Descending motor pathways and cortical physiology after spinal cord injury assessed by transcranial magnetic stimulation: a systematic review

Brain Research

Volumn 1619, Issue , 2015, Pages 139-154

  Nardone, Raffaele ^a,b   Höller, Yvonne ^a   Brigo, Francesco ^b,c   Orioli, Andrea ^b   Tezzon, Frediano ^b   Schwenker, Kerstin ^a   Christova, Monica ^d   Golaszewski, Stefan ^a   Trinka, Eugen ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b FRANZ TAPPEINER HOSPITAL   (Italy)

^c UNIVERSITY OF VERONA   (Italy)

^d MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

Central motor conduction; Intracortical inhibition; Motor evoked potentials; Repetitive transcranial magnetic stimulation; Spinal cord injury; Therapeutic applications; Transcranial magnetic stimulation

Indexed keywords

ARTICLE; BRAIN CORTEX; BRAIN MAPPING; EVOKED MUSCLE RESPONSE; HUMAN; MOTOR CORTEX; MOTOR PERFORMANCE; MOTOR SYSTEM; NEUROIMAGING; NEUROMUSCULAR FUNCTION; PAIN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REPEAT PROCEDURE; REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION; SENSORIMOTOR NEUROPATHY; SPASTICITY; SPINAL CORD INJURY; SYSTEMATIC REVIEW; TRANSCRANIAL MAGNETIC STIMULATION; ANIMAL; COMPLICATION; CONVALESCENCE; INNERVATION; MOTOR ACTIVITY; MOTOR EVOKED POTENTIAL; MUSCLE SPASTICITY; NEURALGIA; PSYCHOMOTOR DISORDERS; PYRAMIDAL TRACT; SKELETAL MUSCLE; SPINAL CORD INJURIES;

ANIMALS; EVOKED POTENTIALS, MOTOR; HUMANS; MOTOR ACTIVITY; MOTOR CORTEX; MUSCLE SPASTICITY; MUSCLE, SKELETAL; NEURALGIA; PSYCHOMOTOR DISORDERS; PYRAMIDAL TRACTS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84908491119     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.09.036     Document Type: Review

References (96)

1. D. Barthélemy, H. Knudsen, M. Willerslev-Olsen, H. Lundell, J.B. Nielsen, and F. Biering-Sørensen Functional implications of corticospinal tract impairment on gait after spinal cord injury Spinal Cord 51 2013 852 856
2. D. Barthélemy, M. Willerslev-Olsen, H. Lundell, B.A. Conway, H. Knudsen, F. Biering-Sørensen, and J.B. Nielsen Impaired transmission in the corticospinal tract and gait disability in spinal cord injured persons J. Neurophysiol. 104 2010 1167 1176
3. M.L. Beaud, E. Schmidlin, T. Wannier, P. Freund, J. Bloch, A. Mir, M.E. Schwab, and E.M. Rouiller Anti-Nogo-A antibody treatment does not prevent cell body shrinkage in the motor cortex in adult monkeys subjected to unilateral cervical cord lesion BMC Neurosci. 9 2008 5
4. M. Belci, M. Catley, M. Husain, H.L. Frankel, and N.J. Davey Magnetic brain stimulation can improve clinical outcome in incomplete spinal cord injured patients Spinal Cord 42 2004 417 419
5. A. Berardelli, M. Inghilleri, J.C. Rothwell, S. Romeo, A. Currà, F. Gilio, N. Modugno, and M. Manfredi Facilitation of muscle evoked responses after repetitive cortical stimulation in man Exp. Brain Res. 122 1998 79 84
6. K.L. Bunday, M. Oudega, and M.A. Perez Aberrant crossed corticospinal facilitation in muscles distant from a spinal cord injury PLoS One 8 2013 e76747
7. 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 J. Neurotrauma 16 1999 49 67
8. D. Centonze, G. Koch, V. Versace, F. Mori, S. Rossi, L. Brusa, K. Grossi, F. Torelli, C. Prosperetti, A. Cervellino, G.A. Marfia, P. Stanzione, M.G. Marciani, L. Boffa, and G. Bernardi Repetitive transcranial magnetic stimulation of the motor cortex ameliorates spasticity in multiple sclerosis Neurology 68 2007 1045 1050
9. R. Chen, D. Cros, A. Curra, V. Di Lazzaro, J.P. Lefaucheur, M.R. Magistris, K. Mills, K.M. Rösler, W.J. Triggs, Y. Ugawa, and U. Ziemann The clinical dagnostic utility of transcranial magnetic stimulation: report of an IFCN committee Clin. Neurophysiol. 119 2008 504 532
10. M. Craggs, V. Balasubramaniam, A. Kuppuswamy, R. Maksimovic, and P. Ellaway The interaction of brain pathways and sacral reflexes following spinal cord lesions in man Neurourol. Urodyn. 26 2007 614 615
11. G. Cruccu, T.Z. Aziz, L. Garcia-Larrea, P. Hansson, T.S. Jensen, J.P. Lefaucheur, B.A. Simpson, and R.S. Taylor EFNS guidelines on neurostimulation therapy for neuropathic pain Eur. J. Neurol. 14 2007 952 970
12. A. Curt, and V. Dietz Electrophysiological recordings in patients with spinal cord injury:significance for predicting outcome Spinal Cord 37 1999 157 165
13. A. Curt, M.E. Keck, and V. Dietz Functional outcome following spinal cord injury: significance of motor-evoked potentials and ASIA scores Arch. Phys. Med. Rehabil. 79 1998 81 86
14. N.J. Davey, H.C. Smith, E. Wells, D.W. Maskill, G. Savic, P.H. Ellaway, and H.L. Frankel Responses of thenar muscles to transcranial magnetic stimulation of the motor cortex in patients with incomplete spinal cord injury J. Neurol. Neurosurg. Psychiatry 65 1998 80 87
15. R. Defrin, L. Grunhaus, D. Zamir, and G. Zeilig The effects of a series of repetitive transcranial magnetic stimulation of the motor cortex on central pain after spinal cord injury Arch. Phys. Med. Rehabil. 88 2007 1574 1580
16. I. Delvendahl, N.H. Jung, N.G. Kuhnke, U. Ziemann, and V. Mall Plasticity of motor threshold and motor-evoked potential amplitude - a model of intrinsic synaptic plasticity in human motor cortex? Brain Stimul. 5 2012 586 593
17. H. Devanne, B.A. Lavoie, and C. Capaday Input-output properties and gain changes in the human corticospinal pathway Exp. Brain Res. 114 1997 329 338
18. V. Di Lazzaro, A. Oliviero, P. Profice, L. Ferrara, E. Saturno, F. Pilato, and P. Tonali The diagnostic value of motor evoked potentials Clin. Neurophysiol. 110 1999 1297 1307
19. Di Lazzaro, V., Oliviero, A., Profice, P., Pennisi, M.A., Pilato, F., Zito, G., Dileone, M., Nicoletti R., Pasqualetti P., Tonali P.A., 2003. Ketamine increases human motor cortex excitability to transcranial magnetic stimulation. Journal of Physiology. vol. 547, pp. 485-496.
20. V. Di Lazzaro, A. Oliviero, F. Pilato, E. Saturno, M. Dileone, P. Mazzone, A. Insola, P.A. Tonali, and J.C. Rothwell The physiological basis of transcranial motor cortex stimulation in conscious humans Clin. Neurophysiol. 115 2004 255 266
21. V. Di Lazzaro, F. Pilato, A. Oliviero, M. Dileone, E. Saturno, P. Mazzone, A. Insola, P. Profice, F. Ranieri, F. Capone, P.A. Tonali, and J.C. Rothwell Origin of facilitation of motor evoked potentials after paired magnetic stimulation: direct recording of epidural activity in conscious humans J. Neurophysiol. 96 2006 1765 1771
22. D.J. Edwards, M. Cortes, G.W. Thickbroom, A. Rykman, A. Pascual-Leone, and B.T. Volpe Preserved corticospinal conduction without voluntary movement after spjnal cord injury Spinal Cord 51 2013 765 767
23. P.H. Ellaway, N. Vásquez, and M. Craggs Induction of central nervous system plasticity by repetitive transcranial magnetic stimulation to promoto sensotimotor recovery in incomplete spinal cord injury Front. Integr. Neurosci. 8 2014 42
24. P. Freund, N. Weiskopf, N.S. Ward, C. Hutton, A. Gall, O. Ciccarelli, M. Craggs, K. Friston, and A.J. Thompson Disability, atrophy and cortical reorganization following spinal cord injury Brain 134 2011 1610 1622
25. P. Freund, J. Rothwell, M. Craggs, A.J. Thompson, and S. Bestmann Corticomotor representation to a human forearm muscle changes following cervical spinal cord injury Eur. J. Neurosci. 34 2011 1839 1846
26. S. Groppa, A. Oliviero, A. Eisen, A. Quartarone, L.G. Cohen, V. Mall, A. Kaelin-Lang, T. Mima, S. Rossi, G.W. Thickbroom, P.M. Rossini, U. Ziemann, J. Valls-Solé, and H.R. Siebner A practical guide to diagnostic transcranial magnetic stimulation: a report of an IFCN committee Clin. Neurophysiol. 123 2012 858 882
27. B.C. Hains, J.A. Black, and S.C. Waxman Primary cortical motor neurons undergo apoptosis after axotomizing spinal cord injury J. Comp. Neurol. 462 2003 328 341
28. M. Hallett Transcranial magnetic stimulation and the human brain Nature 406 2000 147 150
29. C.W. Hess, K.R. Mills, and N.M. Murray Responses in small hand muscles from magnetic simulation of the human brain J. Physiol. 388 1987 397 419
30. M. Hoogendam, G.M. Ramakers, and V. Di Lazzaro Physiology of repetitive transcranial magnetic stimulation of the human brain Brain Stimul. 3 2010 95 118
31. J. Hou, R. Nelson, N. Nissim, R. Parmer, F.J. Thompson, and P.K. Bose Effect of combined treadmill training and magnetic stimulation on spasticity and gait impairments following cervical spinal cord injury J. Neurotrauma 15 2014 1088 1106
32. M. Inghilleri, A. Berardelli, G. Cruccu, and M. Manfredi Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction J. Physiol. 466 1993 521 534
33. P. Julkunen, L. Saisanen, N. Danner, E. Niskanen, T. Hukkanen, E. Mervaala, and M. Kononen Comparison of navigated and non-navigated transcranial magnetic stimulation for motor cortex mapping, motor threshold and motor evoked potentials Neuroimage 44 2009 790 795
34. B.S. Kang, H.I. Shin, and M.S. Bang Effect of repetitive transcranial magnetic stimulation over the hand motor cortical area on central pain after spinal cord injury Arch. Phys. Med. Rehabil. 90 2009 1766 1771
35. V.K. Kimiskidis, S. Papagiannopoulos, K. Sotirakoglou, D.A. Kazis, A. Kazis, and K.R. Mills Silent period to transcanial magnetic stimulation: construction and properties of stimulus-response curves in healthy volunteers Exp. Brain Res. 163 2005 21 31
36. M. Kobayashi, and A. Pascual-Leone Transcranial magnetic stimulation in neurology Lancet Neurol. 2 2003 145 156
37. Y.Z. Huang, M.J. Edwards, E. Rounis, K.P. Bhatia, and J.C. Rothwell Theta burst stimulation of the human motor cortex Neuron 45 2005 201 206
38. M. Knikou, N. Hajela, and C.K. Mummidisetty Corticospinal excitability during walking in humans with absent and partial body weight support Clin. Neurophysiol. 124 2013 2431 2438
39. T. Kujirai, M.D. Caramia, J.C. Rothwell, B.L. Day, P.D. Thompson, A. Ferbert, S. Wroe, P. Asselman, and C.D. Marsden Corticocortical inhibition in human motor cortex J. Physiol. 471 1993 501 519
40. H. Kumru, N. Murillo, J.V. Samso, J. Valls-Sole, D. Edwards, R. Pelayo, A. Valero-Cabre, J.M. Tormos, and A. Pascual-Leone Reduction of spasticity with repetitive transcranial magnetic stimulation in patients with spinal cord injury Neurorehabil. Neural Repair 24 2010 435 441
41. H. Kumru, J. Benito, N. Murillo, J. Valls-Sole, M. Valles, R. Lopez-Blazquez, U. Costa, J.M. Tormos, A. Pascual-Leone, and J. Vidal Effects of high-frequency repetitive transcranial stimulation on motor and gait improvement in incomplete spinal cord injury patients Neurorehabil. Neural Repair 27 2013 421 429
42. A. Kuppuswamy, A.V. Balasubramaniam, R. Maksimovic, C.J. Mathias, A. Gall, M.D. Craggs, and P.H. Ellaway Action of 5 Hz repetitive transcranial magnetic stimulation on sensory, motor and autonomic function in human spinal cord injury Clin. Neurophysiol. 122 2011 2452 2456
43. U. Laubis-Herrmann, J. Dichgans, H. Bilow, and H. Topka Motor reorganization after spinal cord injury: evidence of adaptive changes in remote muscles Restor. Neurol. Neurosci. 17 2000 175 181
44. L. Lee, H.R. Siebner, J.B. Rowe, V. Rizzo, J.C. Rothwell, R.S. Frackowiak, and K.J. Friston Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation J. Neurosci. 23 2003 5308 5318
45. J.P. Lefaucheur, X. Drouot, I. Menard-Lefaucheur, F. Zerah, B. Bendib, P. Cesaro, Y. Keravel, and J.P. Nguyen Neurogenic pain relief by repetitive transcranial magnetic cortical stimulation depends on the origin and the site of pain J. Neurol. Neurosurg. Psychiatry 75 2004 612 657
46. J.P. Lefaucheur, I. Ménard-Lefaucheur, C. Goujon, Y. Keravel, and J.P. Nguyen Predictive value of rTMS in the identification of responders to epidural motor cortex stimulation therapy for pain J. Pain 12 2011 1102 1111
47. J.P. Lefaucheur, N. André-Obadia, E. Poulet, H. Devanne, E. Haffen, A. Londero, B. Cretin, A.M. Leroi, A. Radtchenko, G. Saba, H. Thai-Van, C.F. Litré, L. Vercueil, D. Bouhassira, S.S. Ayache, W.H. Farhat, H.G. Zouari, V. Mylius, M. Nicolier, and L. Garcia-Larrea French guidelines on the use of repetitive transcranial magnetic stimulation (rTMS) Neurophysiol. Clin. 41 2011 221 295
48. J.P. Lefaucheur, S.S. Ayache, M. Sorel, W.H. Farhat, H.G. Zouari, D. Ciampi de Andrade, R. Ahdab, I. Ménard-Lefaucheur, P. Brugières, and C. Goujon Analgesic effects of repetitive transcranial magnetic stimulation of the motor cortex in neuropathic pain: influence of theta burst stimulation priming Eur. J. Pain 16 2012 1403 1413
49. R.J. Leo, and R. Latif Repetitive transcranial magnetic stimulation (rTMS) in experimentally induced and chronic neuropathic pain: a review J. Pain 8 2007 453 459
50. A. Leung, M. Donohue, R. Xu, R. Lee, J.P. Lefaucheur, E.M. Khedr, Y. Saitoh, N. André-Obadia, J. Rollnik, M. Wallace, and R. Chen rTMS for suppressing neuropathic pain: a meta-analysis J. Pain 10 2009 1205 1216
51. W.J. Levy, V.E. Amassian, M. Traad, and J. Cadwell Focal magnetic coil stimulation reveals motor cortical system reorganized in humans after traumatic quadriplegia Brain Res. 510 1990 130 134
52. J. Liepert, P. Schwenkreis, M. Tegenthhoff, and J.P. Malin The glutamate antagonist riluzole suppress intracortical facilitation J. Neural Transm. 104 1997 1207 1214
53. M.A. Lissens, and G.G. Vanderstraeten Motor evoked potentials of the respiratory muscles in tetraplegic patients Spinal Cord 34 1996 673 678
54. M. Lotze, U. Laubis-Herrmann, and H. Topka Combination of TMS and fMRI reveals a specific pattern of reorganization in M1 in patients after complete spinal cord injury Restor. Neurol. Neurosci. 24 2006 97 107
55. W.B. McKay, D.S. Stokic, A.M. Sherwood, G. Vrbova, and M.R. Dimitrijevic Effect of fatiguing maximal voluntary contraction on excitatory and inhibitory responses elicited by transcranial magnetic motor cortex stimulation Muscle Nerve 19 1996 1017 1024
56. B. Meyer, and J. Zentner Do motor evoked potentials allow quantitative assessment of motor function in patients with spinal cord lesions? Eur. Arch. Psychiatry Clin. Neurosci. 241 1992 201 204
57. K.R. Mills, and C.C.B. Thomson Human muscle fatigue investigated by transcranial magnetic stimulation Neuroreport 6 1995 1966 1968
58. I. Moreno-Duarte, L.R. Morse, M. Alam, M. Bikson, R. Zafonte, and F. Fregni Targeted therapies using electrical and magnetic neurral stimulation for the tretmant of chronic pain in spinal cord injury Neuroimage 85 2014 1003 1013
59. K.A. Moxon, A. Oliviero, J. Aguilar, and G. Foffani Cortical reorganization after spinal cord injury: Always for good? Neuroscience 2014 Jul 2. pii: S0306-4522(14)00541-7. 10.1016/j.neuroscience.2014.06.056
60. R. Nardone, S. Golaszewski, J. Bergmann, A. Venturi, I. Prünster, A. Bratti, G. Ladurner, and F. Tezzon Motor cortex excitability changes following a lesion in the posterior columns of the cervical spinal cord Neurosci. Lett. 434 2008 119 123
61. R. Nardone, Y. Höller, F. Brigo, M. Seidl, M. Christova, J. Bergmann, S. Golaszewski, and E. Trinka Functional brain reorganization after spinal cord injury: systematic review of animal and human studies Brain Res. 1504 2013 58 73
62. C.S. Oza, and S.F. Giszter Plasticity and alterations of trunk motor cortex following spinal cord injury and non-stepping robot and treadmill training Exp. Neurol. 256 2014 57 69
63. A. Pascual-Leone, J. Valls-Solé, J.P. Brasil-Neto, A. Cammarota, J. Grafman, and M. Hallett Akinesia in Parkinsons disease. II. Effects of subthreshold repetitive transcranial motor cortex stimulation Neurology 44 1994 892 898
64. A. Pascual-Leone, J.M. Tormos, J. Keenan, F. Tarazona, C. Cañete, and M.D. Catalá Study and modulation of human cortical excitability with transcranial magnetic stimulation J. Clin. Neurophysiol. 15 1998 333 343
65. W. Paulus, J. Classen, L.G. Cohen, C.H. Large, V. Di Lazzaro, M. Nitsche, A. Pascual-Leone, F. Rosenow, J.C. Rothwell, and U. Ziemann State of the art: pharmacologic effects on cortical excitability measures tested by transcranial magnetic stimulation Brain Stimul. 1 2008 151 163
66. M.A. Perez, B.K. Lungholt, and J.B. Nielsen Short-term adaptations in spinal cord circuits evoked by repetitive transcranial magnetic stimulation: possible underlying mechanisms Exp. Brain Res. 162 2005 202 212
67. J.A. Petersen, M. Spiess, A. Curt, V. Dietz, M. Schubert, and EM-SCI Study Group Spinal cord injury: one-year evolution of motor-evoked potentials and recovery of leg motor function in 255 patients Neurorehabil. Neural Repair 26 2012 939 948
68. A.L. Poirrier, Y. Nyssen, F. Scholtes, S. Multon, C. Rinkin, G. Weber, D. Bouhy, G. Brook, R. Franzen, and J. Schoenen Repetitive transcranial magnetic stimulation improves open field locomotor recovery after low but not high thoracic spinal cord compression-injury in adult rats J. Neurosci. Res. 75 2004 253 261
69. A. Quartarone, S. Bagnato, V. Rizzo, F. Morgante, A. Sant Angelo, F. Battaglia, C. Messina, H.R. Siebner, and P. Girlanda Distinct changes in cortical and spinal excitability following high-frequency repetitive TMS to the human motor cortex Exp. Brain Res. 161 2005 114 124
70. F.D. Roy, E.T. Zewdie, and M.A. Gorassini Short-interval intracortical inhibition with incomplete spinal cord injury Clin. Neurophysiol. 122 2011 1387 1395
71. S. Rossi, M. Hallett, P.M. Rossini, A. Pascual-Leone, and The Safety of TMS Consensus Group Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research Clin. Neurophysiol. 120 2009 2008 2039
72. P.M. Rossini, T. Barker, A. Berardelli, M.D. Caramia, G. Caruso, R.Q. Cracco, M.R. Dimitrijevic, M. Hallett, Y. Katayama, C.H. Lucking, A.L. Maertens de Noordhout, C.D. Marsden, N.M.F. Murray, J.C. Rothwell, M. Swash, and C. Tomberg Non invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application: report of IFCN committee Electroencephalogr. Clin. Neurophysiol. 91 1994 79 92
73. J.C. Rothwell, M. Hallett, A. Berardelli, A. Eisen, P. Rossini, and W. Paulus Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology Electroencephalogr. Clin. Neurophysiol. Suppl. 52 1999 97 103
74. E. Saturno, C. Bonato, C. Miniussi, V. Di Lazzaro, and L. Callea Motor cortex changes in spinal cord injury: a TMS study Neurol. Res. 30 2008 1084 1085
75. T. Shimizu, T. Hino, T. Komori, and S. Hirai Loss of the muscle silent period evoked by transcranial magnetic stimulation of the motor cortex in patients with cervical cord lesions Neurosci. Lett. 286 2000 199 202
76. D.M. Schmid, A. Curt, D. Hauri, and B. Schurch Motor evoked potential (MEP) and evoked pressure curves (EPC) from the urethral compressive musculature (UCM) by functional magnetic stimulation in healthy volunteers and patients with neurogenic incontinence Neurourol. Urodyn. 24 2005 117 127
77. J. Silvanto, and A. Pascual-Leone State-dependency of trasncranial magnetic stimulation Brain Topogr. 21 2008 1 10
78. K. Stefan, E. Kunesch, R. Benecke, L.G. Cohen, and J. Classen Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation J. Physiol. 543 2002 699 708
79. H.C. Smith, N.J. Davey, G. Savic, D.W. Maskill, P.H. Ellaway, M.A. Jamous, and H.L. Frankel Modulation of single motor unit discharges using magnetic stimulation of the motor cortex in incomplete spinal cord injury J. Neurol. Neurosurg. Psychiatry 68 2000 516 520
80. H.C. Smith, G. Savic, H.L. Frankel, P.H. Ellaway, D.W. Maskill, M.A. Jamous, and N.J. Davey Corticospinal function studied over time following incomplete spinal cord injury Spinal Cord 38 2000 292 300
81. L.J. Streletz, J.K. Belevich, S.M. Jones, A. Bhushan, S.H. Shah, and G.J. Herbison Transcranial magnetic stimulation: cortical motor maps in acute spinal cord injury Brain Topogr. 7 1995 245 250
82. J.L. Taylor, J.E. Butler, and S.G. Gandevia Altered responses of human elbow flexors to peripheral-nerve and cortical stimulation during a sustained maximal voluntary contractions Exp. Brain Res. 127 1999 108 115
83. H. Topka, L.G. Cohen, R.A. Cole, and M. Hallett Reorganization of corticospinal pathways following spinal cord injury Neurology 41 1991 1276 1283
84. A. Valero-Cabre, M. Oliveri, M. Gangitano, and A. Pascual-Leone Modulation of spinal cord excitability by subthreshold repetitive transcranial magnetic stimulation of the primary motor cortex in humans Neuroreport 12 2001 3845 3848
85. A.C. Valle, K. Dionisio, N.B. Pitskel, A. Pascual-Leone, F. Orsati, M.J. Ferreira, P.S. Boggio, M.C. Lima, S.P. Rigonatti, and F. Fregni Low and high frequency repetitive transcranial magnetic stimulation for the treatment of spasticity Dev. Med. Child Neurol. 49 2007 534 538
86. H.J. van Hedel, C. Murer, V. Dietz, and A. Curt The amplitude of lower leg motor evoked potentials is a reliable measure when controlled for torque and motor task J. Neurol. 254 2007 1089 1098
87. N. Vasquez, V. Balasubramaniam, A. Kuppuswamy, S. Knight, J. Susser, A. Gall, P.H. Ellaway, and M.D. Craggs The interaction of cortico-spinal pathways and the pudendoanal reflex in patients with incomplete spinal cord injury: a pilot study Neurourol. Urodyn. 2014 10.1002/nau.22554
88. M.S. Volz, T.S. Volz, A.R. Brunoni, J.P. de Oliveira, and F. Fregni Analgesic effects on noninvasive brain stimulation in rodent animal models: a systematic review of translational findings Neuromodulation 15 2012 283 295
89. K.J. Werhahn, E. Kunesch, S. Noachtar, R. Benecke, and J. Classen Differential effects on motor cortical inhibition induced by blockade of GABA uptake in humans J. Physiol. 517 1999 591 597
90. B. Wirth, H.J. van Hedel, and A. Curt Ankle dexterity remains intact in patients with incomplete spinal cord injury in contrast to stroke patients Exp. Brain Res. 191 2008 353 361
91. B. Wirth, H.J. Van Hedel, and A. Curt Changes in corticospinal function and ankle motor control during recovery from incomplete spinal cord injury J. Neurotrauma 25 2008 467 478
92. B. YIlmaz, S. Kesikburun, E. Yas Ar, and A.K. Tan The effect of repetitive transcranial magnetic stimulation on refractory neuropathic pain in spinal cord injury J. Spinal Cord Med. 37 2014 397 400
93. J. Zentner, and G. Rieder Diagnostic significance of motor evoked potentials in space-occupying lesions of the brain stem and spinal cord Eur. Arch. Psychiatry Neurol. Sci. 239 1990 285 289
94. U. Ziemann, S. Lonnecker, B.H. Steinhoff, and W. Paulus Effects of antiepileptics drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study Ann. Neurol. 40 1996 367 378
95. U. Ziemann, S. Lonnecker, B.J. Steinhoff, and W. Paulus The effect of lorazepam on the motor cortex excitability in man Exp. Brain Res. 109 1996 127 135
96. U. Zifko, H. Remtulla, K. Power, L. Harker, and C.F. Bolton Transcortical and cervical magnetic stimulation with recording of the diaphragm Muscle Nerve 19 1986 614 620