Impaired crossed facilitation of the corticospinal pathway after cervical spinal cord injury

Journal of Neurophysiology

Volumn 107, Issue 10, 2012, Pages 2901-2911

  Bunday, Karen L ^a   Perez, Monica A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Corticospinal drive; Force; Primary motor cortex; Sensorimotor cortex; Spinal motoneurons

Indexed keywords

ADULT; ARTICLE; CERVICAL SPINAL CORD INJURY; CLINICAL ARTICLE; CLINICAL EXAMINATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROMYOGRAPHY; EVOKED MUSCLE RESPONSE; FACILITATION; FEMALE; GABAERGIC SYSTEM; HAND MUSCLE; HUMAN; MALE; MOTONEURON; MOTOR COORDINATION; MOTOR PERFORMANCE; MUSCLE CONTRACTION; PRIORITY JOURNAL; PSYCHOMOTOR PERFORMANCE; PYRAMIDAL TRACT; TRANSCRANIAL MAGNETIC STIMULATION; VOLUNTARY MOVEMENT;

ADULT; CERVICAL VERTEBRAE; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; HAND; HUMANS; MALE; MIDDLE AGED; MOTOR CORTEX; MOTOR NEURONS; MUSCLE, SKELETAL; PYRAMIDAL TRACTS; SPINAL CORD INJURIES; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84861149086     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00850.2011     Document Type: Article

References (67)

1. Aimonetti JM, Nielsen JB. Changes in intracortical excitability induced by stimulation of wrist afferents in man. J Physiol 534: 891-902, 2001.
2. Barthélemy D, Willerslev-Olsen M, Lundell H, Conway BA, Knudsen H, Biering-Sørensen F, Nielsen JB. Impaired transmission in the corticospinal tract and gait disability in spinal cord injured persons. J Neurophysiol 104: 1167-1176, 2010.
3. Bennett DJ, Sanelli L, Cooke CL, Harvey PJ, Gorassini MA. Spastic long-lasting reflexes in the awake rat after sacral spinal cord injury. J Neurophysiol 91: 2247-2258, 2004.
4. Brus-Ramer M, Carmel JB, Martin JH. Motor cortex bilateral motor representation depends on subcortical and interhemispheric interactions. J Neurosci 29: 6196-6206, 2009.
5. Butler JE, Thomas CK. Effects of sustained stimulation on the excitability of motoneurons innervating paralyzed and control muscles. J Appl Physiol 94: 567-575, 2003.
6. Calancie B, Molano MR, Broton JG. Neural plasticity as revealed by the natural progression of movement expression-both voluntary and involun-tary-in humans after spinal cord injury. Prog Brain Res 128: 71-88, 2000.
7. Carson RG, Kennedy NC, Linden MA, Britton L. Muscle-specific variations in use-dependent crossed-facilitation of corticospinal pathways mediated by transcranial direct current (DC) stimulation. Neurosci Lett 441: 153-157, 2008.
8. Carson RG, Riek S, Mackey DC, Meichenbaum DP, Willms K, Forner M, Byblow WD. Excitability changes in human forearm corticospinal projections and spinal reflex pathways during rhythmic voluntary movement of the opposite limb. J Physiol 560: 929-940, 2004.
9. Chardon MK, Suresh NL, Rymer WZ. An evaluation of passive properties of spastic muscles in hemiparetic stroke survivors. Conf Proc IEEE Eng Med Biol Soc 2010: 2993-2996, 2010.
10. Curt A, Keck ME, Dietz V. Clinical value of F-wave recordings in traumatic cervical spinal cord injury. Electroencephalogr Clin Neurophysiol 105: 189-193, 1997.
11. Davey NJ, Smith HC, Wells E, Maskill DW, Savic G, Ellaway PH, Frankel HL. Responses of thenar muscles to transcranial magnetic stimulation of the motor cortex in patients with incomplete spinal cord injury. J Neurol Neurosurg Psychiatry 65: 80-87, 1998.
12. Davey NJ, Smith HC, Savic G, Maskill DW, Ellaway PH, Frankel HL. Comparison of input-output patterns in the corticospinal system of normal subjects and incomplete spinal cord injured patients. Exp Brain Res 127: 382-390, 1999.
13. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Mazzone P, Insola A, Tonali PA, Rothwell JC. The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115: 255-266, 2004.
14. Ellaway PH, Catley M, Davey NJ, Kuppuswamy A, Strutton P, Frankel HL, Jamous A, Savic G. Review of physiological motor outcome measures in spinal cord injury using transcranial magnetic stimulation and spinal reflexes. J Rehabil Res Dev 44: 69-76, 2007.
15. Espiritu MG, Lin CS, Burke D. Motoneuron excitability and the F wave. Muscle Nerve 27: 720-727, 2003.
16. Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD. Interhemispheric inhibition of the human motor cortex. J Physiol 453: 525-546, 1992.
17. Fierro B, Raimondo D, Modica A. F-response assessment in healthy control subjects. Electromyogr Clin Neurophysiol 30: 501-508, 1990.
18. Fouad K, Pedersen V, Schwab ME, Brösamle C. Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr Biol 11: 1766-1770, 2001.
19. Ghosh A, Sydekum E, Haiss F, Peduzzi S, Zörner B, Schneider R, Baltes C, Rudin M, Weber B, Schwab ME. Functional and anatomical reorganization of the sensory-motor cortex after incomplete spinal cord injury in adult rats. J Neurosci 29: 12210-12219, 2009.
20. Gould HJ, Cusick CG, Pons TP, Kaas JH. The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys. J Comp Neurol 247: 297-325, 1986.
21. Hansen NL, Conway BA, Halliday DM, Hansen S, Pyndt HS, Biering-Sørensen F, Nielsen JB. Reduction of common synaptic drive to ankle dorsiflexor motoneurons during walking in patients with spinal cord lesion. J Neurophysiol 94: 934-942, 2005.
22. Hinder MR, Schmidt MW, Garry MI, Summers JJ. Unilateral contractions modulate interhemispheric inhibition most strongly and most adaptively in the homologous muscle of the contralateral limb. Exp Brain Res 205: 423-433, 2010.
23. Hortobagyi T, Taylor JL, Petersen NT, Russell G, Gandevia SC. Changes in segmental and motor cortical output with contralateral muscle contractions and altered sensory inputs in humans. J Neurophysiol 90: 2451-2459, 2003.
24. Hultborn H, Nielsen JB. H-reflexes and F-responses are not equally sensitive to changes in motoneuronal excitability. Muscle Nerve 18: 1471-1474, 1995.
25. Jankowska E, Cabaj A, Pettersson LG. How to enhance ipsilateral actions of pyramidal tract neurons. J Neurosci 25: 7401-745, 2005.
26. Jankowska E, Stecina K, Cabaj A, Pettersson LG, Edgley SA. Neuronal relays in double crossed pathways between feline motor cortex and ipsilat-eral hindlimb motoneurones. J Physiol 575: 527-541, 2006.
27. Kennedy NC, Carson RG. The effect of simultaneous contractions of ipsi-lateral muscles on changes in corticospinal excitability induced by paired associative stimulation (PAS). Neurosci Lett 445: 7-11, 2008.
28. Kim Y, Aoki T, Ito H. Evaluation of parameters of serially monitored F-wave in acute cervical spinal cord injury. J Nippon Med Sch 74: 106-113, 2007.
29. Kowalczewski J, Chong SL, Galea M, Prochazka A. In-home tele-rehabilitation improves tetraplegic hand function. Neurorehabil Neural Repair 25: 412-422, 2011.
30. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD. Corticocortical inhibition in human motor cortex. J Physiol 471: 501-519, 1993.
31. Lee M, Hinder MR, Gandevia SC, Carroll TJ. The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. J Physiol 588: 201-212, 2010.
32. Lemon RN. Descending pathways in motor control. Annu Rev Neurosci 31: 195-218, 2008.
33. Lin JZ, Floeter MK. Do F-wave measurements detect changes in motor neuron excitability? Muscle Nerve 30: 289-294, 2004.
34. Marino RJ, Barros T, Biering-Sorensen F, Burns SP, Donovan WH, Graves DE, Haak M, Hudson LM, Priebe MM. International standards for neurological classification of spinal cord injury. J Spinal Cord Med 26: 50-56, 2003.
35. Meyer BU, Roricht S, Grafin von Einsiedel H, Kruggel F, Weindl A. Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain 118: 429-440, 1995.
36. Mottram CJ, Wallace CL, Chikando CN, Rymer WZ. Origins of spontaneous firing of motor units in the spastic-paretic biceps brachii muscle of stroke survivors. J Neurophysiol 104: 3168-3179, 2010.
37. Muellbacher W, Facchini S, Boroojerdi B, Hallett M. Changes in motor cortex excitability during ipsilateral hand muscle activation in humans. Clin Neurophysiol 111: 344-349, 2000.
38. Nishimura Y, Isa T. Cortical and subcortical compensatory mechanisms after spinal cord injury in monkeys. Exp Neurol (August 22, 2011). doi:10.1016/ j.expneurol.2011.08.013.
39. Norton JA, Bennett DJ, Knash ME, Murray KC, Gorassini MA. Changes in sensory-evoked synaptic activation of motoneurons after spinal cord injury in man. Brain 131: 1478-1491, 2008.
40. Norton JA, Gorassini MA. Changes in cortically related intermuscular coherence accompanying improvements in locomotor skills in incomplete spinal cord injury. J Neurophysiol 95: 2580-2589, 2006.
41. Panayiotopoulos CP, Chroni E. F-waves in clinical neurophysiology: a review, methodological issues and overall value in peripheral neuropathies. Electroencephalogr Clin Neurophysiol 101: 365-374, 1996.
42. Perez MA, Cohen LG. Mechanisms underlying functional changes in the primary motor cortex ipsilateral to an active hand. J Neurosci 28: 5631-5640, 2008.
43. Perez MA, Cohen LG. Scaling of motor cortical excitability during uni-manual force generation. Cortex 45: 1065-1071, 2009.
44. Perez MA, Wise SP, Willingham DT, Cohen LG. Neurophysiological mechanisms involved in transfer of procedural knowledge. J Neurosci 27: 1045-1053, 2007.
45. Pierrot-Deseilligny E, Burke D. The Circuitry of the Human Spinal Cord. Cambridge, UK: Cambridge Univ. Press, 2005, chapter 10, p. 452-510.
46. Raineteau O, Schwab ME. Plasticity of motor systems after incomplete spinal cord injury. Nat Rev Neurosci 2: 263-273, 2001.
47. Renner CIE, Woldag H, Atanasova R, Hummelsheim H. Change of facilitation during voluntary bilateral hand activation after stroke. J Neurol Sci 239: 25-30, 2005.
48. Ridding MC, Rothwell JC. Afferent input and cortical organisation: a study with magnetic stimulation. Exp Brain Res 126: 536-544, 1999.
49. Rosenzweig ES, Brock JH, Culbertson MD, Lu P, Moseanko R, Edgerton VR, Havton LA, Tuszynski MH. Extensive spinal decussation and bilateral termination of cervical corticospinal projections in rhesus monkeys. J Comp Neurol 513: 151-163, 2009.
50. Rosenzweig ES, Courtine G, Jindrich DL, Brock JH, Ferguson AR, Strand SC, Nout YS, Roy RR, Miller DM, Beattie MS, Havton LA, Bresnahan JC, Edgerton VR, Tuszynski MH. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat Neurosci 13: 1505-1510, 2010.
51. Rothwell JC, Hallett M, Berardelli A, Eisen A, Rossini P, Paulus W. Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 52: 97-103, 1999.
52. Roy FD, Zewdie ET, Gorassini MA. Short-interval intracortical inhibition with incomplete spinal cord injury. Clin Neurophysiol 122: 1387-1395, 2011.
53. Saturno E, Bonato C, Miniussi C, Lazzaro V, Callea L. Motor cortex changes in spinal cord injury: a TMS study. Neurol Res 30: 1084-1085, 2008.
54. Sohn YH, Jung HY, Kaelin-Lang A, Hallett M. Excitability of the ipsilateral motor cortex during phasic voluntary hand movement. Exp Brain Res 148: 176-185, 2003.
55. Soteropoulos DS, Perez MA. Physiological changes underlying bilateral isometric arm voluntary contractions in healthy humans. J Neurophysiol 105: 1594-1602, 2011.
56. Stedman A, Davey NJ, Ellaway PH. Facilitation of human first dorsal interosseous muscle responses to transcranial magnetic stimulation during voluntary contraction of the contralateral homonymous muscle. Muscle Nerve 21: 1033-1039, 1998.
57. Stromberg BV. Contralateral therapy in upper extremity rehabilitation. Am J Phys Med 65: 135-143, 1986.
58. Talelli P, Waddingham W, Ewas A, Rothwell JC, Ward NS. The effect of age on task-related modulation of interhemispheric balance. Exp Brain Res 186: 59-66, 2008.
59. Taylor JL, Martin PG. Voluntary motor output is altered by spike-timing-dependent changes in the human corticospinal pathway. J Neurosci 29: 11708-11716, 2009.
60. Taylor JL, Gandevia SC. Noninvasive stimulation of the human corticospinal tract. J Appl Physiol 96: 1496-1503, 2004.
61. Thomas SL, Gorassini MA. Increases in corticospinal tract function by treadmill training after incomplete spinal cord injury. J Neurophysiol 94: 2844-2855, 2005.
62. Thomas CK, Zaidner EY, Calancie B, Broton JG, Bigland-Ritchie BR. Muscle weakness, paralysis, and atrophy after human cervical spinal cord injury. Exp Neurol 148: 414-23, 1997.
63. Ugawa Y, Genba K, Mannen T, Kanazawa I. Stimulation of corticospinal pathways at the level of the pyramidal decussation in neurological disorders. Brain 115: 1947-1961, 1992.
64. Vercauteren K, Pleysier T, Van Belle L, Swinnen SP, Wenderoth N. Unimanual muscle activation increases interhemispheric inhibition from the active to the resting hemisphere. Neurosci Lett 445: 209-213, 2008.
65. Woldag H, Lukhaup S, Renner C, Hummelsheim H. Enhanced motor cortex excitability during ipsilateral voluntary hand activation in healthy subjects and stroke patients. Stroke 35: 2556-2559, 2004.
66. Zijdewind I, Butler JE, Gandevia SC, Taylor JL. The origin of activity in the biceps brachii muscle during voluntary contractions of the contralateral elbow flexor muscles. Exp Brain Res 175: 526-535, 2006.
67. Zijdewind I, Gant K, Bakels R, Thomas CK. Do additional inputs change maximal voluntary motor unit firing rates after spinal cord injury? Neurore-habil Neural Repair 26: 58-67, 2011.