Consensus paper on short-interval intracortical inhibition and other transcranial magnetic stimulation intracortical paradigms in movement disorders

Brain Stimulation

Volumn 1, Issue 3, 2008, Pages 183-191

  Berardelli, Alfredo ^a   Abbruzzese, Giovanni ^b   Chen, Robert ^c,d   Orth, Michael ^e   Ridding, Michael C ^f   Stinear, Cathy ^g   Suppa, Antonio ^a   Trompetto, Carlo ^b   Thompson, Philip D ^h  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY HEALTH NETWORK   (Canada)

^e UNIVERSITY HOSPITAL ULM   (Germany)

^f UNIVERSITY OF ADELAIDE   (Australia)

^g UNIVERSITY OF AUCKLAND   (New Zealand)

^h ROYAL ADELAIDE HOSPITAL   (Australia)

Author keywords

movement disorders; primary motor cortex; transcranial magnetic stimulation

Indexed keywords

BOTULINUM TOXIN; LEVODOPA; PERGOLIDE;

ATAXIA; ATTENTION DEFICIT DISORDER; BASAL GANGLION; CEREBELLUM; CHOREA; COMORBIDITY; DYSTONIA; ESSENTIAL TREMOR; EVOKED MUSCLE RESPONSE; FACILITATION; GILLES DE LA TOURETTE SYNDROME; HUMAN; MOTOR CORTEX; MOTOR DYSFUNCTION; MYOCLONUS; MYOCLONUS EPILEPSY; OBSESSIVE COMPULSIVE DISORDER; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; TRANSCRANIAL MAGNETIC STIMULATION; BRAIN CORTEX; CONSENSUS; MOVEMENT DISORDERS; NERVE TRACT; PHYSIOLOGY; PROCEDURES;

CEREBRAL CORTEX; CONSENSUS; HUMANS; MOVEMENT DISORDERS; NEURAL PATHWAYS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 49649127191     PISSN: 1935861X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brs.2008.06.005     Document Type: Review

References (103)

1. Kujirai T., Caramia M.D., Rothwell J.C., et al. Corticocortical inhibition in human motor cortex. J Physiol 471 (1993) 501-519
2. Nakamura H., Kitagawa H., Kawaguchi Y., and Tsuji H. Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J Physiol 498 (1997) 817-823
3. Di Lazzaro V., Restuccia D., Oliviero A., et al. Magnetic transcranial stimulation at intensities below active motor threshold activates inhibitory circuits. Exp Brain Res 119 (1998) 265-268
4. Di Lazzaro V., Pilato F., Oliviero A., et al. 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
5. Fisher J., Nakamura Y., Bestmann S., Rothwell J.C., and Bostock H. Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking. Exp Brain Res 143 (2002) 240-248
6. Roshan L., Paradiso G.O., and Chen R. Two phases of short-interval intracortical inhibition. Exp Brain Res 151 (2003) 330-337
7. Chan J.H., Lin C.S., Pierrot-Deseilligny E., and Burke D. Excitability changes in human peripheral nerve axons in a paradigm mimicking paired-pulse transcranial magnetic stimulation. J Physiol 542 (2002) 951-961
8. Strafella A.P., and Paus T. Cerebral blood-flow changes induced by paired-pulse transcranial magnetic stimulation of the primary motor cortex. J Neurophysiol 85 (2001) 2624-2629
9. Schafer M., Biesecker J.C., Schulze-Bonhage A., and Ferbert A. Transcranial magnetic double stimulation: influence of the intensity of the conditioning stimulus. Electroencephalogr Clin Neurophysiol 105 (1997) 462-469
10. Ilic T.V., Meintzschel F., Cleff U., et al. Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol 545 (2002) 153-167
11. Butefisch C.M., Netz J., Wessling M., Seitz R.J., and Homberg V. Remote changes in cortical excitability after stroke. Brain 126 (2003) 470-481
12. Ziemann U., Lönnecker S., Steinhoff B.J., and Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 109 (1996) 127-135
13. Ziemann U., Lönnecker S., Steinhoff B.J., and Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40 (1996) 367-378
14. Liepert J., Schwenkreis P., Tegenthoff M., and Malin J.P. The glutamate antagonist riluzole suppresses intracortical facilitation. J Neural Transm 104 (1997) 1207-1214
15. Ziemann U., Chen R., Cohen L.G., and Hallett M. Dextromethorphan decreases the excitability of the human motor cortex. Neurology 51 (1998) 1320-1324
16. Chen R., Samii A., Caños M., Wassermann E., and Hallett M. Effects of phenytoin on cortical excitability in humans. Neurology 49 (1997) 881-883
17. Ziemann U. TMS and drugs. Clin Neurophysiol 115 (2004) 1717-1729
18. Valls-Sole J., Pascual-Leone A., Wassermann E.M., and Hallett M. Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol 85 (1992) 355-364
19. Wassermann E.M., Samii A., Mercuri B., et al. Responses to paired transcranial magnetic stimuli in resting, active, and recently activated muscle. Exp Brain Res 109 (1996) 158-163
20. Chen R., Lozano A.M., and Ashby P. Mechanism of the silent period following transcranial magnetic stimulation. Evidence from epidural recordings. Exp Brain Res 128 (1999) 539-542
21. Di Lazzaro V., Oliviero A., Mazzone P., et al. Direct demonstration of long latency cortico-cortical inhibition in normal subjects and in a patient with vascular parkinsonism. Clin Neurophysiol 113 (2002) 1673-1679
22. Roick H., von Giesen R., and Benecke R. On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects. Exp Brain Res 94 (1993) 489-498
23. Siebner H.R., Dressnandt J., Auer C., and Conrad B. Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve 21 (1998) 1209-1212
24. Werhahn K.J., Kunesch E., Noachtar S., Benecke R., and Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol 517 (1999) 591-597
25. McDonnell M.N., Orekhov Y., and Ziemann U. The role of GABA(B) receptors in intracortical inhibition in the human motor cortex. Exp Brain Res 173 (2006) 86-93
26. Sanger T.D., Garg R.R., and Chen R. Interactions between two different inhibitory systems in the human motor cortex. J Physiol 530 (2001) 307-317
27. Ridding M.C., Inzelberg R., and Rothwell J.C. Changes in excitability of motor cortical circuitry in patients with Parkinson's disease. Ann Neurol 37 (1995) 181-188
28. Bares M., Kanovsky P., Klajblova H., and Rektor I. Intracortical inhibition and facilitation are impaired in patients with early Parkinson's disease: a paired TMS study. Eur J Neurol 10 (2003) 385-389
29. Hanajima R., Ugawa Y., Terao Y., Ogata K., and Kanazawa I. Ipsilateral cortico-cortical inhibition of the motor cortex in various neurological disorders. J Neurol Sci 140 (1996) 109-116
30. Strafella A.P., Valzania F., Nassetti S.A., et al. Effects of chronic levodopa and pergolide treatment on cortical excitability in patients with Parkinson's disease: a transcranial magnetic stimulation study. Clin Neurophysiol 111 (2000) 1198-1202
31. MacKinnon C.D., Gilley E.A., Weis-McNulty A., and Simuni T. Pathways mediating abnormal intracortical inhibition in Parkinson's disease. Ann Neurol 58 (2005) 516-524
32. Ziemann U., Tergau F., Wassermann E.M., et al. Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J Physiol 511 (1998) 181-190
33. Berardelli A., Rona S., Inghilleri M., and Manfredi M. Cortical inhibition in Parkinson's disease. A study with paired magnetic stimulation. Brain 119 Pt 1 (1996) 71-77
34. Ridding M.C., Taylor J.L., and Rothwell J.C. The effect of voluntary contraction on cortico-cortical inhibition in human motor cortex. J Physiol 487 (1995) 541-548
35. Stinear C.M., and Byblow W.D. Elevated threshold for intracortical inhibition in focal hand dystonia. Mov Disord 19 (2004) 1312-1317
36. Stinear C.M., and Byblow W.D. Impaired modulation of intracortical inhibition in focal hand dystonia. Cereb Cortex 14 (2004) 555-561
37. Butefisch C.M., Boroojerdi B., Chen R., Battaglia F., and Hallett M. Task-dependent intracortical inhibition is impaired in focal hand dystonia. Mov Disord 20 (2005) 545-551
38. Stinear C.M., and Byblow W.D. Role of intracortical inhibition in selective hand muscle activation. J Neurophysiol 89 (2003) 2014-2020
39. Zoghi M., Pearce S.L., and Nordstrom M.A. Differential modulation of intracortical inhibition in human motor cortex during selective activation of an intrinsic hand muscle. J Physiol 550 (2003) 933-946
40. Stinear C.M., and Byblow W.D. Impaired modulation of corticospinal excitability following subthreshold rTMS in focal hand dystonia. Hum Mov Sci 23 (2004) 527-538
41. Hanajima R., and Ugawa Y. Intracortical inhibition of the motor cortex in movement disorders. Brain Dev 22 Suppl. 1 (2000) S132-S135
42. Marchese R., Trompetto C., Buccolieri A., and Abbruzzese G. Abnormalities of motor cortical excitability are not correlated with clinical features in atypical parkinsonism. Mov Disord 15 (2000) 1210-1214
43. Pierantozzi M., Palmieri M.G., Marciani M.G., et al. Effect of apomorphine on cortical inhibition in Parkinson's disease patients: a transcranial magnetic stimulation study. Exp Brain Res 141 (2001) 52-62
44. Avanzino L., Martino D., van de Warrenburg B.P., et al. Cortical excitability is abnormal in patients with the "fixed dystonia" syndrome. Mov Disord 23 5 (2008) 646-652
45. Espay A.J., Morgante F., Purzner J., et al. Cortical and spinal abnormalities in psychogenic dystonia. Ann Neurol 59 (2006) 825-834
46. Ridding M.C., Sheean G., Rothwell J.C., Inzelberg R., and Kujirai T. Changes in the balance between motor cortical excitation and inhibition in focal, task specific dystonia. J Neurol Neurosurg Psychiatry 59 (1995) 493-498
47. Sommer M., Ruge D., Tergau F., et al. Intracortical excitability in the hand motor representation in hand dystonia and blepharospasm. Mov Disord 17 (2002) 1017-1025
48. Kanovsky P., Bares M., Streitova H., et al. Abnormalities of cortical excitability and cortical inhibition in cervical dystonia Evidence from somatosensory evoked potentials and paired transcranial magnetic stimulation recordings. J Neurol 250 (2003) 42-50
49. Huang Y.Z., Trender-Gerhard I., Edwards M.J., et al. Motor system inhibition in dopa-responsive dystonia and its modulation by treatment. Neurology 66 (2006) 1088-1090
50. Edwards M.J., Huang Y.Z., Wood N.W., Rothwell J.C., and Bhatia K.P. Different patterns of electrophysiological deficits in manifesting and non-manifesting carriers of the DYT1 gene mutation. Brain 126 (2003) 2074-2080
51. Hanajima R., Furubayashi T., Kobayashi Iwata N., et al. Further evidence to support different mechanisms underlying intracortical inhibition of the motor cortex. Exp Brain Res 151 (2003) 427-434
52. Gilio F., Curra A., Inghilleri M., et al. Abnormalities of motor cortex excitability preceding movement in patients with dystonia. Brain 126 (2003) 1745-1754
53. McDonnell M.N., Thompson P.D., and Ridding M.C. The effect of cutaneous input on intracortical inhibition in focal task-specific dystonia. Mov Disord 22 (2007) 1286-1292
54. Simonetta-Moreau M., Lourenco G., Sangla S., et al. Lack of inhibitory interaction between somatosensory afferent inputs and intracortical inhibitory interneurons in focal hand dystonia. Mov Disord 21 (2006) 824-834
55. Rosenkranz K., Williamon A., Butler K., et al. Pathophysiological differences between musician's dystonia and writer's cramp. Brain 128 (2005) 918-931
56. Rosenkranz K., Butler K., Williamon A., et al. Sensorimotor reorganization by proprioceptive training in musician's dystonia and writer's cramp. Neurology 70 (2008) 304-315
57. Chen R., Wassermann E.M., Canos M., and Hallett M. Impaired inhibition in writer's cramp during voluntary muscle activation. Neurology 49 (1997) 1054-1059
58. Rona S., Berardelli A., Vacca L., Inghilleri M., and Manfredi M. Alterations of motor cortical inhibition in patients with dystonia. Mov Disord 13 (1998) 118-124
59. Sheean G. Restoring balance in focal limb dystonia with botulinum toxin. Disabil Rehabil 29 (2007) 1778-1788
60. Gilio F., Curra A., Lorenzano C., et al. Effects of botulinum toxin type A on intracortical inhibition in patients with dystonia. Ann Neurol 48 (2000) 20-26
61. Boroojerdi B., Cohen L.G., and Hallett M. Effects of botulinum toxin on motor system excitability in patients with writer's cramp. Neurology 61 (2003) 1546-1550
62. Siebner H.R., Tormos J.M., Ceballos-Baumann A.O., et al. Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer's cramp. Neurology 52 (1999) 529-537
63. Zeuner K.E., Shill H.A., Sohn Y.H., et al. Motor training as treatment in focal hand dystonia. Mov Disord 20 (2005) 335-341
64. Chen R., and Hallett M. Focal dystonia and repetitive motion disorders. Clin Orthop Relat Res 351 (1998) 102-106
65. Classen J. Focal hand dystonia-a disorder of neuroplasticity?. Brain 126 (2003) 2571-2572
66. Quartarone A., Siebner H.R., and Rothwell J.C. Task-specific hand dystonia: can too much plasticity be bad for you?. Trends Neurosci 29 4 (2006) 192-199
67. Koch G., Schneider S., Baumer T., et al. Altered dorsal premotor-motor interhemispheric pathway activity in focal arm dystonia. Mov Disord 23 5 (2008) 660-668
68. Daskalakis Z.J., Christensen B.K., Chen R., et al. Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation. Arch Gen Psychiatry 59 4 (2002) 347-354
69. Abbruzzese G., Buccolieri A., Marchese R., et al. Intracortical inhibition and facilitation are abnormal in Huntington's disease: a paired magnetic stimulation study. Neurosci Lett 228 (1997) 87-90
70. Hanajima R., Ugawa Y., Terao Y., et al. Intracortical inhibition of the motor cortex is normal in chorea. J Neurol Neurosurg Psychiatry 66 (1999) 783-786
71. Nardone R., Lochner P., Marth R., et al. Abnormal intracortical facilitation in early-stage Huntington's disease. Clin Neurophysiol 118 (2007) 1149-1154
72. Abbruzzese G., Marchese R., and Trompetto C. Motor cortical excitability in Huntington's disease. J Neurol Neurosurg Psychiatry 68 (2000) 120-121
73. Modugno N., Currà A., Giovannelli M., et al. The prolonged cortical silent period in patients with Huntington's disease. Clin Neurophysiol 112 (2001) 1470-1474
74. Tegenthoff M., Vorgerd M., Juskowiak F., Roos V., and Malin J.P. Postexcitatory inhibition after transcranial magnetic single and double brain stimulation in Huntington's disease. Clin Neurophysiol 101 (1996) 298-303
75. Priori A., Polidori L., Rona S., Manfredi M., and Berardelli A. Spinal and cortical inhibition in Huntington's chorea. Mov Disord 15 (2000) 938-946
76. Orth M., Amann B., Robertson M.M., and Rothwell J.C. Excitability of motor cortex inhibitory circuits in Tourette syndrome before and after single dose nicotine. Brain 128 (2005) 1292-1300
77. Ziemann U., Paulus W., and Rothenberger A. Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. Am J Psychiatry 154 (1997) 1277-1284
78. Gilbert D.L., Sallee F.R., Zhang J., Lipps T.D., and Wassermann E.M. Transcranial magnetic stimulation-evoked cortical inhibition: a consistent marker of attention-deficit/hyperactivity disorder scores in tourette syndrome. Biol Psychiatry 57 (2005) 1597-1600
79. Orth M., Munchau A., and Rothwell J.C. Corticospinal system excitability at rest is associated with tic severity in Tourette Syndrome. [published online ahead of print February 1, 2008]. Biol Psychiatry (2008) 10.1016/j.biopsych.2007.12.009
80. Chen R., Yaseen Z., Cohen L.G., and Hallett M. Time course of corticospinal excitability in reaction time and self- paced movements. Ann Neurol 44 (1998) 317-325
81. Buchmann J., Gierow W., Weber S., et al. Restoration of disturbed intracortical motor inhibition and facilitation in attention deficit hyperactivity disorder children by methylphenidate. Biol Psychiatry 62 (2007) 963-969
82. Moll G.H., Heinrich H., Trott G.E., et al. Children with comorbid attention-deficit-hyperactivity disorder and tic disorder: evidence for additive inhibitory deficits within the motor system. Ann Neurol 49 (2001) 393-396
83. Richter M.M., Ehlis A.C., Jacob C.P., and Fallgatter A.J. Cortical excitability in adult patients with attention-deficit/hyperactivity disorder (ADHD). Neurosci Lett 419 (2007) 137-141
84. Greenberg B.D., Ziemann U., Cora-Locatelli G., et al. Altered cortical excitability in obsessive-compulsive disorder. Neurology 54 (2000) 142-147
85. Manganotti P., Bongiovanni L.G., Zanette G., and Fiaschi A. Early and late intracortical inhibition in juvenile myoclonic epilepsy. Epilepsia 41 9 (2000) 1129-1138
86. Manganotti P, Tamburin S, Zanette G, Fiaschi A. Hyperexcitable cortical responses in progressive myoclonic epilepsy: a TMS study. Neurology 2001;27;57(10):1793-1799.
87. Manganotti P., Tamburin S., Bongiovanni L.G., Zanette G., and Fiaschi A. Motor responses to afferent stimulation in juvenile myoclonic epilepsy. Epilepsia 45 1 (2004) 77-80
88. Cantello R. Applications of transcranial magnetic stimulation in movement disorders. J Clin Neurophysiol 19 4 (2002) 272-293
89. Lefaucheur J.P. Myoclonus and transcranial magnetic stimulation. Neurophysiol Clin 36 5-6 (2006) 293-297
90. Chen R., Cros D., Curra A., et al. The clinical diagnostic utility of transcranial magnetic stimulation: Report of an IFCN committee. Clin Neurophysiol 119 (2008) 504-532
91. Valzania F., Strafella A.P., Tropeani A., et al. Facilitation of rhythmic events in progressive myoclonus epilepsy: a transcranial magnetic stimulation study. Clin Neurophysiol 110 1 (1999) 152-157
92. van Rootselaar A.F., van der Salm S.M., Bour L.J., et al. Decreased cortical inhibition and yet cerebellar pathology in familial cortical myoclonic tremor with epilepsy. Mov Disord 22 16 (2007) 2378-2385
93. Suppa A., Brancati F., Marianetti M., et al. Familial cortical myoclonic tremor with epilepsy: a new italian pedigree linked to chromosome 2p11.1-q12.2. Mov Disord (2008) abstract
94. Brown P., Ridding M.C., Werhahn K.J., et al. Abnormalities of the balance between inhibition and excitation in the motor cortex of patients with cortical myoclonus. Brain 119 (1996) 309-317
95. Britton T.C., Thompson P.D., Day B.L., et al. Modulation of postural wrist tremors by magnetic stimulation of the motor cortex in patients with Parkinson's disease or essential tremor and in normal subjects mimicking tremor. Ann Neurol 33 5 (1993) 473-479
96. Romeo S., Berardelli A., Pedace F., et al. Cortical excitability in patients with essential tremor. Muscle Nerve 21 10 (1998) 1304-1308
97. Modugno N., Nakamura Y., Bestmann S., et al. Neurophysiological investigations in patients with primary writing tremor. Mov Disord 17 6 (2002) 1336-1340
98. Ugawa Y., Hanajima R., and Kanazawa I. Motor cortex inhibition in patients with ataxia. Electroencephalogr Clin Neurophysiol 93 3 (1994) 225-229
99. Wessel K., Tegenthoff M., Vorgerd M., et al. Enhancement of inhibitory mechanisms in the motor cortex of patients with cerebellar degeneration: a study with transcranial magnetic brain stimulation. Electroencephalogr Clin Neurophysiol 101 4 (1996) 273-280
100. Liepert J., Wessel K., Schwenkreis P., et al. Reduced intracortical facilitation in patients with cerebellar degeneration. Acta Neurol Scand 98 5 (1998) 318-323
101. Schwenkreis P., Tegenthoff M., Witscher K., et al. Motor cortex activation by transcranial magnetic stimulation in ataxia patients depends on the genetic defect. Brain 125 Pt 2 (2002) 301-309
102. Restivo D.A., Lanza S., Saponara R., et al. Changes of cortical excitability of human motor cortex in spinocerebellar ataxia type 2: a study with paired transcranial magnetic stimulation. J Neurol Sci 198 1-2 (2002) 87-92
103. Tamburin S., Fiaschi A., Marani S., et al. Enhanced intracortical inhibition in cerebellar patients. J Neurol Sci 217 2 (2004) 205-210