Annals of Clinical Neurophysiology

The Korean Society of Clinical Neurophysiology (대한임상신경생리학회)
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Neurophysiological Evaluation of the Motor System Using Transcranial Magnetic Stimulation

뇌자기자극을 이용한 운동신경계의 신경생리학적 평가

  • Shin, Hae-Won (Department of Neurology, Chung-Ang University College of Medicine) ;
  • Sohn, Young-H. (Department of Neurology, Yonsei University College of Medicine)
  • 신혜원 (중앙대학교 의과대학 신경과학교실) ;
  • 손영호 (연세대학교 의과대학 신경과학교실)
  • Received : 2011.05.31
  • Accepted : 2011.06.02
  • Published : 2011.06.30
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Abstract

Transcranial magnetic stimulation (TMS) is a non-invasive tool used to study aspects of human brain physiology, including motor function and the pathophysiology of various brain disorders. A brief electric current passed through a magnetic coil produces a high-intensity magnetic field, which can excite or inhibit the cerebral cortex. Although various brain regions can be evaluated by TMS, most studies have focused on the motor cortex where motor evoked potentials (MEPs) are produced. Single-pulse and paired-pulse TMS can be used to measure the excitability of the motor cortex via various parameters, while repetitive TMS induces cortical plasticity via long-term potentiation or long-term depression-like mechanisms. Therefore, TMS is useful in the evaluation of physiological mechanisms of various neurological diseases, including movement disorders and epilepsy. In addition, it has diagnostic utility in spinal cord diseases, amyotrophic lateral sclerosis and demyelinating diseases. The therapeutic effects of repetitive TMS on stroke, Parkinson disease and focal hand dystonia are limited since the duration and clinical benefits seem to be temporary. New TMS techniques, which may improve clinical utility, are being developed to enhance clinical utilities in various neurological diseases.

Keywords

References

  1. Hallett M. Transcranial magnetic stimulation: a primer. Neuron 2007;55:187-199. https://doi.org/10.1016/j.neuron.2007.06.026
  2. Merton PA, Morton HB. Stimulation of the cerebral cortex in the intact human subject. Nature 1980;285:227. https://doi.org/10.1038/285227a0
  3. Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet 1985;1:1106-1107.
  4. Terao Y, Ugawa Y. Basic mechanisms of TMS. J Clin Neurophysiol 2002;19:322-343. https://doi.org/10.1097/00004691-200208000-00006
  5. Hallett M. Transcranial magnetic stimulation and the human brain. Nature 2000;406:147-150. https://doi.org/10.1038/35018000
  6. Rothwell JC. Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods 1997;74:113-122. https://doi.org/10.1016/S0165-0270(97)02242-5
  7. Rossini PM, Rossi S. Transcranial magnetic stimulation: diagnostic, therapeutic, and research potential. Neurology 2007;68:484-488. https://doi.org/10.1212/01.wnl.0000250268.13789.b2
  8. Sohn YH, Hallett M. Transcranial magnetic stimulation. In: Bradley WG, Daroff RB, Fenichel GM, Jankovic J. Neurology in clinical practice. 5th ed. Philadelphia: Butterworth Heinemann Elsevier. 2008;511-516.
  9. Kernell D, Chien-Ping WU. Responses of the pyramidal tract to stimulation of the baboon's motor cortex. J Physiol 1967;191:653-672 https://doi.org/10.1113/jphysiol.1967.sp008273
  10. Di Lazzaro V, Oliviero A, Profice P, Saturno E, Pilato F, Insola A, et al. Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. Electroencephalogr Clin Neurophysiol 1998;109:397-401. https://doi.org/10.1016/S0924-980X(98)00038-1
  11. Ziemann U. TMS and drugs. Clin Neurophysiol 2004;115:1717-1729. https://doi.org/10.1016/j.clinph.2004.03.006
  12. Chen R, Lozano AM, Ashby P. Mechanism of the silent period following transcranial magnetic stimulation. Evidence from epidural recordings. Exp Brain Res 1999;128:539-542. https://doi.org/10.1007/s002210050878
  13. Curra A, Modugno N, Inghilleri M, Manfredi M, Hallett M, Berardelli A. Transcranial magnetic stimulation techniques in clinical investigation. Neurology 2002;59:1851-1859. https://doi.org/10.1212/01.WNL.0000038744.30298.D4
  14. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol 1999;517:591-597. https://doi.org/10.1111/j.1469-7793.1999.0591t.x
  15. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol 1993;471:501-519. https://doi.org/10.1113/jphysiol.1993.sp019912
  16. Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 1996;109:127-135.
  17. Ziemann U, Chen R, Cohen LG, Hallett M. Dextromethorphan decreases the excitability of the human motor cortex. Neurology 1998;51:1320-1324. https://doi.org/10.1212/WNL.51.5.1320
  18. Wassermann EM, Samii A, Mercuri B, Ikoma K, Oddo D, Grill SE, et al. Responses to paired transcranial magnetic stimuli in resting, active, and recently activated muscles. Exp Brain Res 1996;109:158-163.
  19. McDonnell MN, Orekhov Y, Ziemann U. The role of GABA(B) receptors in intracortical inhibition in the human motor cortex. Exp Brain Res 2006;173:86-93. https://doi.org/10.1007/s00221-006-0365-2
  20. Reis J, Swayne OB, Vandermeeren Y, Camus M, Dimyan MA, Harris-Love M, et al. Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control. J Physiol 2008;586:325-351. https://doi.org/10.1113/jphysiol.2007.144824
  21. Ziemann U, Tergau F, Wassermann EM, Wischer S, Hildebrandt J, Paulus W. Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J Physiol 1998;511:181-190. https://doi.org/10.1111/j.1469-7793.1998.181bi.x
  22. Rouiller EM, Babalian A, Kazennikov O, Moret V, Yu XH, Wiesendanger M. Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys. Exp Brain Res 1994;102:227-243.
  23. Wahl M, Lauterbach-Soon B, Hattingen E, Jung P, Singer O, Volz S, et al. Human motor corpus callosum: topography, somatotopy, and link between microstructure and function. J Neurosci 2007;27:12132-12138. https://doi.org/10.1523/JNEUROSCI.2320-07.2007
  24. Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD. Interhemispheric inhibition of the human motor cortex. J Physiol 1992;453:525-546. https://doi.org/10.1113/jphysiol.1992.sp019243
  25. Hanajima R, Ugawa Y, Machii K, Mochizuki H, Terao Y, Enomoto H, et al. Interhemispheric facilitation of the hand motor area in humans. J Physiol 2001;531:849-859. https://doi.org/10.1111/j.1469-7793.2001.0849h.x
  26. Chen R. Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res 2004;154:1-10. https://doi.org/10.1007/s00221-003-1684-1
  27. Di Lazzaro V, Oliviero A, Profice P, Pennisi MA, Di Giovanni S, Zito G, et al. Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex. Exp Brain Res 2000;135:455-461. https://doi.org/10.1007/s002210000543
  28. Di Lazzaro V, Oliviero A, Tonali PA, Marra C, Daniele A, Profice P, et al. Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation. Neurology 2002;59:392-397. https://doi.org/10.1212/WNL.59.3.392
  29. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Marra C, et al. Neurophysiological predictors of long term response to AChE inhibitors in AD patients. J Neurol Neurosurg Psychiatry 2005;76:1064-1069. https://doi.org/10.1136/jnnp.2004.051334
  30. Nardone R, Marth R, Ausserer H, Bratti A, Tezzon F. Reduced short latency afferent inhibition in patients with Down syndrome and Alzheimer-type dementia. Clin Neurophysiol 2006;117:2204-2210. https://doi.org/10.1016/j.clinph.2006.07.134
  31. Sohn YH, Hallett M. Surround inhibition in human motor system. Exp Brain Res 2004;158:397-404.
  32. Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 1994;117:847-858. https://doi.org/10.1093/brain/117.4.847
  33. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 1997;48:1398-1403. https://doi.org/10.1212/WNL.48.5.1398
  34. Bliss TV, Gardner-Medwin AR. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 1973;232:357-374. https://doi.org/10.1113/jphysiol.1973.sp010274
  35. Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 1973;232:331-356. https://doi.org/10.1113/jphysiol.1973.sp010273
  36. Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 2000;123:572-584. https://doi.org/10.1093/brain/123.3.572
  37. Di Lazzaro V, Dileone M, Profice P, Pilato F, Oliviero A, Mazzone P, et al. LTD-like plasticity induced by paired associative stimulation: direct evidence in humans. Exp Brain Res 2009;194:661-664. https://doi.org/10.1007/s00221-009-1774-9
  38. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron 2005;45:201-206. https://doi.org/10.1016/j.neuron.2004.12.033
  39. Hamada M, Ugawa Y. Quadripulse stimulation--a new patterned rTMS. Restor Neurol Neurosci 28:419-424.
  40. Lo YL, Chan LL, Lim W, Tan SB, Tan CT, Chen JL, et al. Systematic correlation of transcranial magnetic stimulation and magnetic resonance imaging in cervical spondylotic myelopathy. Spine (Phila Pa 1976) 2004;29:1137-1145. https://doi.org/10.1097/00007632-200405150-00017
  41. Mills KR. The natural history of central motor abnormalities in amyotrophic lateral sclerosis. Brain 2003;126:2558-2566. https://doi.org/10.1093/brain/awg260
  42. Truffert A, Rosler KM, Magistris MR. Amyotrophic lateral sclerosis versus cervical spondylotic myelopathy: a study using transcranial magnetic stimulation with recordings from the trapezius and limb muscles. Clin Neurophysiol 2000;111:1031-1038. https://doi.org/10.1016/S1388-2457(00)00292-3
  43. Ziemann U, Winter M, Reimers CD, Reimers K, Tergau F, Paulus W. Impaired motor cortex inhibition in patients with amyotrophic lateral sclerosis. Evidence from paired transcranial magnetic stimulation. Neurology 1997;49:1292-1298. https://doi.org/10.1212/WNL.49.5.1292
  44. Beer S, Rosler KM, Hess CW. Diagnostic value of paraclinical tests in multiple sclerosis: relative sensitivities and specificities for reclassification according to the Poser committee criteria. J Neurol Neurosurg Psychiatry 1995;59:152-159. https://doi.org/10.1136/jnnp.59.2.152
  45. Humm AM, Magistris MR, Truffert A, Hess CW, Rosler KM. Central motor conduction differs between acute relapsing-remitting and chronic progressive multiple sclerosis. Clin Neurophysiol 2003;114:2196-2203. https://doi.org/10.1016/S1388-2457(03)00231-1
  46. Kandler RH, Jarratt JA, Davies-Jones GA, Gumpert EJ, Venables GS, Sagar HJ, et al. The role of magnetic stimulation as a quantifier of motor disability in patients with multiple sclerosis. J Neurol Sci 1991;106:31-34. https://doi.org/10.1016/0022-510X(91)90190-I
  47. Kandler RH, Jarratt JA, Gumpert EJ, Davies-Jones GA, Venables GS, Sagar HJ. The role of magnetic stimulation in the diagnosis of multiple sclerosis. J Neurol Sci 1991;106:25-30. https://doi.org/10.1016/0022-510X(91)90189-E
  48. Hendricks HT, van Limbeek J, Geurts AC, Zwarts MJ. Motor recovery after stroke: a systematic review of the literature. Arch Phys Med Rehabil 2002;83:1629-1637. https://doi.org/10.1053/apmr.2002.35473
  49. Cantello R. Applications of transcranial magnetic stimulation in movement disorders. J Clin Neurophysiol 2002;19:272-293. https://doi.org/10.1097/00004691-200208000-00003
  50. Lefaucheur JP. Motor cortex dysfunction revealed by cortical excitability studies in Parkinson's disease: influence of antiparkinsonian treatment and cortical stimulation. Clin Neurophysiol 2005;116:244-253. https://doi.org/10.1016/j.clinph.2004.11.017
  51. Mink JW. The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 1996;50:381-425. https://doi.org/10.1016/S0301-0082(96)00042-1
  52. Shin HW, Kang SY, Sohn YH. Disturbed surround inhibition in preclinical parkinsonism. Clin Neurophysiol 2007;118:2176-2179. https://doi.org/10.1016/j.clinph.2007.06.058
  53. Sohn YH, Hallett M. Disturbed surround inhibition in focal hand dystonia. Ann Neurol 2004;56:595-599. https://doi.org/10.1002/ana.20270
  54. Quartarone A, Bagnato S, Rizzo V, Siebner HR, Dattola V, Scalfari A, et al. Abnormal associative plasticity of the human motor cortex in writer's cramp. Brain 2003;126:2586-2596. https://doi.org/10.1093/brain/awg273
  55. Quartarone A, Rizzo V, Bagnato S, Morgante F, Sant'Angelo A, Romano M, et al. Homeostatic-like plasticity of the primary motor hand area is impaired in focal hand dystonia. Brain 2005;128:1943-1950. https://doi.org/10.1093/brain/awh527
  56. Morgante F, Espay AJ, Gunraj C, Lang AE, Chen R. Motor cortex plasticity in Parkinson's disease and levodopa-induced dyskinesias. Brain 2006;129:1059-1069. https://doi.org/10.1093/brain/awl031
  57. Macdonell RA, King MA, Newton MR, Curatolo JM, Reutens DC, Berkovic SF. Prolonged cortical silent period after transcranial magnetic stimulation in generalized epilepsy. Neurology 2001;57:706-708. https://doi.org/10.1212/WNL.57.4.706
  58. Reutens DC, Berkovic SF. Increased cortical excitability in generalised epilepsy demonstrated with transcranial magnetic stimulation. Lancet 1992;339:362-363.
  59. Tassinari CA, Cincotta M, Zaccara G, Michelucci R. Transcranial magnetic stimulation and epilepsy. Clin Neurophysiol 2003;114:777-798. https://doi.org/10.1016/S1388-2457(03)00004-X
  60. Brown P, Ridding MC, Werhahn KJ, Rothwell JC, Marsden CD. Abnormalities of the balance between inhibition and excitation in the motor cortex of patients with cortical myoclonus. Brain 1996;119:309-317. https://doi.org/10.1093/brain/119.1.309
  61. Manganotti P, Tamburin S, Zanette G, Fiaschi A. Hyperexcitable cortical responses in progressive myoclonic epilepsy: a TMS study. Neurology 2001;57:1793-1799. https://doi.org/10.1212/WNL.57.10.1793
  62. Inghilleri M, Mattia D, Berardelli A, Manfredi M. Asymmetry of cortical excitability revealed by transcranial stimulation in a patient with focal motor epilepsy and cortical myoclonus. Electroencephalogr Clin Neurophysiol 1998;109:70-72. https://doi.org/10.1016/S0924-980X(97)00062-3
  63. Rizzo V, Quartarone A, Bagnato S, Battaglia F, Majorana G, Girlanda P. Modification of cortical excitability induced by gabapentin: a study by transcranial magnetic stimulation. Neurol Sci 2001;22:229-232. https://doi.org/10.1007/s100720100002
  64. Sohn YH, Kaelin-Lang A, Jung HY, Hallett M. Effect of levetiracetam on human corticospinal excitability. Neurology 2001;57:858-863. https://doi.org/10.1212/WNL.57.5.858
  65. Strafella AP, Paus T, Barrett J, Dagher A. Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci 2001;21:RC157.
  66. Edwards MJ, Talelli P, Rothwell JC. Clinical applications of transcranial magnetic stimulation in patients with movement disorders. Lancet Neurol 2008;7:827-840. https://doi.org/10.1016/S1474-4422(08)70190-X
  67. Calabresi P, Giacomini P, Centonze D, Bernardi G. Levodopainduced dyskinesia: a pathological form of striatal synaptic plasticity? Ann Neurol 2000;47:S60-68; discussion S68-69.
  68. Rektorova I, Sedlackova S, Telecka S, Hlubocky A, Rektor I. Dorsolateral prefrontal cortex: a possible target for modulating dyskinesias in Parkinson's disease by repetitive transcranial magnetic stimulation. Int J Biomed Imaging 2008;2008:372125.
  69. Koch G, Brusa L, Caltagirone C, Peppe A, Oliveri M, Stanzione P, et al. rTMS of supplementary motor area modulates therapyinduced dyskinesias in Parkinson disease. Neurology 2005;65:623-625. https://doi.org/10.1212/01.wnl.0000172861.36430.95
  70. Ceballos-Baumann AO, Passingham RE, Warner T, Playford ED, Marsden CD, Brooks DJ. Overactive prefrontal and underactive motor cortical areas in idiopathic dystonia. Ann Neurol 1995;37:363-372. https://doi.org/10.1002/ana.410370313
  71. Murase N, Rothwell JC, Kaji R, Urushihara R, Nakamura K, Murayama N, et al. Subthreshold low-frequency repetitive transcranial magnetic stimulation over the premotor cortex modulates writer's cramp. Brain 2005;128:104-115.
  72. Siebner HR, Tormos JM, Ceballos-Baumann AO, Auer C, Catala MD, Conrad B, et al. Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer's cramp. Neurology 1999;52:529-537. https://doi.org/10.1212/WNL.52.3.529
  73. Khedr EM, Ahmed MA, Fathy N, Rothwell JC. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology 2005;65:466-468. https://doi.org/10.1212/01.wnl.0000173067.84247.36
  74. Kim YH, You SH, Ko MH, Park JW, Lee KH, Jang SH, et al. Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke 2006;37:1471-1476. https://doi.org/10.1161/01.STR.0000221233.55497.51
  75. Takeuchi N, Chuma T, Matsuo Y, Watanabe I, Ikoma K. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 2005;36:2681-2686. https://doi.org/10.1161/01.STR.0000189658.51972.34