Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2012 (2012), Article ID 254948, 13 pages
http://dx.doi.org/10.1155/2012/254948
Review Article

Plasticity of Corticospinal Neural Control after Locomotor Training in Human Spinal Cord Injury

Maria Knikou1,2,3,4

1Graduate Center and Physical Therapy Department, College of Staten Island, City University of New York, Staten Island, NY 10314, USA
2Physical Medicine and Rehabilitation, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA
3Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, IL 60611-2654, USA
4Electrophysiological Analysis of Gait and Posture Laboratory, Rehabilitation Institute of Chicago, Chicago, IL 60611, USA

Received 14 February 2012; Revised 9 April 2012; Accepted 10 April 2012

Academic Editor: Marie-Hélène Canu

Copyright © 2012 Maria Knikou. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. O. Raineteau and M. E. Schwab, “Plasticity of motor systems after incomplete spinal cord injury,” Nature Reviews Neuroscience, vol. 2, no. 4, pp. 263–273, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. H. C. Smith, G. Savic, H. L. Frankel et al., “Corticospinal function studied over time following incomplete spinal cord injury,” Spinal Cord, vol. 38, no. 5, pp. 292–300, 2000. View at Google Scholar · View at Scopus
  3. J. H. Kaas, H. X. Qi, M. J. Burish, O. A. Gharbawie, S. M. Onifer, and J. M. Massey, “Cortical and subcortical plasticity in the brains of humans, primates, and rats after damage to sensory afferents in the dorsal columns of the spinal cord,” Experimental Neurology, vol. 209, no. 2, pp. 407–416, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Bruehlmeier, V. Dietz, K. L. Leenders, U. Roelcke, J. Missimer, and A. Curt, “How does the human brain deal with a spinal cord injury?” European Journal of Neuroscience, vol. 10, no. 12, pp. 3918–3922, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Curt, H. Alkadhi, G. R. Crelier, S. H. Boendermaker, M. C. Hepp-Reymond, and S. S. Kollias, “Changes of non-affected upper limb cortical representation in paraplegic patients as assessed by fMRI,” Brain, vol. 125, no. 11, pp. 2567–2578, 2002. View at Google Scholar · View at Scopus
  6. T. Endo, C. Spenger, T. Tominaga, S. Brené, and L. Olson, “Cortical sensory map rearrangement after spinal cord injury: fMRI responses linked to Nogo signalling,” Brain, vol. 130, no. 11, pp. 2951–2961, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. G. W. Huntley, “Correlation between patterns of horizontal connectivity and the extent of short-term representational plasticity in rat motor cortex,” Cerebral Cortex, vol. 7, no. 2, pp. 143–156, 1997. View at Publisher · View at Google Scholar · View at Scopus
  8. D. L. Adkins, J. Boychuk, M. S. Remple, and J. A. Kleim, “Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord,” Journal of Applied Physiology, vol. 101, no. 6, pp. 1776–1782, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. R. D. de Leon, J. A. Hodgson, R. R. Roy, and V. R. Edgerton, “Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats,” Journal of Neurophysiology, vol. 79, no. 3, pp. 1329–1340, 1998. View at Google Scholar · View at Scopus
  10. M. Bélanger, T. Drew, J. Provencher, and S. Rossignol, “A comparison of treadmill locomotion in adult cats before and after spinal transection,” Journal of Neurophysiology, vol. 76, no. 1, pp. 471–491, 1996. View at Google Scholar · View at Scopus
  11. A. Frigon and S. Rossignol, “Adaptive changes of the locomotor pattern and cutaneous reflexes during locomotion studied in the same cats before and after spinalization,” Journal of Physiology, vol. 586, no. 12, pp. 2927–2945, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. G. Barrière, H. Leblond, J. Provencher, and S. Rossignol, “Prominent role of the spinal central pattern generator in the recovery of locomotion after partial spinal cord injuries,” Journal of Neuroscience, vol. 28, no. 15, pp. 3976–3987, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Rossignol, C. Chau, E. Brustein, M. Bélanger, H. Barbeau, and T. Drew, “Locomotor capacities after complete and partial lesions of the spinal cord,” Acta Neurobiologiae Experimentalis, vol. 56, no. 1, pp. 449–463, 1996. View at Google Scholar · View at Scopus
  14. S. Rossignol and A. Frigon, “Recovery of locomotion after spinal cord injury: some facts and mechanisms,” Annual Review of Neuroscience, vol. 34, pp. 413–440, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Barbeau, M. Wainberg, and L. Finch, “Description and application of a system for locomotor rehabilitation,” Medical and Biological Engineering and Computing, vol. 25, no. 3, pp. 341–344, 1987. View at Google Scholar · View at Scopus
  16. H. Barbeau and S. Rossignol, “Recovery of locomotion after chronic spinalization in the adult cat,” Brain Research, vol. 412, no. 1, pp. 84–95, 1987. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Courtine, Y. Gerasimenko, R. Van Den Brand et al., “Transformation of nonfunctional spinal circuits into functional states after the loss of brain input,” Nature Neuroscience, vol. 12, no. 10, pp. 1333–1342, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. R. D. de Leon, J. A. Hodgson, R. R. Roy, and V. R. Edgerton, “Retention of hindlimb stepping ability in adult spinal cats after the cessation of step training,” Journal of Neurophysiology, vol. 81, no. 1, pp. 85–94, 1999. View at Google Scholar · View at Scopus
  19. R. G. Lovely, R. J. Gregor, R. R. Roy, and V. R. Edgerton, “Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat,” Experimental Neurology, vol. 92, no. 2, pp. 421–435, 1986. View at Google Scholar · View at Scopus
  20. Y. Goldshmit, N. Lythgo, M. P. Galea, and A. M. Turnley, “Treadmill training after spinal cord hemisection in mice promotes axonal sprouting and synapse formation and improves motor recovery,” Journal of Neurotrauma, vol. 25, no. 5, pp. 449–465, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. M. J. Oh, T. B. Seo, K. B. Kwon et al., “Axonal outgrowth and Erk1/2 activation by training after spinal cord injury in rats,” Journal of Neurotrauma, vol. 26, no. 11, pp. 2071–2082, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. K. J. Hutchinson, F. Gómez-Pinilla, M. J. Crowe, Z. Ying, and D. M. Basso, “Three exercise paradigms differentially improve sensory recovery after spinal cord contusion in rats,” Brain, vol. 127, no. 6, pp. 1403–1414, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Liu, J. E. Stevens-Lapsley, A. Jayaraman et al., “Impact of treadmill locomotor training on skeletal muscle IGF1 and myogenic regulatory factors in spinal cord injured rats,” European Journal of Applied Physiology, vol. 109, no. 4, pp. 709–720, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. J. C. Petruska, R. M. Ichiyama, D. L. Jindrich et al., “Changes in motoneuron properties and synaptic inputs related to step training after spinal cord transection in rats,” Journal of Neuroscience, vol. 27, no. 16, pp. 4460–4471, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. J. R. Wolpaw and J. S. Carp, “Plasticity from muscle to brain,” Progress in Neurobiology, vol. 78, no. 3–5, pp. 233–263, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. L. L. Cai, G. Courtine, A. J. Fong, J. W. Burdick, R. R. Roy, and V. R. Edgerton, “Plasticity of functional connectivity in the adult spinal cord,” Philosophical Transactions of the Royal Society B, vol. 361, no. 1473, pp. 1635–1646, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. A. L. Behrman, A. R. Lawless-Dixon, S. B. Davis et al., “Locomotor training progression and outcomes after incomplete spinal cord injury,” Physical Therapy, vol. 85, no. 12, pp. 1356–1371, 2005. View at Google Scholar · View at Scopus
  28. A. L. Behrman and S. J. Harkema, “Locomotor training after human spinal cord injury: a series of case studies,” Physical Therapy, vol. 80, no. 7, pp. 688–700, 2000. View at Google Scholar · View at Scopus
  29. V. Dietz, M. Wirz, A. Curt, and G. Colombo, “Locomotor pattern in paraplegic patients: training effects and recovery of spinal cord function,” Spinal Cord, vol. 36, no. 6, pp. 380–390, 1998. View at Google Scholar · View at Scopus
  30. E. C. Field-Fote, “Combined use of body weight support, functional electric stimulation, and treadmill training to improve walking ability in individuals with chronic incomplete spinal cord injury,” Archives of Physical Medicine and Rehabilitation, vol. 82, no. 6, pp. 818–824, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. E. C. Field-Fote and K. E. Roach, “Influence of a locomotor training approach on walking speed and distance in people with chronic spinal cord injury: a randomized clinical trial,” Physical Therapy, vol. 91, no. 1, pp. 48–60, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. J. R. Wolpaw and A. M. Tennissen, “Activity-dependent spinal cord plasticity in health and disease,” Annual Review of Neuroscience, vol. 24, pp. 807–843, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. D. M. Armstrong and T. Drew, “Discharges of pyramidal tract and other motor cortical neurones during locomotion in the cat,” Journal of Physiology, vol. 346, pp. 471–495, 1984. View at Google Scholar · View at Scopus
  34. D. M. Armstrong and T. Drew, “Locomotor-related neuronal discharges in cat motor cortex compared with peripheral receptive fields and evoked movements,” Journal of Physiology, vol. 346, pp. 497–517, 1984. View at Google Scholar · View at Scopus
  35. T. Drew, “Motor cortical activity during voluntary gait modifications in the cat. I. Cells related to the forelimbs,” Journal of Neurophysiology, vol. 70, no. 1, pp. 179–199, 1993. View at Google Scholar · View at Scopus
  36. P. V. Zelenin, T. G. Deliagina, G. N. Orlovsky et al., “Contribution of different limb controllers to modulation of motor cortex neurons during locomotion,” Journal of Neuroscience, vol. 31, no. 12, pp. 4636–4649, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. I. N. Beloozerova and M. G. Sirota, “The role of the motor cortex in the control of accuracy of locomotor movements in the cat,” Journal of Physiology, vol. 461, pp. 1–25, 1993. View at Google Scholar · View at Scopus
  38. T. Drew, “Motor cortical cell discharge during voluntary gait modification,” Brain Research, vol. 457, no. 1, pp. 181–187, 1988. View at Google Scholar · View at Scopus
  39. T. Drew, “Visuomotor coordination in locomotion,” Current Opinion in Neurobiology, vol. 1, no. 4, pp. 652–657, 1991. View at Google Scholar · View at Scopus
  40. K. Seki, N. Kudo, F. Kolb, and T. Yamaguchi, “Effects of pyramidal tract stimulation on forelimb flexor motoneurons during fictive locomotion in cats,” Neuroscience Letters, vol. 230, no. 3, pp. 195–198, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Grillner, “Control of locomotion in bipeds, tetrapods, and fish,” in Handbook of Physiology: The Nervous System, V. B. Brooks, Ed., vol. 2, pp. 1179–1236, American Physiological Society, Bethesda, Md, USA, 1981. View at Google Scholar
  42. S. Rossignol, A. Frigon, G. Barrière et al., “Spinal plasticity in the recovery of locomotion,” Progress in Brain Research, vol. 188, pp. 229–241, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Rossignol, “Plasticity of connections underlying locomotor recovery after central and/or peripheral lesions in the adult mammals,” Philosophical Transactions of the Royal Society B, vol. 361, no. 1473, pp. 1647–1671, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Drew, W. Jiang, and W. Widajewicz, “Contributions of the motor cortex to the control of the hindlimbs during locomotion in the cat,” Brain Research Reviews, vol. 40, no. 1–3, pp. 178–191, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. U. Ziemann, “Transcranial magnetic stimulation at the interface with other techniques: a powerful tool for studying the human cortex,” Neuroscientist, vol. 17, no. 4, pp. 368–381, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Reis, O. B. Swayne, Y. Vandermeeren et al., “Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control,” Journal of Physiology, vol. 586, no. 2, pp. 325–351, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Fukuyama, Y. Ouchi, S. Matsuzaki et al., “Brain functional activity during gait in normal subjects: a SPECT study,” Neuroscience Letters, vol. 228, no. 3, pp. 183–186, 1997. View at Publisher · View at Google Scholar · View at Scopus
  48. I. Miyai, H. C. Tanabe, I. Sase et al., “Cortical mapping of gait in humans: a near-infrared spectroscopic topography study,” NeuroImage, vol. 14, no. 5, pp. 1186–1192, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Suzuki, I. Miyai, T. Ono et al., “Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study,” NeuroImage, vol. 23, no. 3, pp. 1020–1026, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. H. T. Petersen, M. Willerslev-Olsen, B. A. Conway, and J. B. Nielsen, “The motor cortex drives the muscles during walking in human subjects,” Journal of Physiology, vol. 590, no. 10, pp. 2443–2452, 2012. View at Publisher · View at Google Scholar
  51. D. Barthélemy, M. J. Grey, J. B. Nielsen, and L. Bouyer, “Involvement of the corticospinal tract in the control of human gait,” Progress in Brain Research, vol. 192, pp. 181–197, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. D. M. Halliday, J. R. Rosenberg, A. M. Amjad, P. Breeze, B. A. Conway, and S. F. Farmer, “A framework for the analysis of mixed time series/point process data-theory and application to the study of physiological tremor, single motor unit discharges and electromyograms,” Progress in Biophysics and Molecular Biology, vol. 64, no. 2-3, pp. 237–278, 1995. View at Google Scholar · View at Scopus
  53. U. Ziemann and J. C. Rothwell, “I-waves in motor cortex,” Journal of Clinical Neurophysiology, vol. 17, no. 4, pp. 397–405, 2000. View at Google Scholar · View at Scopus
  54. V. Di Lazzaro, U. Ziemann, and R. N. Lemon, “State of the art: physiology of transcranial motor cortex stimulation,” Brain Stimulation, vol. 1, no. 4, pp. 345–362, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Groppa, B. H. Schlaak, A. Münchau et al., “The human dorsal premotor cortex facilitates the excitability of ipsilateral primary motor cortex via a short latency cortico-cortical route,” Human Brain Mapping, vol. 33, no. 2, pp. 419–430, 2012. View at Publisher · View at Google Scholar
  56. J. Nielsen and N. Petersen, “Evidence favouring different descending pathways to soleus motoneurones activated by magnetic brain stimulation in man,” Journal of Physiology, vol. 486, no. 3, pp. 779–788, 1995. View at Google Scholar · View at Scopus
  57. J. Nielsen, H. Morita, J. Baumgarten, N. Petersen, and L. O. Christensen, “On the comparability of H-reflexes and MEPs,” Electroencephalography and Clinical Neurophysiology, vol. 51, pp. 93–101, 1999. View at Google Scholar · View at Scopus
  58. D. Burke, S. C. Gandevia, and B. McKeon, “Monosynaptic and oligosynaptic contributions to human ankle jerk and H-reflex,” Journal of Neurophysiology, vol. 52, no. 3, pp. 435–448, 1984. View at Google Scholar · View at Scopus
  59. S. S. Geertsen, A. T. Zuur, and J. B. Nielsen, “Voluntary activation of ankle muscles is accompanied by subcortical facilitation of their antagonists,” Journal of Physiology, vol. 588, no. 13, pp. 2391–2402, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Schneider, B. A. Lavoie, H. Barbeau, and C. Capaday, “Timing of cortical excitability changes during the reaction time of movements superimposed on tonic motor activity,” Journal of Applied Physiology, vol. 97, no. 6, pp. 2220–2227, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. J. B. Nielsen, “Motoneuronal drive during human walking,” Brain Research Reviews, vol. 40, no. 1–3, pp. 192–201, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. V. Di Lazzaro, D. Restuccia, A. Oliviero et al., “Magnetic transcranial stimulation at intensities below active motor threshold activates intracortical inhibitory circuits,” Experimental Brain Research, vol. 119, no. 2, pp. 265–268, 1998. View at Publisher · View at Google Scholar · View at Scopus
  63. N. T. Petersen, J. E. Butler, V. Marchand-Pauvert et al., “Suppression of EMG activity by transcranial magnetic stimulation in human subjects during walking,” Journal of Physiology, vol. 537, no. 2, pp. 651–656, 2001. View at Publisher · View at Google Scholar · View at Scopus
  64. N. J. Davey, P. Romaiguere, D. W. Maskill, and P. H. Ellaway, “Suppression of voluntary motor activity revealed using transcranial magnetic stimulation of the motor cortex in man,” Journal of Physiology, vol. 477, no. 2, pp. 223–235, 1994. View at Google Scholar · View at Scopus
  65. J. Valls-Solé, A. Pascual-Leone, E. M. Wassermann, and M. Hallett, “Human motor evoked responses to paired transcranial magnetic stimuli,” Electroencephalography and Clinical Neurophysiology, vol. 85, no. 6, pp. 355–364, 1992. View at Publisher · View at Google Scholar · View at Scopus
  66. T. Kujirai, M. D. Caramia, J. C. Rothwell et al., “Corticocortical inhibition in human motor cortex,” Journal of Physiology, vol. 471, pp. 501–519, 1993. View at Google Scholar · View at Scopus
  67. E. M. Wassermann, A. Samii, B. Mercuri et al., “Responses to paired transcranial magnetic stimuli in resting, active, and recently activated muscles,” Experimental Brain Research, vol. 109, no. 1, pp. 158–163, 1996. View at Google Scholar · View at Scopus
  68. H. Nakamura, H. Kitagawa, Y. Kawaguchi, and H. Tsuji, “Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans,” Journal of Physiology, vol. 498, no. 3, pp. 817–823, 1997. View at Google Scholar · View at Scopus
  69. T. D. Sanger, R. R. Garg, and R. Chen, “Interactions between two different inhibitory systems in the human motor cortex,” Journal of Physiology, vol. 530, no. 2, pp. 307–317, 2001. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Ferbert, A. Priori, J. C. Rothwell, B. L. Day, J. G. Colebatch, and C. D. Marsden, “Interhemispheric inhibition of the human motor cortex,” Journal of Physiology, vol. 453, pp. 525–546, 1992. View at Google Scholar · View at Scopus
  71. W. Taube, M. Gruber, S. Beck, M. Faist, A. Gollhofer, and M. Schubert, “Cortical and spinal adaptations induced by balance training: correlation between stance stability and corticospinal activation,” Acta Physiologica, vol. 189, no. 4, pp. 347–358, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. M. A. Perez, B. K. S. Lungholt, K. Nyborg, and J. B. Nielsen, “Motor skill training induces changes in the excitability of the leg cortical area in healthy humans,” Experimental Brain Research, vol. 159, no. 2, pp. 197–205, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. J. L. Jensen, P. C. D. Marstrand, and J. B. Nielsen, “Motor skill training and strength training are associated with different plastic changes in the central nervous system,” Journal of Applied Physiology, vol. 99, no. 4, pp. 1558–1568, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. N. Alexeeva, J. G. Broton, and B. Calancie, “Latency of changes in spinal motoneuron excitability evoked by transcranial magnetic brain stimulation in spinal cord injured individuals,” Electroencephalography and Clinical Neurophysiology, vol. 109, no. 4, pp. 297–303, 1998. View at Publisher · View at Google Scholar · View at Scopus
  75. D. Barthélemy, M. Willerslev-Olsen, H. Lundell et al., “Impaired transmission in the corticospinal tract and gait disability in spinal cord injured persons,” Journal of Neurophysiology, vol. 104, no. 2, pp. 1167–1176, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. B. Calancie, N. Alexeeva, J. G. Broton, S. Suys, A. Hall, and K. J. Klose, “Distribution and latency of muscle responses to transcranial magnetic stimulation of motor cortex after spinal cord injury in humans,” Journal of Neurotrauma, vol. 16, no. 1, pp. 49–67, 1999. View at Google Scholar · View at Scopus
  77. B. Wirth, H. J. A. Van Hedel, and A. Curt, “Changes in corticospinal function and ankle motor control during recovery from incomplete spinal cord injury,” Journal of Neurotrauma, vol. 25, no. 5, pp. 467–478, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. P. Winchester, R. McColl, R. Querry et al., “Changes in supraspinal activation patterns following robotic locomotor therapy in motor-incomplete spinal cord injury,” Neurorehabilitation and Neural Repair, vol. 19, no. 4, pp. 313–324, 2005. View at Publisher · View at Google Scholar · View at Scopus
  79. C. Enzinger, H. Dawes, H. Johansen-Berg et al., “Brain activity changes associated with treadmill training: after stroke,” Stroke, vol. 40, no. 7, pp. 2460–2467, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. S. L. Thomas and M. A. Gorassini, “Increases in corticospinal tract function by treadmill training after incomplete spinal cord injury,” Journal of Neurophysiology, vol. 94, no. 4, pp. 2844–2855, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. J. A. Norton and M. A. Gorassini, “Changes in cortically related intermuscular coherence accompanying improvements in locomotor skills in incomplete spinal cord injury,” Journal of Neurophysiology, vol. 95, no. 4, pp. 2580–2589, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. N. Petersen, L. O. D. Christensen, and J. Nielsen, “The effect of transcranial magnetic stimulation on the soleus H reflex during human walking,” Journal of Physiology, vol. 513, no. 2, pp. 599–610, 1998. View at Google Scholar · View at Scopus
  83. C. Capaday, B. A. Lavoie, H. Barbeau, C. Schneider, and M. Bonnard, “Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex,” Journal of Neurophysiology, vol. 81, no. 1, pp. 129–139, 1999. View at Google Scholar · View at Scopus
  84. M. Schubert, A. Curt, L. Jensen, and V. Dietz, “Corticospinal input in human gait: modulation of magnetically evoked motor responses,” Experimental Brain Research, vol. 115, no. 2, pp. 234–246, 1997. View at Publisher · View at Google Scholar · View at Scopus
  85. M. Knikou, “The H-reflex as a probe: pathways and pitfalls,” Journal of Neuroscience Methods, vol. 171, no. 1, pp. 1–12, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Knikou, “Neural control of locomotion and training-induced plasticity after spinal and cerebral lesions,” Clinical Neurophysiology, vol. 121, no. 10, pp. 1655–1668, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Nielsen, N. Petersen, G. Deuschl, and M. Ballegaard, “Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man,” Journal of Physiology, vol. 471, pp. 223–243, 1993. View at Google Scholar · View at Scopus
  88. J. M. A. Cowan, B. L. Day, C. Marsden, and J. C. Rothwell, “The effect of percutaneous motor cortex stimulation on H reflexes in muscles of the arm and leg in intact man,” Journal of Physiology, vol. 377, pp. 333–347, 1986. View at Google Scholar · View at Scopus
  89. J. F. Iles and J. V. Pisini, “Cortical modulation of transmission in spinal reflex pathways of man,” Journal of Physiology, vol. 455, pp. 425–446, 1992. View at Google Scholar · View at Scopus
  90. J. Nielsen, N. Petersen, and B. Fedirchuk, “Evidence suggesting a transcortical pathway from cutaneous foot afferents to tibialis anterior motoneurones in man,” Journal of Physiology, vol. 501, no. 2, pp. 473–484, 1997. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Nielsen, C. Crone, T. Sinkjaer, E. Toft, and H. Hultborn, “Central control of reciprocal inhibition during fictive dorsiflexion in man,” Experimental Brain Research, vol. 104, no. 1, pp. 99–106, 1995. View at Google Scholar · View at Scopus
  92. J. B. Preston and D. G. Whitlock, “A comparison of motor cortex effects on slow and fast muscle innervations in the monkey,” Experimental Neurology, vol. 7, no. 4, pp. 327–341, 1963. View at Google Scholar · View at Scopus
  93. D. H. Stewart and J. B. Preston, “Functional coupling between the pyramidal tract and segmental motoneurons in cat and primate,” Journal of Neurophysiology, vol. 30, no. 3, pp. 453–465, 1967. View at Google Scholar · View at Scopus
  94. N. Petersen, L. O. D. Christensen, H. Morita, T. Sinkjær, and J. Nielsen, “Evidence that a transcortical pathway contributes to stretch reflexes in the tibialis anterior muscle in man,” Journal of Physiology, vol. 512, no. 1, pp. 267–276, 1998. View at Publisher · View at Google Scholar · View at Scopus
  95. J. Van Doornik, Y. Masakado, T. Sinkjaer, and J. B. Nielsen, “The suppression of the long-latency stretch reflex in the human tibialis anterior muscle by transcranial magnetic stimulation,” Experimental Brain Research, vol. 157, no. 3, pp. 403–406, 2004. View at Google Scholar · View at Scopus
  96. J. L. Taylor, W. Fogel, B. L. Day, and J. C. Rothwell, “Ipsilateral cortical stimulation inhibited the long-latency response to stretch in the long finger flexors in humans,” Journal of Physiology, vol. 488, no. 3, pp. 821–831, 1995. View at Google Scholar · View at Scopus
  97. L. O. D. Christensen, J. B. Andersen, T. Sinkjær, and J. Nielsen, “Transcranial magnetic stimulation and stretch reflexes in the tibialis anterior muscle during human walking,” Journal of Physiology, vol. 531, no. 2, pp. 545–557, 2001. View at Publisher · View at Google Scholar · View at Scopus
  98. B. L. Day, H. Riescher, A. Struppler, J. C. Rothwell, and C. D. Marsden, “Changes in the response to magnetic and electrical stimulation of the motor cortex following muscle stretch in man,” Journal of Physiology, vol. 433, pp. 41–57, 1991. View at Google Scholar · View at Scopus
  99. D. L. Wolfe, K. C. Hayes, P. J. Potter, and G. A. Delaney, “Conditioning lower limb H-reflexes by transcranial magnetic stimulation of motor cortex reveals preserved innervation in SCI patients,” Journal of Neurotrauma, vol. 13, no. 6, pp. 281–291, 1996. View at Google Scholar · View at Scopus
  100. T. Serranova, J. Valls-Sole, E. Munoz, D. Genis, R. Jech, and P. Seeman, “Abnormal corticospinal tract modulation of the soleus H reflex in patients with pure spastic paraparesis,” Neuroscience Letters, vol. 437, no. 1, pp. 15–19, 2008. View at Publisher · View at Google Scholar
  101. M. A. Perez, J. Lundbye-Jensen, and J. B. Nielsen, “Task-specific depression of the soleus H-reflex after cocontraction training of antagonistic ankle muscles,” Journal of Neurophysiology, vol. 98, no. 6, pp. 3677–3687, 2007. View at Publisher · View at Google Scholar · View at Scopus
  102. A. Holtermann, K. Roeleveld, M. Engstrøm, and T. Sand, “Enhanced H-reflex with resistance training is related to increased rate of force development,” European Journal of Applied Physiology, vol. 101, no. 3, pp. 301–312, 2007. View at Publisher · View at Google Scholar
  103. P. Aagaard, E. B. Simonsen, J. L. Andersen, P. Magnusson, and P. Dyhre, “Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses,” Journal of Applied Physiology, vol. 92, no. 6, pp. 2309–2318, 2002. View at Google Scholar · View at Scopus
  104. J. Duclay, A. Martin, A. Robbe, and M. Pousson, “Spinal reflex plasticity during maximal dynamic contractions after eccentric training,” Medicine and Science in Sports and Exercise, vol. 40, no. 4, pp. 722–734, 2008. View at Publisher · View at Google Scholar · View at Scopus
  105. R. M. Eccles and A. Lundberg, “Significance of supraspinal control of reflex actions by impulses in muscle afferents,” Experientia, vol. 14, no. 6, pp. 197–199, 1958. View at Publisher · View at Google Scholar · View at Scopus
  106. A. Lundberg and P. Voorhoeve, “Effects from the pyramidal tract on spinal reflex arcs,” Acta Physiologica Scandinavica, vol. 56, pp. 201–219, 1962. View at Google Scholar · View at Scopus
  107. A. Lundberg, “Multisensory control of spinal reflex pathways,” Progress in Brain Research C, vol. 50, pp. 11–28, 1979. View at Publisher · View at Google Scholar · View at Scopus
  108. X. Y. Chen, J. S. Carp, L. Chen, and J. R. Wolpaw, “Corticospinal tract transection prevents operantly conditioned H-reflex increase in rats,” Experimental Brain Research, vol. 144, no. 1, pp. 88–94, 2002. View at Publisher · View at Google Scholar · View at Scopus
  109. X. Y. Chen and J. R. Wolpaw, “Probable corticospinal tract control of spinal cord plasticity in the rat,” Journal of Neurophysiology, vol. 87, no. 2, pp. 645–652, 2002. View at Google Scholar · View at Scopus
  110. J. Benito Penalva, E. Opisso, J. Medina et al., “H reflex modulation by transcranial magnetic stimulation in spinal cord injury subjects after gait training with electromechanical systems,” Spinal Cord, vol. 48, no. 5, pp. 400–406, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. I. Miyai, M. Suzuki, M. Hatakenaka, and K. Kubota, “Effect of body weight support on cortical activation during gait in patients with stroke,” Experimental Brain Research, vol. 169, no. 1, pp. 85–91, 2006. View at Publisher · View at Google Scholar · View at Scopus
  112. C.-L. Yen, R. Y. Wang, K. K. Liao, C. C. Huang, and Y. R. Yang, “Gait training-induced change in corticomotor excitability in patients with chronic stroke,” Neurorehabilitation and Neural Repair, vol. 22, no. 1, pp. 22–30, 2008. View at Publisher · View at Google Scholar · View at Scopus
  113. C. Capaday and R. B. Stein, “Amplitude modulation of the soleus H-reflex in the human during walking and standing,” Journal of Neuroscience, vol. 6, no. 5, pp. 1308–1313, 1986. View at Google Scholar · View at Scopus
  114. T. Sinkjær, J. B. Andersen, and B. Larsen, “Soleus stretch reflex modulation during gait in humans,” Journal of Neurophysiology, vol. 76, no. 2, pp. 1112–1120, 1996. View at Google Scholar · View at Scopus
  115. M. Knikou, C. A. Angeli, C. K. Ferreira, and S. J. Harkema, “Soleus H-reflex modulation during body weight support treadmill walking in spinal cord intact and injured subjects,” Experimental Brain Research, vol. 193, no. 3, pp. 397–407, 2009. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Faist, M. Ertel, W. Berger, and V. Dietz, “Impaired modulation of quadriceps tendon jerk reflex during spastic gait: differences between spinal and cerebral lesions,” Brain, vol. 122, no. 3, pp. 567–579, 1999. View at Publisher · View at Google Scholar · View at Scopus
  117. J. F. Yang, J. Fung, M. Edamura, R. Blunt, R. B. Stein, and H. Barbeau, “H-reflex modulation during walking in spastic paretic subjects,” Canadian Journal of Neurological Sciences, vol. 18, no. 4, pp. 443–452, 1991. View at Google Scholar · View at Scopus
  118. M. Knikou, N. Hajela, C. K. Mummidisetty, M. Xiao, and A. C. Smith, “Soleus H-reflex phase-dependent modulation is preserved during stepping within a robotic exoskeleton,” Clinical Neurophysiology, vol. 122, no. 7, pp. 1396–1404, 2011. View at Publisher · View at Google Scholar · View at Scopus
  119. M. Knikou, “Plantar cutaneous afferents normalize the reflex modulation patterns during stepping in chronic human spinal cord injury,” Journal of Neurophysiology, vol. 103, no. 3, pp. 1304–1314, 2010. View at Publisher · View at Google Scholar · View at Scopus
  120. E. B. Simonsen and P. Dyhre, “Test-retest reliability of the soleus H-reflex excitability measured during human walking,” Human Movement Science, vol. 30, no. 2, pp. 333–340, 2011. View at Publisher · View at Google Scholar · View at Scopus
  121. C. Crone, J. Nielsen, N. Petersen, M. Ballegaard, and H. Hultborn, “Disynaptic reciprocal inhibition of ankle extensors in spastic patients,” Brain, vol. 117, no. 5, pp. 1161–1168, 1994. View at Google Scholar · View at Scopus
  122. M. Knikou and C. K. Mummidisetty, “Reduced reciprocal inhibition during assisted stepping in human spinal cord injury,” Experimental Neurology, vol. 231, no. 1, pp. 104–112, 2011. View at Publisher · View at Google Scholar · View at Scopus
  123. G. I. Boorman, R. G. Lee, W. J. Becker, and U. R. Windhorst, “Impaired “natural reciprocal inhibition” in patients with spasticity due to incomplete spinal cord injury,” Electroencephalography and Clinical Neurophysiology, vol. 101, no. 2, pp. 84–92, 1996. View at Publisher · View at Google Scholar · View at Scopus
  124. C. Crone, L. L. Johnsen, F. Biering-Sørensen, and J. B. Nielsen, “Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury,” Brain, vol. 126, no. 2, pp. 495–507, 2003. View at Publisher · View at Google Scholar · View at Scopus
  125. P. Crenna and C. Frigo, “Excitability of the soleus H-reflex arc during walking and stepping in man,” Experimental Brain Research, vol. 66, no. 1, pp. 49–60, 1987. View at Google Scholar · View at Scopus
  126. K. Akazawa, J. W. Aldridge, J. D. Steeves, and R. B. Stein, “Modulation of stretch reflexes during locomotion in the mesencephalic cat,” Journal of Physiology, vol. 329, pp. 553–567, 1982. View at Google Scholar · View at Scopus
  127. B. A. Lavoie, H. Devanne, and C. Capaday, “Differential control of reciprocal inhibition during walking versus postural and voluntary motor tasks in humans,” Journal of Neurophysiology, vol. 78, no. 1, pp. 429–438, 1997. View at Google Scholar · View at Scopus
  128. N. Petersen, H. Morita, and J. Nielsen, “Modulation of reciprocal inhibition between ankle extensors and flexors during walking in man,” Journal of Physiology, vol. 520, no. 2, pp. 605–619, 1999. View at Publisher · View at Google Scholar · View at Scopus
  129. A. M. Degtyarenko, E. S. Simon, and R. E. Burke, “Differential modulation of disynaptic cutaneous inhibition and excitation in ankle flexor motoneurons during fictive locomotion,” Journal of Neurophysiology, vol. 76, no. 5, pp. 2972–2985, 1996. View at Google Scholar · View at Scopus
  130. C. A. Pratt and L. M. Jordan, “Ia inhibitory interneurons and Renshaw cells as contributors to the spinal mechanisms of fictive locomotion,” Journal of Neurophysiology, vol. 57, no. 1, pp. 56–71, 1987. View at Google Scholar · View at Scopus
  131. S. S. Geertsen, K. Stecina, C. F. Meehan, J. B. Nielsen, and H. Hultborn, “Reciprocal Ia inhibition contributes to motoneuronal hyperpolarisation during the inactive phase of locomotion and scratching in the cat,” Journal of Physiology, vol. 589, no. 1, pp. 119–134, 2011. View at Publisher · View at Google Scholar · View at Scopus
  132. J. C. Eccles, P. Fatt, and S. Landgren, “The inhibitory pathway to motoneurones,” Progress in Neurobiology, no. 2, pp. 72–82, 1956. View at Google Scholar · View at Scopus
  133. H. Hultborn, M. Illert, and M. Santini, “Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. III. Effects from supraspinal pathways,” Acta Physiologica Scandinavica, vol. 96, no. 3, pp. 368–391, 1976. View at Google Scholar · View at Scopus
  134. H. Hultborn, E. Jankowska, and S. Lindström, “Recurrent inhibition from motor axon collaterals of transmission in the Ia inhibitory pathway to motoneurones,” Journal of Physiology, vol. 215, no. 3, pp. 591–612, 1971. View at Google Scholar · View at Scopus
  135. T. Hongo, E. Jankowska, and A. Lundberg, “The rubrospinal tract. II. Facilitation of interneuronal transmission in reflex paths to motoneurones,” Experimental Brain Research, vol. 7, no. 4, pp. 365–391, 1969. View at Publisher · View at Google Scholar · View at Scopus
  136. A. Lundgren and P. Voorhoeve, “Effects from the pyramidal tract on spinal reflex arcs,” Acta Physiologica Scandinavica, vol. 56, pp. 201–219, 1962. View at Google Scholar · View at Scopus
  137. E. Jankowska, Y. Padel, and R. Tanaka, “Disynaptic inhibition of spinal motoneurones from the motor cortex in the monkey,” Journal of Physiology, vol. 258, no. 2, pp. 467–487, 1976. View at Google Scholar · View at Scopus
  138. A. Lundberg, “Supraspinal control of transmission in reflex paths to motoneurones and primary afferents,” Progress in Brain Research, vol. 12, no. C, pp. 197–221, 1964. View at Publisher · View at Google Scholar · View at Scopus
  139. A. Lundberg, “Multisensory control of spinal reflex pathways,” Progress in Brain Research C, vol. 50, pp. 11–28, 1979. View at Publisher · View at Google Scholar · View at Scopus
  140. C. Crone, H. Hultborn, B. Jespersen, and J. Nielsen, “Reciprocal Ia inhibition between ankle flexors and extensors in man,” Journal of Physiology, vol. 389, pp. 163–185, 1987. View at Google Scholar · View at Scopus
  141. C. Crone and J. Nielsen, “Central control of disynaptic reciprocal inhibition in humans,” Acta Physiologica Scandinavica, vol. 152, no. 4, pp. 351–363, 1994. View at Google Scholar · View at Scopus
  142. E. Jankowska and R. Tanaka, “Neuronal mechanism of the disynaptic inhibition evoked in primate spinal motoneurones from the corticospinal tract,” Brain Research, vol. 75, no. 1, pp. 163–166, 1974. View at Publisher · View at Google Scholar · View at Scopus
  143. J. C. Rothwell, B. L. Day, A. Berardelli, and C. D. Marsden, “Effects of motor cortex stimulation on spinal interneurones in intact man,” Experimental Brain Research, vol. 54, no. 2, pp. 382–384, 1984. View at Google Scholar · View at Scopus
  144. M. A. Perez, E. C. Field-Fote, and M. K. Floeter, “Patterned sensory stimulation induces plasticity in reciprocal Ia inhibition in humans,” Journal of Neuroscience, vol. 23, no. 6, pp. 2014–2018, 2003. View at Google Scholar · View at Scopus
  145. S. S. Geertsen, J. Lundbye-Jensen, and J. B. Nielsen, “Increased central facilitation of antagonist reciprocal inhibition at the onset of dorsiflexion following explosive strength training,” Journal of Applied Physiology, vol. 105, no. 3, pp. 915–922, 2008. View at Publisher · View at Google Scholar · View at Scopus
  146. M. Knikou and C. Taglianetti, “On the methods employed to record and measure the human soleus H-reflex,” Somatosensory and Motor Research, vol. 23, no. 1-2, pp. 55–62, 2006. View at Publisher · View at Google Scholar · View at Scopus
  147. L. Kudina, P. Ashby, and L. Downes, “Effects of cortical stimulation on reciprocal inhibition in humans,” Experimental Brain Research, vol. 94, no. 3, pp. 533–538, 1993. View at Google Scholar · View at Scopus
  148. M. Baret, R. Katz, J. C. Lamy, A. Pénicaud, and I. Wargon, “Evidence for recurrent inhibition of reciprocal inhibition from soleus to tibialis anterior in Man,” Experimental Brain Research, vol. 152, no. 1, pp. 133–136, 2003. View at Publisher · View at Google Scholar · View at Scopus
  149. S. Meunier, “Modulation by corticospinal volleys of presynaptic inhibition to Ia afferents in man,” Journal of Physiology Paris, vol. 93, no. 4, pp. 387–394, 1999. View at Publisher · View at Google Scholar · View at Scopus
  150. F. C. Hummel and L. G. Cohen, “Drivers of brain plasticity,” Current Opinion in Neurology, vol. 18, no. 6, pp. 667–674, 2005. View at Google Scholar · View at Scopus
  151. R. J. Nudo, “Plasticity,” NeuroRx, vol. 3, no. 4, pp. 420–427, 2006. View at Publisher · View at Google Scholar · View at Scopus