Advertisement

Psychopharmacology

, Volume 168, Issue 4, pp 359–376 | Cite as

Transcranial magnetic stimulation: studying motor neurophysiology of psychiatric disorders

  • Fumiko Maeda
  • Alvaro Pascual-LeoneEmail author
Review

Abstract

Rationale.

Transcranial magnetic stimulation (TMS) is a noninvasive tool that directly stimulates cortical neurons by inducing magnetic and secondary electric fields. Traditionally TMS has been used to study the motor neurophysiology of healthy subjects and those with neurological disorders.

Objective.

Given the known motor dysfunctions in many psychiatric disorders supplemental usage of TMS to study the underlying pathophysiology of certain psychiatric disorders and to assess treatment outcomes is underway. Such studies include examination of motor neuronal membrane, corticospinal and intracortical excitability. Our objective is to overview the past findings.

Methods.

We review the past literature that used TMS as an assessment tool in psychiatric disorders such as schizophrenia, mood disorders, Tourette's syndrome, obsessive-compulsive disorder, attention-deficit hyperactivity disorder, and substance abuse.

Results.

While the findings are still preliminary due to small sample-size, inconsistent patient population (diagnosis, medication), differences in methodology between research groups, studies restricted to the motor region and possible lack of sensitivity and specificity, the studies are yielding interesting results which could potentially lead to trait- and state-markers of psychiatric disorders.

Conclusions.

Future studies using TMS alone or in combination with other neuroimaging techniques promise to further expand the application of TMS from studies of motor excitability to higher cognitive functions.

Keywords.

Transcranial magnetic stimulation Psychiatry Trait-marker State-marker Cortical excitability Neurophysiology 

Notes

Acknowledgements.

This research was supported in part by grants from the Cellular Science Research Foundation, Yoshida Science Foundation, and the Japan North America Medical Exchange Foundation to F.M., and the National Alliance for Research and Schizophrenia and Depression and the National Institutes of Mental Health (RO1MH57980) to A. P.-L.

References

  1. Abarbanel JM, Lemberg T, Yaroslavski U, Grisaru N, Belmaker RH (1996) Electrophysiological responses to transcranial magnetic stimulation in depression and schizophrenia. Biol Psychiatry 40:148–150PubMedGoogle Scholar
  2. Amassian VE, Quirk GJ, Stewart M (1990) A comparasion of corticospinal activation by magnetic coil and electrical stimulation of monkey motor cortex. Electroencephalogr Clin Neurophysiol 77:390–401PubMedGoogle Scholar
  3. Arana GW, Baldessarini RJ, Ornsteen M (1985) The dexamethasone suppression test for diagnosis and prognosis in psychiatry. Commentary and review. Arch Gen Psychiatry 42:1193–1204PubMedGoogle Scholar
  4. Austin MP, Ross M, Murray C, O'Carroll RE, Ebmeier KP, Goodwin GM (1992) Cognitive function in major depression. J Affect Disord 25:21–29PubMedGoogle Scholar
  5. Barker AT (1999) The history and basic principles of magnetic nerve stimulation. Electroencephalogr Clin Neurophysiol Suppl 51:3–21PubMedGoogle Scholar
  6. Barker AT, Freeston IL, Jalinous R, Merton PA, Morton HB (1985a) Magnetic stimulation of the human brain. J Physiol (Lond) 369:3PGoogle Scholar
  7. Barker AT, Jalinous R, Freeston IL (1985b) Non-invasive magnetic stimulation of the human motor cortex. Lancet I:1106–1107Google Scholar
  8. Bench CJ, Frackowiak RS, Dolan RJ (1995) Changes in regional cerebral blood flow on recovery from depression. Psychol Med 25:247–261PubMedGoogle Scholar
  9. Berardelli A, Rona S, Inghilleri M, Manfredi M (1996) Cortical inhibition in Parkinson's disease. A study with paired magnetic stimulation. Brain 119:71–77PubMedGoogle Scholar
  10. Berman RM, Narasimhan M, Sanacora G, Miano AP, Hoffman RE, Hu XS, Charney DS, Boutros NN (2000) A randomized clinical trial of repetitive transcranial magnetic stimulation in the treatment of major depression. Biol Psychiatry 47:332–337PubMedGoogle Scholar
  11. Blackwood DH, Whalley LJ, Christie JE, Blackburn IM, St Clair DM, McInnes A (1987) Changes in auditory P3 event-related potential in schizophrenia and depression. Br J Psychiatry 150:154–160PubMedGoogle Scholar
  12. Bohning DE, Shastri A, Nahas Z, Lorberbaum JP, Andersen SW, Dannels WR, Haxthausen EU, Vincent DJ, George MS (1998) Echoplanar BOLD fMRI of brain activation induced by concurrent transcranial magnetic stimulation. Invest Radiol 33:336–340CrossRefPubMedGoogle Scholar
  13. Bohning DE, Shastri A, McConnell KA, Nahas Z, Lorberbaum JP, Roberts DR, Teneback C, Vincent DJ, Boroojerdi B, Foltys H, Krings T, Spetzger U, Thron A, Topper R (1999) Localization of the motor hand area using transcranial magnetic stimulation and functional magnetic resonance imaging. Clin Neurophysiol 110:699–704PubMedGoogle Scholar
  14. Bohning DE, Shastri A, McGavin L, McConnell KA, Nahas Z, Lorberbaum JP, Roberts DR, George MS (2000a) Motor cortex brain activity induced by 1-Hz transcranial magnetic stimulation is similar in location and level to that for volitional movement. Invest Radiol 35:676–683CrossRefPubMedGoogle Scholar
  15. Bohning DE, Shastri A, Wassermann EM, Ziemann U, Lorberbaum JP, Nahas Z, Lomarev MP, George MS (2000b) BOLD-f MRI response to single-pulse transcranial magnetic stimulation (TMS). J Magn Reson Imaging 11:569–574CrossRefPubMedGoogle Scholar
  16. Boroojerdi B, Topper H, Foltys H, Meincke U (1999) Transcallosal inhibition and motor conduction studies in patients with schizophrenia using transcranial magnetic stimulation. Br J Psychiatry 175:375–379PubMedGoogle Scholar
  17. Boutros NN, Lisanby SH, Tokuno H, Torello MW, Campbell D, Berman R, Malison R, Krystal JH, Kosten T (2001) Elevated motor threshold in drug-free, cocaine-dependent patients assessed with transcranial magnetic stimulation. Biol Psychiatry 49:369–373PubMedGoogle Scholar
  18. Boylan LS, Sackeim HA (2000) Magnetoelectric brain stimulation in the assessment of brain physiology and pathophysiology. Clin Neurophysiol 111:504–512PubMedGoogle Scholar
  19. Brasil-Neto JP, Cohen LG, Panizza M, Nilsson J, Roth BJ, Hallett M (1992) Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J Clin Neurophysiol 9:132–136PubMedGoogle Scholar
  20. Brasil-Neto JP, Cohen LG, Hallett M (1994) Central fatigue as revealed by postexercise decrement of motor evoked potentials. Muscle Nerve 17:713–719PubMedGoogle Scholar
  21. Brasil-Neto JP, Cammarota A, Valls-Solé J, Pascual-Leone A, Hallett M, Cohen LG (1995) Role of intracortical mechanisms in the late part of the silent period to transcranial stimulation of the human motor cortex. Acta Neurol Scand 92:383–386PubMedGoogle Scholar
  22. Burke D, Hicks R, Gandevia SC, Stephen J, Woodforth I, Crawford M (1993) Direct comparison of corticospinal volleys in human subjects to transcranial magnetic and electrical stimulation. J Physiol (Lond) 470:383–393Google Scholar
  23. Catafau AM, Perez V, Gironell A, Martin JC, Kulisevsky J, Estorch M, Carrio I, Alvarez E (2001) SPECT mapping of cerebral activity changes induced by repetitive transcranial magnetic stimulation in depressed patients. A pilot study. Psychiatry Res 106:151–160PubMedGoogle Scholar
  24. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403PubMedGoogle Scholar
  25. Chen YL, Chen YH, Mak FL (2000) Soft neurological signs in schizophrenic patients and their nonpsychotic siblings. J Nerv Ment Dis 188:84–89CrossRefPubMedGoogle Scholar
  26. Chokroverty S, Picone MA, Chokroverty M (1991) Percutaneous magnetic stimulation of human cervical vertebral column: site of stimulation and clinical applicationperipheral nerves. Electroencephalogra Clin Neurophysiol 81:359–365Google Scholar
  27. Curtis CE, Calkins ME, Grove WM, Feil KJ, Iacono WG (2001) Saccadic disinhibition in patients with acute and remitted schizophrenia and their first-degree biological relatives. Am J Psychiatry 158:100–106PubMedGoogle Scholar
  28. Date M, Schmid UD, Hess CW, Schmid J (1991) Influence of peripheral nerve stimulation on the responses in small hand muscles to transcranial magnetic cortex stimulation. In: Levy WJ, Cracco RQ, Barker AT, Rothwell J (eds) Magnetic motor stimulation: basic principles and clinical experience. Elsevier, Amsterdam, pp 212–223Google Scholar
  29. Davey NJ, Puri BK (2000) Motor responses to transcranial magnetic stimulation in schizophrenia Br J Psychiatry 176:400CrossRefGoogle Scholar
  30. Davey NJ, Puri BK, Lewis HS, Lewis SW, Ellaway PH (1997) Effects of antipsychotic medication on electromyographic responses to transcranial magnetic stimulation of the motor cortex in schizophrenia. J Neurol Neurosurg Psychiatry 63:468–473PubMedGoogle Scholar
  31. Davidson RJ (1998) Cerebral asymmetry, affective style, and psychopathology. In: Kinsbourne M (ed) Cerebral hemisphere function in depression. American Psychiatric, Washington, pp 1–2Google Scholar
  32. Davidson RJ, Abercrombie H, Nitschke JB, Putnam K (1999) Regional brain function, emotion and disorders of emotion. Curr Opin Neurobiol 9:228–234PubMedGoogle Scholar
  33. Day BL, Dressler D, Maertens De Noordhout A, Marsden CD, Nakashima K, Rothwell JC, Thompson PD (1989) Electrical and magnetic stimulation of human motor cortex: surface EMG and single motor-unit responses. J Physiol (Lond) 412:449–473Google Scholar
  34. Detsch O, Kochs E (1997) Effects of ketamine on CNS-function. Anaesthesist 46:S20–S29PubMedGoogle Scholar
  35. Di Lazzaro V, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (1999a) Direct demonstration of interhemispheric inhibition of the human motor cortex produced by transcranial magnetic stimulation. Exp Brain Res 124:520–524PubMedGoogle Scholar
  36. Di Lazzaro V, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (1999b) Direct recordings of descending volleys after transcranial magnetic and electric motor cortex stimulation in conscious humans. Electroencephalogr Clin Neurophysiol Suppl 51:120–126PubMedGoogle Scholar
  37. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 73:2608–2611PubMedGoogle Scholar
  38. Fadiga L, Buccino G, Craighero L, Fogassi L, Gallese V, Pavesi G (1999) Corticospinal excitability is specifically modulated by motor imagery: a magnetic stimulation study. Neuropsychologia 37:147–158CrossRefPubMedGoogle Scholar
  39. Fox P, Ingham R, George MS, Mayberg H, Ingham J, Roby J, Martin C, Jerabek P (1997) Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport 8:2787–2791PubMedGoogle Scholar
  40. Freund S, Keenan JP, Tarsy D, Pascual-Leone A (1999) Intracortical disinhibition in tardive dystonia demonstrated by paired-pulse transcranial magnetic stimulation (TMS). Mov Disord 14:902Google Scholar
  41. Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81:257–262PubMedGoogle Scholar
  42. Fukushima J, Fukushima K, Morita N, Yamashita I (1990) Further analysis of the control of voluntary saccadic eye movements in schizophrenic patients. Biol Psychiatry 28:943–958PubMedGoogle Scholar
  43. George MS (1999) A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol Psychiatry 45:385–394PubMedGoogle Scholar
  44. George MS, Belmaker RH (2000) Transcranial magnetic stimulation in neuropsychiatry. APA, Washington DCGoogle Scholar
  45. George MS, Wassermann EM, Williams WA, Callahan A, Ketter TA, Basser P, Hallett M, Post RM (1995) Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression. Neuroreport 6:1853–1856PubMedGoogle Scholar
  46. George MS, Wassermann EM, Kimbrell TA, Little JT, Williams WE, Danielson AL, Greenberg BD, Hallett M, Post RM (1997) Mood improvement following daily left prefrontal repetitive transcranial magnetic stimulation in patients with depression: a placebo-controlled crossover trial. Am J Psychiatry 154:1752–1756PubMedGoogle Scholar
  47. George MS, Lisanby SH, Sackeim HA (1999) Transcranial magnetic stimulation: applications in neuropsychiatry. Arch Gen Psychiatry 56:300–311PubMedGoogle Scholar
  48. George MS, Nahas Z, Molloy M, Speer AM, Oliver NC, Li XB, Arana GW, Risch SC, Ballenger JC (2000) A controlled trial of daily left prefrontal cortex TMS for treating depression. Biol Psychiatry 48:962–970PubMedGoogle Scholar
  49. Goodwin GM, Austin MP, Dougall N, Ross M, Murray C, O'Carroll RE, Moffoot A, Prentice N, Ebmeier KP (1993) State changes in brain activity shown by the uptake of 99mTc-exametazime with single photon emission tomography in major depression before and after treatment. J Affect Disord 29:243–253PubMedGoogle Scholar
  50. Greenberg BD, Ziemann U, Cora-Locatelli G, Harmon A, Murphy DL, Keel JC, Wassermann EM (2000) Altered cortical excitability in obsessive-compulsive disorder. Neurology 54:142–147PubMedGoogle Scholar
  51. Grunhaus L, Dannon PN, Schreiber S, Dolberg OH, Amiaz R, Ziv R, Lefkifker E (2000) Repetitive transcranial magnetic stimulation is as effective as electroconvulsive therapy in the treatment of nondelusional major depressive disorder: an open study. Biol Psychiatry 47:314–324PubMedGoogle Scholar
  52. Gunther W, Streck P, Steinberg R, Gunther R, Raith L, Backmund M (1989) Psychomotor disturbances in psychiatric patients as a possible basis for new attempts at differential diagnosis and therapy. IV. Brain dysfunction during motor activation measured by EEG mapping. Eur Arch Psychiatry Neurol Sci 239:194–209PubMedGoogle Scholar
  53. Hadzi-Pavlovic D, Hickie I, Brodaty H, Boyce P, Mitchell P, Wilhelm K, Parker G (1993) Inter-rater reliability of a refined index of melancholia: the CORE system. J Affect Disord 27:155–162PubMedGoogle Scholar
  54. Hallett M (1995) Transcranial magnetic stimulation. Negative effects. Adv Neurol 67:107–113PubMedGoogle Scholar
  55. Hallett M, Fieldman J, Cohen LG, Sadato N, Pascual-Leone A (1994) Involvement of primary motor cortex in motor imagery and mental practice. Behav Brain Sci 17:210Google Scholar
  56. Hess CW, Mills KR, Murray NM (1986) Magnetic stimulation of the human brain: facilitation of motor responses by voluntary contraction of ipsilateral and contralateral muscles with additional observations on an amputee. Neurosci Lett 71:235–240PubMedGoogle Scholar
  57. Hodgkin AL, Huxley AF (1952a) Currents carried out by sodium and potassium ions through the membrace of the giant axon of Loligo. J Physiol (Lond) 116:449–472Google Scholar
  58. Hodgkin AL, Huxley AF (1952b) The components of membrane conductance in the giant axon of Loligo. J Physiol (Lond) 116:473–496Google Scholar
  59. Hodgkin AL, Huxley AF (1952c) A quantitative description of membrance current and its application to conduction and excitation in nerve. J Physiol (Lond) 116:500–544Google Scholar
  60. Hollge J, Kunkel M, Ziemann U, Tergau F, Geese R, Reimers CD (1997) Central fatigue in sports and daily exercises. A magnetic stimulation study. Int J Sports Med 18:614–617PubMedGoogle Scholar
  61. Ilmoniemi RJ, Virtanen J, Ruohonen J, Karhu J, Aronen HJ, Naatanen R, Katila T (1997) Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 8:3537–3540PubMedGoogle Scholar
  62. Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol (Lond) 466:521–534Google Scholar
  63. Inghilleri M, Berardelli A, Marchetti P, Manfredi M (1996) Effects of diazepam, baclofen and thiopental on the silent period evoked by transcranial magnetic stimulation in humans. Exp Brain Res 109:467–472PubMedGoogle Scholar
  64. Ismail B, Cantor-Graae E, McNeil TF (1998) Neurological abnormalities in schizophrenic patients and their siblings. Am J Psychiatry 155:84–89PubMedGoogle Scholar
  65. Izumi S, Takase M, Arita M, Masakado Y, Kimura A, Chino N (1997) Transcranial magnetic stimulation-induced changes in EEG and responses recorded from the scalp of healthy humans. Electroencephalogr Clin Neurophysiol 103:319–322PubMedGoogle Scholar
  66. Kahkonen S, Kesaniemi M, Nikouline VV, Karhu J, Ollikainen M, Holi M, Ilmoniemi RJ (2001) Ethanol modulates cortical activity: direct evidence with combined TMS and EEG. Neuroimage 14:322–328PubMedGoogle Scholar
  67. Kaneko K, Kawai S, Fuchigami Y, Morita H, Ofuji A (1996a) The effect of current direction induced by transcranial magnetic stimulation on the corticospinal excitability in human brain. Electroencephalogr Clin Neurophysiol 101:478–482PubMedGoogle Scholar
  68. Kaneko K, Kawai S, Fuchigami Y, Shiraishi G, Ito T (1996b) Effect of stimulus intensity and voluntary contraction on corticospinal potentials following transcranial magnetic stimulation. J Neurol Sci 139:131–136PubMedGoogle Scholar
  69. Kiers L, Cros D, Chiappa KH, Fang J (1993) Variability of motor potentials evoked by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 89:415–423PubMedGoogle Scholar
  70. Kimbrell TA, Little JT, Dunn RT, Frye MA, Greenberg BD, Wassermann EM, Repella JD, Danielson AL, Willis MW, Benson BE, Speer AM, Osuch E, George MS, Post RM (1999) Frequency dependence of antidepressant response to left prefrontal repetitive transcranial magnetic stimulation (rTMS) as a function of baseline cerebral glucose metabolism. Biol Psychiatry 46:1603–1613PubMedGoogle Scholar
  71. Klein E, Kreinin I, Chistyakov A, Koren D, Mecz L, Marmur S, Ben-Shachar D, Feinsod M (1999) Therapeutic efficacy of right prefrontal slow repetitive transcranial magnetic stimulation in major depression: a double-blind controlled study. Arch Gen Psychiatry 56:315–320PubMedGoogle Scholar
  72. Kozel FA, Nahas Z, deBrux C, Molloy M, Lorberbaum JP, Bohning D, Risch SC, George MS (2000) How coil-cortex distance relates to age, motor threshold, and antidepressant response to repetitive transcranial magnetic stimulation. J Neuropsychiatry Clin Neurosci 12:376–384PubMedGoogle Scholar
  73. Kubota F, Miyata H, Shibata N, Yarita H (1999) A study of motor dysfunction associated with schizophrenia based on analyses of movement-related cerebral potentials and motor conduction time. Biol Psychiatry 45:412–416PubMedGoogle Scholar
  74. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol (Lond) 471:501–519Google Scholar
  75. Landau WM (1952) Patterns of movement elicited in medullary pyramidal stimulation in the cat. Electroencephalogr Clin Neurophysiol 5:527–545CrossRefGoogle Scholar
  76. Liepert J, Tegenthoff M, Malin JP (1996) Changes of inhibitory interneurons during transcallosal stimulations. J Neural Transm 103:917–924PubMedGoogle Scholar
  77. Liepert J, Schwenkreis P, Tegenthoff M, Malin JP (1997) The glutamate antagonist riluzole suppresses intracortical facilitation. J Neural Transm 104:1207–1214PubMedGoogle Scholar
  78. Lisanby SH, Sackeim HA (2000) Transcranial magnetic stimulation in major depression. In: George MS, Belmaker RH (eds) Transcranial magnetic stimulation (TMS) in neuropsychiatry. American Psychiatric, Washington, pp 185–200Google Scholar
  79. Lohr JB, Caligiuri MP (1995) Motor asymmetry, a neurobiologic abnormality in the major psychoses. Psychiatry Res 57:279–282PubMedGoogle Scholar
  80. Maeda F, Keenan J, Tormos JM, Topka H, Pascual-Leone A (2000a) Interindividual variability of the modulatory effect of repetitive transcranial magnetic stimulation on cortico-spinal excitability. Exp Brain Res 133:425–430PubMedGoogle Scholar
  81. Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000b) Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 111:800–805PubMedGoogle Scholar
  82. Maeda F, Keenan J, Pascual-Leone A (2000c) Interhemispheric asymmetry of motor cortical excitability as measured by transcranial magnetic stimulation in major depression. Br J Psychiatry 177:169–173PubMedGoogle Scholar
  83. Maeda F, Keenan J, Freund S, Vaccaro B, Birnbaum R, Pascual-Leone A (2000d) Transcranial magnetic stimulation studies of cortical excitability in depression. Biol Psychiatry 46:169SGoogle Scholar
  84. Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000e) Interindividual variability of the modulatory effect of repetitive transcranial magnetic stimulation on cortico-spinal excitability. Exp Brain Res 133:425–430PubMedGoogle Scholar
  85. Maeda F, Topka H, Keenan JP, Pascual-Leone A (2000f) Effects of cerebellar output on intracortical motor cortex excitability studied by transcranial magnetic stimulation. Ann Neurol 48:475Google Scholar
  86. Maeda F, Kleiner-Fisman G, Pascual-Leone A (2002a) Motor facilitation while observing hand actions: specificity of the effect and role of observer' s orientation. J Neurophysiol 87:1329–1335PubMedGoogle Scholar
  87. Maeda F, Gangitano M, Thall M, Pascual-Leone A (2002b) Inter- and intra-individual variability of paired-pulse curves with transcranial magnetic stimulation (TMS). Clin Neurophysiol 113:376–382PubMedGoogle Scholar
  88. Manschreck TC, Keuthen NJ, Schneyer ML, Celada MT, Laughery J, Collins P (1990) Abnormal involuntary movements and chronic schizophrenic disorders. Biol Psychiatry 27:150–158PubMedGoogle Scholar
  89. Maruff P, Danckert J, Pantelis C, Currie J (1998) Saccadic and attentional abnormalities in patients with schizophrenia. Psychol Med 28:1091–1100Google Scholar
  90. Matsunaga K, Uozumi T, Tsuji S, Murai Y (1998) Age-dependent changes in physiological threshold asymmetries for the motor evoked potential and silent period following transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 109:502–507PubMedGoogle Scholar
  91. McConnell KA, Nahas Z, Shastri A, Lorberbaum JP, Kozel FA, Bohning DE, George MS (2001) The transcranial magnetic stimulation motor threshold depends on the distance from coil to underlying cortex: a replication in healthy adults comparing two methods of assessing the distance to cortex. Biol Psychiatry 49:454–459PubMedGoogle Scholar
  92. McDonnell RAL, Shapiro BE, Chiappa KH, Helmers SL, Cros D, Day BJ, Shahani BT (1991) Hemispherice threshold differences for motor evoked potentials produced by magnetic coil stimulation. Neurology 41:1441–1444PubMedGoogle Scholar
  93. McDowell JE, Clementz BA (2001) Behavioral and brain imaging studies of saccadic performance in schizophrenia. Biol Psychol 57:5–22PubMedGoogle Scholar
  94. Mills KR (1999) Magnetic stimulation of the human nervous system. Oxford University Press, OxfordGoogle Scholar
  95. Mills KR, Murray NMF (1986) Electrical stimulation over the human vertebral column: which elements are excited? Electroencephalogr Clin Neurophysiol 63:582–589Google Scholar
  96. Mills KR, Nithi KA (1997) Corticomotor threshold to magnetic stimulation: normal values and repeatability. Muscle Nerve 20:570–576Google Scholar
  97. Mills KR, Boniface SJ, Schubert M (1992) Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr Clin Neurophysiol 85:17–21PubMedGoogle Scholar
  98. Moffoot AP, O'Carroll RE, Bennie J, Carroll S, Dick H, Ebmeier KP, Goodwin GM (1994) Diurnal variation of mood and neuropsychological function in major depression with melancholia. J Affect Disord 32:257–269PubMedGoogle Scholar
  99. Mottaghy FM, Krause BJ, Kemna LJ, Topper R, Tellmann L, Beu M, Pascual-Leone A, Muller-Gartner HW (2000) Modulation of the neuronal circuitry subserving working memory in healthy human subjects by repetitive transcranial magnetic stimulation. Neurosci Lett 280:167–170PubMedGoogle Scholar
  100. Nakamura H, Kitagawa H, Kawaguchi Y, Tsuji H (1996) Direct and indirect activation of human corticospinal neurons by transcranial magnetic and electrical stimulation. Neurosci Lett 210:45–48PubMedGoogle Scholar
  101. Nikouline V, Ruohonen J, Ilmoniemi RJ (1999) The role of the coil click in TMS assessed with simultaneous EEG. Clin Neurophysiol 110:1325–1328PubMedGoogle Scholar
  102. Pascual-Leone A RB, Pallardo F, Catala MD (1996) Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. Lancet 348:233–237PubMedGoogle Scholar
  103. Pascual-Leone A, Tormos JM, Keenan J, Tarazona F, Cañete C, Catalá MD (1998) Study and modulation of human cortical excitability with transcranial magnetic stimulation. J Clin Neurophysiol 15:333–343PubMedGoogle Scholar
  104. Pascual-Leone A, Bartres-Faz D, Keenan JP (1999) Transcranial magnetic stimulation: studying the brain-behaviour relationship by induction of 'virtual lesions'. Philos Trans R Soc Lond B Biol Sci 354:1229–1238PubMedGoogle Scholar
  105. Pascual-Leone A, Manoach D, Birnbaum B, Goff D (2002) Motor excitability in schizophrenia. Biol Psychiatry 52:24–31CrossRefPubMedGoogle Scholar
  106. Pascual-Leone A, Walsh V, Rothwell J (2000) Transcranial magnetic stimulation in cognitive neuroscience – virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol 10:232–237PubMedGoogle Scholar
  107. Paus T, Wolforth M (1998) Transcranial magnetic stimulation during PET: reaching and verifying the target site. Hum Brain Mapp 6:399–402CrossRefPubMedGoogle Scholar
  108. Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans AC (1997) Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J Neurosci 17:3178–3184PubMedGoogle Scholar
  109. Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans AC (1998) Dose-dependent reduction of cerebral blood flow during rapid-rate transcranial magnetic stimulation of the human sensorimotor cortex. J Neurophysiol 79:1102–1107PubMedGoogle Scholar
  110. Pecuch PW, Evers S, Folkerts HW, Michael N, Arolt V (2000) The cerebral hemodynamics of repetitive transcranial magnetic stimulation. Eur Arch Psychiatry Clin Neurosci 250:320–324PubMedGoogle Scholar
  111. Peschina W, Conca A, Konig P, Fritzsche H, Beraus W (2001) Low frequency rTMS as an add-on antidepressive strategy: heterogeneous impact on 99m Tc-HMPAO and 18 F-FDG uptake as measured simultaneously with the double isotope SPECT technique. Pilot study. Nucl Med Commun 22:867–873CrossRefPubMedGoogle Scholar
  112. Post RM, Kimbrell TA, McCann UD, Dunn RT, Osuch EA, Speer AM, Weiss SR (1999) Repetitive transcranial magnetic stimulation as a neuropsychiatric tool: present status and future potential. J ECT 15:39–59PubMedGoogle Scholar
  113. Pridmore S (1999) Rapid transcranial magnetic stimulation and normalization of the dexamethasone suppression test. Psychiatry Clin Neurosci 53:33–37PubMedGoogle Scholar
  114. Pridmore S, Belmaker R (1999) Transcranial magnetic stimulation in the treatment of psychiatric disorders. Psychiatry Clin Neurosci 53:541–548CrossRefPubMedGoogle Scholar
  115. Pridmore S, Fernandes Filho JA, Nahas Z, Liberatos C, George MS (1998) Motor threshold in transcranial magnetic stimulation: a comparison of a neurophysiological method and a visualization of movement method. J ECT 14:25–27PubMedGoogle Scholar
  116. Priori A, Berardelli A, Inghilleri M, Accornero N, Manfredi M (1994) Motor cortical inhibition and the dopaminergic system. Pharmacological changes in the silent period after transcranial brain stimulation in normal subjects, patients with Parkinson's disease and drug-induced parkinsonism. Brain 117:317–323PubMedGoogle Scholar
  117. Priori A, Berardelli A, Mercuri B, Inghilleri M, Manfredi M (1995) The effect of hyperventilation on motor cortical inhibition in humans: a study of the electromyographic silent period evoked by transcranial brain stimulation. Electroencephalogr Clin Neurophysiol 97:69–72PubMedGoogle Scholar
  118. Priori A, Oliviero A, Donati E, Callea L, Bertolasi L, Rothwell JC (1999) Human handedness and asymmetry of the motor cortical silent period. Exp Brain Res 128:390–396CrossRefPubMedGoogle Scholar
  119. Puri BK, Davey NJ, Ellaway PH, Lewis SW (1996) An investigation of motor function in schizophrenia using transcranial magnetic stimulation of the motor cortex. Br J Psychiatry 169:690–695PubMedGoogle Scholar
  120. Reid PD, Pridmore S (1999) Dexamethasone suppression test reversal in rapid transcranial magnetic stimulation-treated depression. Aust N Z J Psychiatry 33:274–277CrossRefPubMedGoogle Scholar
  121. Ridding MC, Inzelberg R, Rothwell JC (1995) Changes in excitability of motor cortical circuitry in patients with Parkinson's disease. Ann Neurol 37:181–188PubMedGoogle Scholar
  122. Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD (2000) Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res 131:135–143CrossRefPubMedGoogle Scholar
  123. Rollnik JD, Schubert M, Dengler R (2000) Subthreshold prefrontal repetitive transcranial magnetic stimulation reduces motor cortex excitability. Muscle Nerve 23:112–114CrossRefPubMedGoogle Scholar
  124. Rosen AJ, Lockhart JJ, Gants ES, Westergaard CK (1991) Maintenance of grip-induced muscle tension: a behavioral marker of schizophrenia. J Abnorm Psychol 100:583–593PubMedGoogle Scholar
  125. Ross RG, Harris JG, Olincy A, Radant A, Adler LE, Freedman R (1998) Familial transmission of two independent saccadic abnormalities in schizophrenia. Schizophr Res 30:59–70PubMedGoogle Scholar
  126. Rossini PM, Rossi S (1998) Clinical applications of motor evoked potentials. Electroencephalogr Clin Neurophysiol 106:180–194PubMedGoogle Scholar
  127. Rossini PM, Caramia M, Zarola F (1987) Central motor tract propagation in man: studies with non-invasive, unifocal, scalp stimulation. Brain Res 415:211–225PubMedGoogle Scholar
  128. Rossini PM, Barker AT, Beradelli A, Caramia MR, Caruso G, Cracco RQ, Dimitrijevic MR, Katayama Y, Lucking CH, Maertens de Noordhout AL, Marsden CD, Murray NMF, Rothwell JC, Swash M, Tomberg C (1994) Electroencephalogr Clin Neurophysiol 91:79–92PubMedGoogle Scholar
  129. Rossini PM, Caramia MD, Iani C, Desiato MT, Sciarretta G, Bernardi G (1995) Magnetic transcranial stimulation in healthy humans: influence on the behavior of upper limb motor units. Brain Res 676:314–324PubMedGoogle Scholar
  130. Sakai K, Ugawa Y, Terao Y, Hanajima R, Furubayashi T, Kanazawa I (1997) Preferential activation of different I waves by transcranial magnetic stimulation with a figure-of-eight-shaped coil. Exp Brain Res 113:24–32PubMedGoogle Scholar
  131. Samii A, Wassermann EM, Ikoma K, Mercuri B, George MS, O'Fallon A, Dale JK, Straus SE, Hallett M (1996) Decreased postexercise facilitation of motor evoked potentials in patients with chronic fatigue syndrome or depression. Neurology 47:1410–1414PubMedGoogle Scholar
  132. Sander D, Meyer BU, Roricht S, Klingelhofer J (1995) Effect of hemisphere-selective repetitive magnetic brain stimulation on middle cerebral artery blood flow velocity. Electroencephalogr Clin Neurophysiol 97:43–48PubMedGoogle Scholar
  133. Sander D, Meyer BU, Roricht S, Matzander G, Klingelhofer J (1996) Increase of posterior cerebral artery blood flow velocity during threshold repetitive magnetic stimulation of the human visual cortex: hints for neuronal activation without cortical phosphenes. Electroencephalogr Clin Neurophysiol 99:473–478PubMedGoogle Scholar
  134. Schnitzler A, Kessler KR, Benecke R (1996) Transcallosally mediated inhibition of interneurons within human primary motor cortex. Exp Brain Res 112:381–391PubMedGoogle Scholar
  135. Schonle PW, Isenberg C, Crozier TA, Dressler D, Machetanz J, Conrad B (1989) Changes of transcranially evoked motor responses in man by midazolam, a short acting benzodiazepine. Neurosci Lett 101:321–324PubMedGoogle Scholar
  136. Schurmann M, Nikouline VV, Soljanlahti S, Ollikainen M, Basar E, Ilmoniemi RJ (2001) EEG responses to combined somatosensory and transcranial magnetic stimulation. Clin Neurophysiol 112:19–24PubMedGoogle Scholar
  137. Schutter DJLG, van Honk J, d'Alfonso AAL, Postma A, de Haan EHF (2001) Effects of slow rTMS at the right dorsolateral prefrontal cortex on EEG asymmetry and mood. Neuroreport 12:445–447PubMedGoogle Scholar
  138. Shajahan PM, Glabus MF, Gooding PA, Shah PJ, Ebmeier KP (1999a) Reduced cortical excitability in depression. Impaired post-exercise motor facilitation with transcranial magnetic stimulation. Br J Psychiatry 174:449–454PubMedGoogle Scholar
  139. Shajahan PM, Glabus MF, Jenkins JA, Ebmeier KP (1999b) Postexercise motor evoked potentials in depressed patients, recovered depressed patients, and controls. Neurology 53:644–646PubMedGoogle Scholar
  140. Shibasaki H, Barrett G, Halliday E, Halliday AM (1980) Components of the movement-related cortical potential and their scalp topography. Electroencephalogr Clin Neurophysiol 49:213–226PubMedGoogle Scholar
  141. Siebner HR, Willoch F, Peller M, Auer C, Boecker H, Conrad B, Bartenstein P (1998) Imaging brain activation induced by long trains of repetitive transcranial magnetic stimulation. Neuroreport 9:943–948PubMedGoogle Scholar
  142. Siebner HR, Peller M, Willoch F, Auer C, Bartenstein P, Drzezga A, Schwaiger M, Conrad B (1999) Imaging functional activation of the auditory cortex during focal repetitive transcranial magnetic stimulation of the primary motor cortex in normal subjects. Neurosci Lett 270:37–40PubMedGoogle Scholar
  143. Siebner H, Peller M, Bartenstein P, Willoch F, Rossmeier C, Schwaiger M, Conrad B (2001) Activation of frontal premotor areas during suprathreshold transcranial magnetic stimulation of the left primary sensorimotor cortex: a glucose metabolic PET study. Hum Brain Mapp 12:157–167PubMedGoogle Scholar
  144. Smith MJ, Keel JC, Greenberg BD, Adams LF, Schmidt PJ, Rubinow DA, Wassermann EM (1999) Menstrual cycle effects on cortical excitability. Neurology 53:2069–2072PubMedGoogle Scholar
  145. Sobin C, Sackeim HA (1997) Psychomotor symptoms of depression. Am J Psychiatry 154:4–17PubMedGoogle Scholar
  146. Stallings LE, Speer AM, Spicer KM, Cheng KT, George MS (1997) Combining SPECT and repetitive transcranial magnetic stimulation (rTMS)-left prefrontal stimulation decreases relative perfusion locally in a dose dependant manner. Neuroimage 5:S521Google Scholar
  147. Steele JD, Glabus MF, Shajahan PM, Ebmeier KP (2000) Increased cortical inhibition in depression: a prolonged silent period with transcranial magnetic stimulation (TMS). Psychol Med 30:565–570PubMedGoogle Scholar
  148. Strafella AP, Paus T (2000) Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. Neuroreport 11:2289–2292PubMedGoogle Scholar
  149. Strafella AP, Paus T (2001) Cerebral blood-flow changes induced by paired-pulse transcranial magnetic stimulation of the primary motor cortex. J Neurophysiol 85:2624–2629PubMedGoogle Scholar
  150. Strafella AP, Paus T, Barrett J, Dagher A (2001) Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci 21:RC157PubMedGoogle Scholar
  151. Teneback CC, Nahas Z, Speer AM, Molloy M, Stallings LE, Spicer KM, Risch SC, George MS (1999) Changes in prefrontal cortex and paralimbic activity in depression following two weeks of daily left prefrontal TMS. J Neuropsychiatry Clin Neurosci 11:426–435PubMedGoogle Scholar
  152. Terao Y, Ugawa Y, Sakai K, Miyauchi S, Fukuda H, Sasaki Y, Takino R, Hanajima R, Furubayashi T, Putz B, Kanazawa I (1998) Localizing the site of magnetic brain stimulation by functional MRI. Exp Brain Res 121:145–152PubMedGoogle Scholar
  153. Tergau F, Wanschura V, Canelo M, Wischer S, Wassermann EM, Ziemann U, Paulus W (1999) Complete suppression of voluntary motor drive during the silent period after transcranial magnetic stimulation. Exp Brain Res 124:447–454CrossRefPubMedGoogle Scholar
  154. Tiitinen H, Virtanen J, Ilmoniemi RJ, Kamppuri J, Ollikainen M, Ruohonen J, Naatanen R (1999) Separation of contamination caused by coil clicks from responses elicited by transcranial magnetic stimulation. Clin Neurophysiol 110:982–985PubMedGoogle Scholar
  155. Tormos JM, Catala MD, Juan C, Pascual-Leone Pascual A, Keenan JP, Pascual-Leone A (1998) Effects of repetitive transcranial magnetic stimulation on EEG. Neurology 50:A317–318Google Scholar
  156. Triggs WJ, Subramanium B, Rossi F (1999a) Hand preference and transcranial magnetic stimulation asymmetry of cortical motor representation. Brain Res 835:324–329PubMedGoogle Scholar
  157. Triggs WJ, McCoy KJ, Greer R, Rossi F, Bowers D, Kortenkamp S, Nadeau SE, Heilman KM, Goodman WK (1999b) Effects of left frontal transcranial magnetic stimulation on depressed mood, cognition, and corticomotor threshold. Biol Psychiatry 45:1440–1446PubMedGoogle Scholar
  158. Ucles P, Serrano JL, Rosa F (2000) Central conduction time of magnetic brain stimulation in attention-deficit hyperactivity disorder. J Child Neurol 15:723–728PubMedGoogle Scholar
  159. Ugawa Y (1999) Magnetic cerebellar stimulation. Electroencephalogr Clin Neurophysiol Suppl 49:222–225PubMedGoogle Scholar
  160. Valls-Solé J, Pascual-Leone A, Wassermann EM, Hallett M (1992) Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol 85:355–364PubMedGoogle Scholar
  161. Virtanen J, Ruohonen J, Naatanen R, Ilmoniemi RJ (1999) Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Med Biol Eng Comput 37:322–326Google Scholar
  162. Walker EF (1994) Developmentally moderated expressions of the neuropathology underlying schizophrenia. Schizophr Bull 20:453–480Google Scholar
  163. Walsh V, Rushworth M (1999) A primer of magnetic stimulation as a tool for neuropsychology. Neuropsychologia 37:125–135PubMedGoogle Scholar
  164. Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7:1996. Electroencephalogr Clin Neurophysiol 108:1–16PubMedGoogle Scholar
  165. Wassermann EM, McShane LM, Hallett M, Cohen LG (1992) Noninvasive mapping of muscle representations in human motor cortex. Electroencephalogr Clin Neurophysiol 85:1–8PubMedGoogle Scholar
  166. Wassermann EM, Pascual-Leone A, Valls-Solé J, Toro C, Cohen LG, Hallett M (1993) Topography of the inhibitory and excitatory responses to transcranial magnetic stimulation in a hand muscle. Electroencephalogr Clin Neurophysiol 89:424–433PubMedGoogle Scholar
  167. Wassermann EM, Samii A, Mercuri B, Ikoma K, Oddo D, Grill SE, Hallett M (1996) Responses to paired transcranial magnetic stimuli in resting, active, and recently activated muscles. Exp Brain Res 109:158–163PubMedGoogle Scholar
  168. Wassermann EM, Tormos JM, Pascual-Leone A (1998) Finger movements induced by transcranial magnetic stimulation change with hand posture, but not with coil position. Hum Brain Mapp 6:390–393CrossRefPubMedGoogle Scholar
  169. Werhahn KJ, Fong JK, Meyer BU, Priori A, Rothwell JC, Day BL, Thompson PD (1994) The effect of magnetic coil orientation on the latency of surface EMG and single motor unit responses in the first dorsal interosseous muscle. Electroencephalogr Clin Neurophysiol 93:138–146PubMedGoogle Scholar
  170. Werhahn KJ, Forderreuther S, Straube A (1998) Effects of the serotonin1B/1D receptor agonist zolmitriptan on motor cortical excitability in humans. Neurology 51:896–898PubMedGoogle Scholar
  171. Wheeler RE, Davidson RJ, Tomarken AJ (1993) Frontal brain asymmetry and emotional reactivity: a biological substrate of affective style. Psychophysiology 30:82–89PubMedGoogle Scholar
  172. Zheng XM (2000) Regional cerebral blood flow changes in drug-resistant depressed patients following treatment with transcranial magnetic stimulation: a statistical parametric mapping analysis. Psychiatry Res 100:75–80PubMedGoogle Scholar
  173. Ziemann U (1999) Intracortical inhibition and facilitation in the conventional paired TMS paradigm. Electroencephalogr Clin Neurophysiol Suppl 51:127–136PubMedGoogle Scholar
  174. Ziemann U, Netz J, Szelenyi A, Homberg V (1993) Spinal and supraspinal mechanisms contribute to the silent period in the contracting soleus muscle after transcranial magnetic stimulation of human motor cortex. Neurosci Lett 156:167–171PubMedGoogle Scholar
  175. Ziemann U, Bruns D, Paulus W (1996a) Enhancement of human motor cortex inhibition by the dopamine receptor agonist pergolide: evidence from transcranial magnetic stimulation. Neurosci Lett 208:187–190PubMedGoogle Scholar
  176. Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996b) Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:367–378PubMedGoogle Scholar
  177. Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996c) The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 109:127–135PubMedGoogle Scholar
  178. Ziemann U, Rothwell JC, Ridding MC (1996d) Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol (Lond) 496:873–881Google Scholar
  179. Ziemann U, Paulus W, Rothenberger A (1997) Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. Am J Psychiatry 154:1277–1284PubMedGoogle Scholar
  180. Ziemann U, Steinhoff BJ, Tergau F, Paulus W (1998) Transcranial magnetic stimulation: its current role in epilepsy research. Epilepsy Res 30:11–30PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of Psychology, Stanford University, Stanford, Calif., USA
  2. 2.Laboratory for Magnetic Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, 330 Brookline Ave. KS452, Boston, MA 02215, USA
  3. 3.Institute for Bioengineering, Miguel Hernandez University, Alicante, Spain

Personalised recommendations