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Nervenheilkunde 2003; 22(04): 182-188
DOI: 10.1055/s-0038-1624396
Original- und Übersichtsarbeiten/Original and Review Articles
Schattauer GmbH

Kortikale Exzitabilität – Messung und Modulation

Cortical excitability – measurement and modulation
C. Plewnia
1   Institut für medizinische Psychologie und Verhaltensneurobiologie Tübingen (Direktor: Prof. Niels Birbaumer)
2   Labor für kortikale Physiologie, Neurologische Klinik Tübingen(Leiter: Priv.-Doz. Dr. C. Gerloff)
,
G. W. Eschweiler
3   Universitätsklinik für Psychiatrie und Psychotherapie Tübingen (Direktor: Prof. Gerhard Buchkremer)
› Author Affiliations
Further Information

Publication History

Publication Date:
15 January 2018 (online)

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Zusammenfassung

Mit der transkraniellen Magnetstimulation (TMS) steht eine nichtinvasive Methode zur Verfügung, die kortikale Erregbarkeit sowohl zu messen als auch zu modulieren. Damit stellt diese Technik ein besonders attraktives Forschungsinstrument der biologischen Psychiatrie dar und bietet darüber hinaus möglicherweise neue Therapieoptionen für unterschiedliche zentralnervöse Störungen. Nach einer kurzen Übersicht über die üblicherweise verwendeten Messmethoden der durch die TMS fassbaren Parameter kortikaler Exzitabilität wird der bisherige Kenntnisstand zur physiologischen bzw. pathophysiologischen Bedeutung der Parameter beschrieben. Nachfolgend werden die Möglichkeiten der Modulation kortikaler Erregbarkeit dargestellt. Abschließend werden offene Fragen und Perspektiven der neuropsychiatrischen Forschung mit TMS diskutiert.

Summary

Transcranial magnetic stimulation (TMS) offers a noninvasive tool for the assessment and modulation of cortical excitability. These characteristics qualify this technique as an interesting method for neuropsychiatric research and may yield new therapeutic strategies for various disorders of the central nervous system. After a short summary of the common methods of cortical excitation measurement and modulation including single pulse TMS, double pulse TMS, slow and rapid-rate TMS, the current literature regarding the physiological and pathophysiological role of cortical excitability is described. Finally we discuss open questions and perspectives of measurement and modulation of cortical excitability for neuropsychiatric research with TMS.

Schlüsselwörter

Transkranielle Magnetstimulation (TMS) - kortikale Erregbarkeit - Doppelpuls-TMS - repetitive TMS (rTMS) - Psychopharmakologie

Keywords

Transcranial magnetic stimulation (TMS) - cortical excitability - double pulse TMS - repetitive transcranial magnetic stimulation - psychopharmacology
 

  • Literatur

  • 1 Berardelli A. Transcranial magnetic stimulation in movement disorders. Electroencephalogr Clin Neurophysiol Suppl 1999; 51: 276-80.
    PubMedSearch in Google Scholar
  • 2 Boroojerdi B, Battaglia F, Muellbacher W, Cohen LG. Mechanisms influencing stimulusresponse properties of the human corticospinal system. Clin Neurophysiol 2001; 112: 931-7.
    CrossrefPubMedSearch in Google Scholar
  • 3 Boroojerdi B, Meister IG, Foltys H, Sparing R, Cohen LG, Topper R. Visual and motor cortex excitability: a transcranial magnetic stimulation study. Clin Neurophysiol 2002; 113: 1501-4.
    CrossrefPubMedSearch in Google Scholar
  • 4 Boroojerdi B, Prager A, Muellbacher W, Cohen LG. Reduction of human visual cortex excitability using 1-Hz transcranial magnetic stimulation. Neurology 2000; 54: 1529-31.
    CrossrefPubMedSearch in Google Scholar
  • 5 Butefisch CM, Davis BC, Sawaki L, Waldvogel D, Classen J, Kopylev L. et al. Modulation of use-dependent plasticity by d-amphetamine. Ann Neurol 2002; 51: 59-68.
    CrossrefPubMedSearch in Google Scholar
  • 6 Butefisch CM, Davis BC, Wise SP, Sawaki L, Kopylev L, Classen J. et al. Mechanisms of use-dependent plasticity in the human motor cortex. Proc Natl Acad Sci USA 2000; 97: 3661-5.
    CrossrefPubMedSearch in Google Scholar
  • 7 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 1997a 48: 1398-403.
  • 8 Chen R, Wassermann EM, Canos M, Hallett M. Impaired inhibition in writer’s cramp during voluntary muscle activation. Neurology 1997b 49: 1054-9.
  • 9 Chen R, Samii A, Canos M, Wassermann EM, Hallett M. Effects of phenytoin on cortical excitability in humans. Neurology 1997c 49: 881-3.
  • 10 Devanne H, Lavoie BA, Capaday C. Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 1997; 114: 329-38.
    CrossrefPubMedSearch in Google Scholar
  • 11 Di Lazzaro V, Oliviero A, Proficie P, Pennisi MA, Di Giovanni S, Zito G, Tonali P, Rothwell JC. Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex. Exp Brain Res 2000; 135: 455-61.
    CrossrefPubMedSearch in Google Scholar
  • 12 Enomoto H, Ugawa Y, Hanajima R, Yuasa K, Mochizuki H, Terao Y. et al. Decreased sensory cortical excitability after 1 Hz rTMS over the ipsilateral primary motor cortex. Clin Neurophysiol 2001; 112: 2154-8.
    CrossrefPubMedSearch in Google Scholar
  • 13 Feeney DM, Weisend MP, Kline AE. Noradrenergic pharmacotherapy, intracerebral infusion and adrenal transplantation promote functional recovery after cortical damage. J Neural Transplant Plast 1993; 04: 199-213.
    CrossrefPubMedSearch in Google Scholar
  • 14 Fisher RJ, Nakamura Y, Bestmann S, Rothwell JC, Bostock H. Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking. Exp Brain Res 2002; 143: 240-8.
    CrossrefPubMedSearch in Google Scholar
  • 15 Froc DJ, Chapman CA, Trepel C, Racine RJ. Long-term depression and depotentiation in the sensorimotor cortex of the freely moving rat. J Neurosci 2000; 20: 438-45.
    CrossrefPubMedSearch in Google Scholar
  • 16 Gangitano M, Valero-Cabre A, Tormos JM, Mottaghy FM, Romero JR, Pascual-Leone A. Modulation of input-output curves by low and high frequency repetitive transcranial magnetic stimulation of the motor cortex. Clin Neurophysiol 2002; 113: 1249-57.
    CrossrefPubMedSearch in Google Scholar
  • 17 Gerschlager W, Siebner HR, Rothwell JC. Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology 2001; 57: 449-55.
    CrossrefPubMedSearch in Google Scholar
  • 18 Goldstein LB. Effects of amphetamines and small related molecules on recovery after stroke in animals and man. Neuropharmacology 2000; 39: 852-9.
    CrossrefPubMedSearch in Google Scholar
  • 19 Greenberg BD, Ziemann U, Cora-Locatelli G, Harmon A, Murphy DL, Keel JC. et al. Altered cortical excitability in obsessive-compulsive disorder. Neurology 2000; 54: 142-7.
    CrossrefPubMedSearch in Google Scholar
  • 20 Herwig U, Brauer K, Connemann B, Spitzer M, Schonfeldt-Lecuona C. Intracortical excitability is modulated by a norepinephrine-reuptake inhibitor as measured with paired-pulse transcranial magnetic stimulation. Psychopharmacology (Berl) 2002; 164: 228-32.
    CrossrefPubMedSearch in Google Scholar
  • 21 Herwig U, Schonfeldt-Lecuona C, Wunderlich AP, von Tiesenhausen C, Thielscher A, Walter H. et al. The navigation of transcranial magnetic stimulation. Psychiatry Res 2001; 108: 123-31.
    CrossrefPubMedSearch in Google Scholar
  • 22 Heynen AJ, Abraham WC, Bear MF. Bidirectional modification of CA1 synapses in the adult hippocampus in vivo. Nature 1996; 381: 163-6.
    CrossrefPubMedSearch in Google Scholar
  • 23 Hoffman RE, Cavus I. Slow transcranial magnetic stimulation, long-term depotentiation, and brain hyperexcitability disorders. Am J Psychiatry 2002; 159: 1093-102.
    CrossrefPubMedSearch in Google Scholar
  • 24 Hoffman RE, Hawkins KA, Gueorguieva R, Boutros NN, Rachid F, Carroll K. et al. Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. Arch Gen Psychiatry 2003; 60: 49-56.
    CrossrefPubMedSearch in Google Scholar
  • 25 Ilic TV, Korchounov A, Ziemann U. Complex modulation of human motor cortex excitability by the specific serotonin re-uptake inhibitor sertraline. Neurosci Lett 2002; 319: 116-20.
    CrossrefPubMedSearch in Google Scholar
  • 26 Kammer T. Phosphenes and transient scotomas induced by magnetic stimulation of the occipital lobe: their topographic relationship. Neuropsychologia 1999; 37: 191-8.
    PubMedSearch in Google Scholar
  • 27 Kammer T, Beck S, Thielscher A, Laubis-Herrmann U, Topka H. Motor thresholds in humans: a transcranial magnetic stimulation study comparing different pulse waveforms, current directions and stimulator types. Clin Neurophysiol 2001; 112: 250-8.
    CrossrefPubMedSearch in Google Scholar
  • 28 Karl A, Birbaumer N, Lutzenberger W, Cohen LG, Flor H. Reorganization of motor and somatosensory cortex in upper extremity amputees with phantom limb pain. J Neurosci 2001; 21: 3609-18.
    CrossrefPubMedSearch in Google Scholar
  • 29 Kessler KR, Schnitzler A, Classen J, Benecke R. Reduced inhibition within primary motor cortex in patients with poststroke focal motor seizures. Neurology 2002; 59: 1028-33.
    CrossrefPubMedSearch in Google Scholar
  • 30 Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A. et al. Corticocortical inhibition in human motor cortex. J Physiol 1993; 471: 501-19.
    CrossrefPubMedSearch in Google Scholar
  • 31 Liebetanz D, Nitsche MA, Tergau F, Paulus W. Pharmacological approach to the mechanisms of transcranial DCstimulation-induced aftereffects of human motor cortex excitability. Brain 2002; 125: 2238-47.
    CrossrefPubMedSearch in Google Scholar
  • 32 Liepert J, Schwenkreis P, Tegenthoff M, Malin JP. The glutamate antagonist riluzole suppresses intracortical facilitation. J Neural Transm 1997; 104: 1207-14.
    CrossrefPubMedSearch in Google Scholar
  • 33 Liepert J, Schardt S, Weiller C. Orally administered atropine enhances motor cortex excitability: a transcranial magnetic stimulation study in human subjects. Neurosci Lett 2001; 300: 149-52.
    CrossrefPubMedSearch in Google Scholar
  • 34 Linden DJ. Long-term synaptic depression in the mammalian brain. Neuron 1994; 12: 457-72.
    CrossrefPubMedSearch in Google Scholar
  • 35 Lippold OC, Redfearn JW. Mental changes resulting from the passage of small direct currents throug the human brain. Br J Psychiatry 1964; 110: 768-72.
    CrossrefPubMedSearch in Google Scholar
  • 36 Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A. Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 2000; 133: 425-30.
    CrossrefPubMedSearch in Google Scholar
  • 37 Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 2000; 111: 800-5.
    CrossrefPubMedSearch in Google Scholar
  • 38 Manahan-Vaughan D, Braunewell KH. Novelty acquisition is associated with induction of hippocampal longterm depression. Proc Natl Acad Sci USA 1999; 96: 8739-44.
    CrossrefPubMedSearch in Google Scholar
  • 39 Manganotti P, Bortolomasi M, Zanette G, Pawelzik T, Giacopuzzi M, Fiaschi A. Intravenous clomipramine decreases excitability of human motor cortex. A study with paired magnetic stimulation. Neurol Sci 2001; 184: 27-32.
    CrossrefPubMedSearch in Google Scholar
  • 40 Manganotti P, Patuzzo S, Cortese F, Palermo A, Smania N, Fiaschi A. Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke. Clin Neurophysiol 2002; 113: 936-43.
    CrossrefPubMedSearch in Google Scholar
  • 41 Modugno N, Nakamura Y, MacKinnon CD, Filipovic SR, Bestmann S, Berardelli A. et al. Motor cortex excitability following short trains of repetitive magnetic stimuli. Exp Brain Res 2001; 140: 453-9.
    CrossrefPubMedSearch in Google Scholar
  • 42 Moll GH, Heinrich H, Trott GE, Wirth S, Bock N, Rothenberger A. Children with comorbid attention-deficit-hyperactivity disorder and tic disorder: evidence for additive inhibitory deficits within the motor system. Ann Neurol 2001; 49: 393-6.
    CrossrefPubMedSearch in Google Scholar
  • 43 Muellbacher W, Ziemann U, Boroojerdi B, Hallett M. Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior. Clin Neurophysiol 2000; 111: 1002-7.
    CrossrefPubMedSearch in Google Scholar
  • 44 Nakamura H, Kitagawa H, Kawaguchi Y, Tsuji H. Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J Physiol 1997; 498: 817-23.
    CrossrefPubMedSearch in Google Scholar
  • 45 Nitsche MA, Liebetanz D, Tergau F, Paulus W. Modulation kortikaler Erregbarkeit beim Menschen durch transkranielle Gleichstromstimulation. Nervenarzt 2002; 73: 332-5.
    CrossrefPubMedSearch in Google Scholar
  • 46 Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 2000; 527 Pt 3: 633-9.
    CrossrefPubMedSearch in Google Scholar
  • 47 Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 2001; 57: 1899-901.
    CrossrefPubMedSearch in Google Scholar
  • 48 Nudo RJ, Plautz EJ, Frost SB. Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle Nerve 2001; 24: 1000-19.
    CrossrefPubMedSearch in Google Scholar
  • 49 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: 847-58.
    CrossrefPubMedSearch in Google Scholar
  • 50 Plewnia C. Durchführung der Transkraniellen Magnetstimulation. In: Elekromagnetische Therapien in der Psychiatrie. Eschweiler GW, Wild B, Bartels M. (eds). Darmstadt: Steinkopff, 2003: 151-9.
    Search in Google Scholar
  • 51 Plewnia C. Transkranielle Magnetstimulation in der neuropsychiatrischen Forschung. In: Elektromagnetische Therapien in der Psychiatrie. Eschweiler GW, Wild B, Bartels M. (eds). Darmstadt: Steinkopff 2003: 160-78.
    Search in Google Scholar
  • 52 Plewnia C, Bartels M, Cohen L, Gerloff C. Noradrenergic modulation of human cortex excitability by the presynaptic alpha(2)-antagonist yohimbine. Neurosci Lett 2001; 307: 41-4.
    CrossrefPubMedSearch in Google Scholar
  • 53 Plewnia C, Hoppe J, Hiemke C, Bartels M, Cohen LG, Gerloff C. Enhancement of human cortico-motoneuronal excitability by the selective norepinephrine reuptake inhibitor reboxetine. Neurosci Lett 2002; 330: 231-4.
    CrossrefPubMedSearch in Google Scholar
  • 54 Plewnia C, Hoppe J, Godde B, Cohen LG, Gerloff C. Noradrenergic enhancement of gross but not fine motor skill training. Society for Neuroscience Abstracts. 32. 662.7. 2002
    PubMedSearch in Google Scholar
  • 55 Plewnia C, Bartels M, Gerloff C. Transient suppression of tinnitus by transcranial magnetic stimulation. Ann Neurol 2003; 53: 263-6.
    CrossrefPubMedSearch in Google Scholar
  • 56 Plewnia C, Lotze M, Gerloff C. Disinhibition of the contralateral motor cortex by low-frequency rTMS. Neuroreport. In press.
  • 57 Reis J, Tergau F, Hamer HM, Muller HH, Knake S, Fritsch B, Oertel WH, Rosenow F. Topiramate selectively decreases intracortical excitability in human motor cortex. Epilepsia 2002; 43: 1149-56.
    CrossrefPubMedSearch in Google Scholar
  • 58 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: 229-32.
    CrossrefPubMedSearch in Google Scholar
  • 59 Sailer A, Molnar GF, Cunic DI, Chen R. Effects of peripheral sensory input on cortical inhibition in humans. J Physiol 2002; 544: 617-29.
    CrossrefPubMedSearch in Google Scholar
  • 60 Schambra HM, Sawaki L, Cohen LG. Modulation of excitability of human motor cortex (M1) by 1 Hz transcranial magnetic stimulation of the contralateral M1. Clin Neurophysiol 2003; 114: 130-3.
    CrossrefPubMedSearch in Google Scholar
  • 61 Schwenkreis P, Witscher K, Janssen F, Addo A, Dertwinkel R, Zenz M, Malin JP, Tegenthoff M. Influence of the N-methyl-D-aspartate antagonist memantine on human motor cortex excitability. Neurosci Lett 1999; 270: 137-40.
    CrossrefPubMedSearch in Google Scholar
  • 62 Shimizu T, Hosaki A, Hino T, Sato M, Komori T, Hirai S. et al. Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain 2002; 125: 1896-907.
    CrossrefPubMedSearch in Google Scholar
  • 63 Siebner HR, Tormos JM, Ceballos-Baumann AO, Auer C, Catala MD, Conrad B. et al. Lowfrequency repetitive transcranial magnetic stimulation of the motor cortex in writer’s cramp. Neurology 1999; 52: 529-37.
    CrossrefPubMedSearch in Google Scholar
  • 64 Sohn YH, Kaelin-Lang A, Yung HY, Hallett M. Effect of levetiracetam on human corticospinal excitability. Neurology 2001; 57: 858-63.
    CrossrefPubMedSearch in Google Scholar
  • 65 Tergau F, Naumann U, Paulus W, Steinhoff BJ. Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet 1999; 353: 2209.
    CrossrefPubMedSearch in Google Scholar
  • 66 Touge T, Ichihara N, Ishibashi T, Ikeguchi M, Sasaki I, Takeuchi H. Afferent and efferent excitabilities of the transcortical loop in patients with dentatorubral-pallidoluysian atrophy. J Neurol Sci 2000; 176: 28-36.
    CrossrefPubMedSearch in Google Scholar
  • 67 Walker-Batson D, Smith P, Curtis S, Unwin H, Greenlee R. Amphetamine paired with physical therapy accelerates motor recovery after stroke. Further evidence. Stroke 1995; 26: 2254-9.
    CrossrefPubMedSearch in Google Scholar
  • 68 Wassermann EM. 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 1998; 108: 1-16.
    CrossrefPubMedSearch in Google Scholar
  • 69 Werhahn KJ, Forderreuther S, Straube A. Effects of the serotonin1B/1D receptor agonist zolmitriptan on motor cortical excitability in humans. Neurology 1998; 51: 896-8.
    CrossrefPubMedSearch in Google Scholar
  • 70 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: 591-7.
    CrossrefPubMedSearch in Google Scholar
  • 71 Werhahn KJ, Mortensen J, Kaelin-Lang A, Boroojerdi B, Cohen LG. Cortical excitability changes induced by deafferentation of the contralateral hemisphere. Brain 2002; 125: 1402-13.
    CrossrefPubMedSearch in Google Scholar
  • 72 Wohlfarth K, Schneider U, Haacker T, Schubert M, Schulze-Bonhage A, Zedler M, Emrich HM, Dengler R, Rollnik JD. Acamprosate reduces motor cortex excitability determined by transcranial magnetic stimulation. Neuropsychobiology 2000; 42: 183-5.
    CrossrefPubMedSearch in Google Scholar
  • 73 Ziemann U. Transkranielle Magnetstimulation: Neue Einsatzmöglichkeiten zur Messung kortikaler und kortikospinaler Erregbarkeit. Akt Neurol 2001; 28: 249-64.
    Thieme ConnectSearch in Google Scholar
  • 74 Ziemann U, Lönnecker S, Paulus W. Inhibition of human motor cortex by ethanol. A transcranial magnetic stimulation study. Brain 1995; 118: 1437-46.
    CrossrefPubMedSearch in Google Scholar
  • 75 Ziemann U, Bruns D, Paulus W. Enhancement of human motor cortex inhibition by the dopamine receptor agonist pergolide: evidence from transcranial magnetic stimulation. Neurosci Lett 1996a 208: 187-90.
  • 76 Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 1996b 40: 367-78.
  • 77 Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 1996c 109: 127-35.
  • 78 Ziemann U, Paulus W, Rothenberger A. Decreased motor inhibition in Tourette’s disorder: evidence from transcranial magnetic stimulation. Am J Psychiatry 1997a 154: 1277-84.
  • 79 Ziemann U, Tergau F, Bruns D, Baudewig J, Paulus W. Changes in human motor cortex excitability induced by dopaminergic and antidopaminergic drugs. Electroenc Clin Neurophys 1997b 105: 430-7.
  • 80 Ziemann U, Chen R, Cohen LG, Hallett M. Dextromethorphan decreases the excitabiliy of the human motor cortex. Neurology 1998; 51: 1320-4.
    CrossrefPubMedSearch in Google Scholar
  • 81 Ziemann U, Muellbacher W, Hallett M, Cohen LG. Modulation of practice-dependent plasticity in human motor cortex. Brain 2001; 124: 1171-81.
    CrossrefPubMedSearch in Google Scholar