gait Posture. 2005;22:233–239
  42. Phadke CP, Wu SS, Thompson FJ, Behrman AL. Soleus H-reflex modulation in response to change in percentage of leg loading in standing after incomplete spinal cord injury. Neurosci Lett. 2006;403:6–10
  43. Nakazawa K, Kawashima N, Akai M. Enhanced stretch reflex excitability of the soleus muscle in persons with incomplete rather than complete chronic spinal cord injury. Arch Phys Med Rehabil. 2006;87:71–75
  44. Garrett M, Kerr T, Caulfield B. Phase-dependent inhibition of H-reflexes during walking in humans is independent of reduction in knee angular velocity. J Neurophysiol. 1999;82:747–753
  45. Chalmers GR, Knutzen KM. Soleus Hoffmann-reflex modulation during walking in healthy elderly and young adults. J Gerontol A Biol Sci Med Sci. 2000;55:B570–B579
  46. Ethier C, Imbeault MA, Ung V, Capaday C. On the soleus H-reflex modulation pattern during walking. Exp Brain Res. 2003;151:420–425
  47. Hollander M, Wolfe DA. Nonparametric statistical methods. New York: John Wiley & Sons; 1999;
  48. Koceja DM, Markus CA, Trimble MH. Postural modulation of the soleus H reflex in young and old subjects. Electroencephalogr Clin Neurophysiol. 1995;97:387–393
  49. Tsuruike M, Koceja DM, Yabe K, Shima N. Age comparison of H-reflex modulation with the Jendrássik maneuver and postural complexity. Clin Neurophysiol. 2003;114:945–953
  50. Schneider C, Capaday C. Progressive adaptation of the soleus H-reflex with daily training at walking backward. J Neurophysiol. 2003;89:648–656
  51. Lee JK, Emch GS, Johnson CS, Wrathall JR. Effect of spinal cord injury severity on alterations of the H-reflex. Exp Neurol. 2005;196:430–440
  52. Schindler-Ivens SM, Shields RK. Soleus H-reflex recruitment is not altered in persons with chronic spinal cord injury. Arch Phys Med Rehabil. 2004;85:840–847
  53. Thompson FJ, Reier PJ, Lucas CC, Parmer R. Altered patterns of reflex excitability subsequent to contusion injury of the rat spinal cord. J Neurophysiol. 1992;68:1473–1486
  54. Taylor S, Ashby P, Verrier M. Neurophysiological changes following traumatic spinal lesions in man. J Neurol Neurosurg Psychiatry. 1984;47:1102–1108
  55. Calancie B, Broton JG, Klose KJ, Traad M, Difini J, Ayyar DR. Evidence that alterations in presynaptic inhibition contribute to segmental hypo- and hyperexcitability after spinal cord injury in man. Electroencephalogr Clin Neurophysiol. 1993;89:177–186
  56. Ferris DP, Aagaard P, Simonsen EB, Farley CT, Dyhre-Poulsen P. Soleus H-reflex gain in humans walking and running under simulated reduced gravity. J Physiol. 2001;530(Pt 1):167–180
  57. Chen G, Patten C. Treadmill training with harness support: selection of parameters for individuals with poststroke hemiparesis. J Rehabil Res Dev. 2006;43:485–498
  58. Beres-Jones JA, Harkema SJ. The human spinal cord interprets velocity-dependent afferent input during stepping. Brain. 2004;127(Pt 10):2232–2246
  59. Visintin M, Barbeau H. The effects of parallel bars, body weight support and speed on the modulation of the locomotor pattern of spastic paretic gait (A preliminary communication). Paraplegia. 1994;32:540–553
  60. Conway BA, Hultborn H, Kiehn O. Proprioceptive input resets central locomotor rhythm in the spinal cat. Exp Brain Res. 1987;68:643–656
  61. Maegele M, Muller S, Wernig A, Edgerton VR, Harkema SJ. Recruitment of spinal motor pools during voluntary movements versus stepping after human spinal cord injury. J Neurotrauma. 2002;19:1217–1229
  62. Wolpaw JR, Lee CL, Calaitges JG. Operant conditioning of primate triceps surae H-reflex produces reflex asymmetry. Exp Brain Res. 1989;75:35–39
  63. Wolpaw JR, Tennissen AM. Activity-dependent spinal cord plasticity in health and disease. Annu Rev Neurosci. 2001;24:807–843
  64. Cote MP, Gossard JP. Step training-dependent plasticity in spinal cutaneous pathways. J Neurosci. 2004;24:11317–11327
  65. Trimble MH, Behrman AL, Flynn SM, Thigpen MT, Thompson FJ. Acute effects of locomotor training on overground walking speed and H-reflex modulation in individuals with incomplete spinal cord injury. J Spinal Cord Med. 2001;24:74–80
  66. Reese NB, Skinner RD, Mitchell D, et al. Restoration of frequency-dependent depression of the H-reflex by passive exercise in spinal rats. Spinal Cord. 2006;44:28–34
  67. Dobkin BH, Harkema SJ, Requejo PS, Edgerton VR. Modulation of locomotor-like EMG activity in subjects with complete and incomplete spinal cord injury. J Neurol Rehabil. 1995;9:183–190
  68. Pepin A, Norman KE, Barbeau H. Treadmill walking in incomplete spinal-cord-injured subjects: 1 (Adaptation to changes in speed). Spinal Cord. 2003;41:257–270

 Supported by the National Institutes of Health (grant no. KO1 HD01348) and VA Rehabilitation Research and Development Service (grant no. F2182C).

 No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated.

PII: S0003-9993(07)01484-0

doi: 10.1016/j.apmr.2007.07.031

Archives of Physical Medicine and Rehabilitation
Volume 88, Issue 12 , Pages 1606-1613 , December 2007