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Persistent effects of high frequency repetitive TMS on the coupling between motor areas in the human

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Abstract

Repetitive transcranial magnetic stimulation (rTMS) shows promise as a treatment for various movement and psychiatric disorders. How rTMS may have persistent effects on cortical function remains unclear. We hypothesised that it may act by modulating cortico-cortical connectivity. To this end we assessed cortico-cortical coherence before and after high frequency rTMS of the motor cortex. Sixteen healthy subjects received a single train (5 Hz, active motor threshold, 50 stimuli) of rTMS to the left motor hand area. Spectral power and coherence estimates were calculated between different EEG signals at rest and while muscles of the distal upper limb were tonically contracted. Repetitive TMS over the left motor hand area caused a significant decrease in the intrahemispheric EEG-EEG coherence between motor and premotor cortex in the 10.7–13.6 Hz (upper alpha band) lasting a few minutes after stimulation. There was no significant change in interhemispheric EEG-EEG coherence between motor areas. Thus, high frequency rTMS of the motor cortex decreases ipsilateral cortico-cortical intrahemispheric in the upper alpha band.

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References

  • Andrew C, Pfurtscheller G (1997) On the existence of different alpha band rhythms in the hand area of man. Neurosci Lett 222:103–106

    Article  CAS  PubMed  Google Scholar 

  • Berardelli A, Inghilleri M, Rothwell JC, Romeo S, Curra A, Gilio, F, Modugno N, Manfredi M (1998) Facilitation of muscle evoked responses after repetitive cortical stimulation in man. Exp Brain Res 122:79–84

    CAS  PubMed  Google Scholar 

  • 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 9:132–136

    CAS  PubMed  Google Scholar 

  • 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 48:1398–1403

    CAS  PubMed  Google Scholar 

  • Chen R, Yaseen Z, Cohen LG, Hallett M (1998) Time course of corticospinal excitability in reaction time and self-paced movements. Ann Neurol 44:317–325

    CAS  PubMed  Google Scholar 

  • Civardi C, Cantello R, Asselman P, Rothwell JC (2001) Transcranial magnetic stimulation can be used to test connections to primary motor areas from frontal and medial cortex in humans. Neuroimage 14:1444–1453

    Article  CAS  PubMed  Google Scholar 

  • Cohen LG, Celnik P, Pascual-Leone A, Corwell B, Falz L, Dambrosia J, Honda M, Sadato N, Gerloff C, Catala MD, Hallett M (1997) Functional relevance of cross-modal plasticity in blind humans. Nature 389:180–183

    CAS  PubMed  Google Scholar 

  • Cohen LG, Ziemann U, Chen R, Classen J, Hallett M, Gerloff C, Butefisch C (1998) Studies of neuroplasticity with transcranial magnetic stimulation. J Clin Neurophysiol 15:305–324

    PubMed  Google Scholar 

  • Deiber MP, Caldara R, Ibanez V, Hauert CA (2001) Alpha band power changes in unimanual and bimanual sequential movements, and during motor transitions. Clin Neurophysiol 112:1419–1435

    CAS  PubMed  Google Scholar 

  • Di Lazzaro V, Oliviero A, Meglio M, Cioni B, Tamburrini G, Tonali P, Rothwell JC (2000) Direct demonstration of the effect of lorazepam on the excitability of the human motor cortex. Clin Neurophysiol 111:794–799

    PubMed  Google Scholar 

  • Di Lazzaro V, Oliviero A, Mazzone P, Pilato F, Saturno E, Dileone M, Insola A, Tonali PA, Rothwell JC (2002) Short-term reduction of intracortical inhibition in the human motor cortex induced by repetitive transcranial magnetic stimulation. Exp Brain Res 147:108–113

    PubMed  Google Scholar 

  • Gerloff C, Richard J, Hadley J, Schulman A, Honda M, Hallett M (1998) Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. Brain 121:1513–1531

    PubMed  Google Scholar 

  • Gerschlagher W, Siebner HR, Rothwell JC (2001) Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology 57:449–455

    CAS  PubMed  Google Scholar 

  • Grafman J, Wassermann E (1999) Transcranial magnetic stimulation can measure and modulate learning and memory. Neuropsychologia 37:159–167

    CAS  PubMed  Google Scholar 

  • Halliday DM, Rosenberg JR, Amjad AM, Breeze P, Conway BA, Farmer SF (1995) A framework for the analysis of mixed time series/point process data theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. Prog Biophys Mol Biol 64:237–278

    CAS  PubMed  Google Scholar 

  • Homan RW, Herman J, Purdy P (1987) Cerebral location of international 10–20 system electrode placement. Electroencephalogr Clin Neurophysiol 66:376–382

    Google Scholar 

  • Hummel F, Andres F, Altenmuller E, Dichgans J, Gerloff C (2002) Inhibitory control of acquired motor programmes in the human brain. Brain 125:404–420

    Article  PubMed  Google Scholar 

  • Jing H, Takigawa M (2000) Observation of EEG coherence after repetitive transcranial magnetic stimulation. Clin Neurophysiol 111:1620–1631

    CAS  PubMed  Google Scholar 

  • 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 471:501–519

    CAS  PubMed  Google Scholar 

  • Leocani L, Toro C, Manganotti P, Zhuang P, Hallett M (1997) Event-related coherence and event-related desynchronisation/synchronisation in the 10 Hz and 20 Hz EEG during self-paced movements. Electroencephalogr Clin Neurophysiol 104:199–206

    CAS  PubMed  Google Scholar 

  • Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 111:800–805

    CAS  PubMed  Google Scholar 

  • Manganotti P, Gerloff C, Toro C, Katsuta H, Sadato N, Zhuang P, Leocani L, Hallett M (1998) Task-related coherence and task-related spectral power changes during sequential finger movements. Electroencephalogr Clin Neurophysiol 109:50–62

    CAS  PubMed  Google Scholar 

  • Mills KR, Boniface SJ, Schubert M (1992) Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr Clin Neurophysiol 85:17–21

    CAS  PubMed  Google Scholar 

  • Mima T, Matsuoka T, Hallett M (2000a) Functional coupling of human right and left cortical motor areas demonstrated with partial coherence analysis. Neurosci Lett 287:93–96

    Article  CAS  PubMed  Google Scholar 

  • Mima T, Steger J, Schulman AE, Gerloff C, Hallett M (2000b) Electroencephalographic measurement of motor cortex control of muscle activity in humans. Clin Neurophysiol 111:326–337

    CAS  PubMed  Google Scholar 

  • Nuñez PL, Srinivasan R, Westdorp AF, Wijesinghe RS, Tucker DM, Silberstein RB, Cadusch PJ (1997) EEG coherency 1: statistics, reference electrode, volume conduction, Laplacians, cortical imaging and interpretation at multiple scales. Electroencephalogr Clin Neurophysiol 103:499–515

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    CAS  PubMed  Google Scholar 

  • Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M (1994) Related articles, responses to rapid-rate transcranial magnetic stimulation of the human motor cotex. Brain 117:847–858

    PubMed  Google Scholar 

  • Pascual-Leone A, Tormos JM, Keenan J, Tarazona F, Canete C, Catala MD (1998) Study and modulation of human cortical excitability with transcranial magnetic stimulation. J Clin Neurophysiol 15:333–343

    CAS  PubMed  Google Scholar 

  • Peinemann A, Lehner C, Mentschel C, Munchau A, Conrad B, Siebner HR (2000) Subthreshold 5-Hz repetitive transcranial magnetic stimulation of the human primary motor cortex reduces intracortical paired-pulse inhibition. Neurosci Lett 296:21–24

    CAS  PubMed  Google Scholar 

  • Pfurtscheller G (1988) Mapping of event-related desynchronisation and type of derivation. Electroencephalogr Clin Neurophysiol 70:190–193

    CAS  PubMed  Google Scholar 

  • Pfurtscheller G (1992) Event-related synchronisation (ERS): an electrophysiological correlate of cortical areas at rest. Electroencephalogr Clin Neurophysiol 83:62–69

    CAS  PubMed  Google Scholar 

  • Pfurtscheller G, Sager W, Wege W (1981) Correlations between CT scan and sensorimotor EEG rhythms in patients with cerebrovascular disorders. Electroencephalogr Clin Neurophysiol 52:473–485

    CAS  PubMed  Google Scholar 

  • Pfurtscheller G, Prezenger M, Neuper C (1994) Visualisation of sensorimotor areas involved in preparation for hand movement based on classification of mu and central beta rhythms in single EEG trials in man. Neurosci Lett 181:43–46

    CAS  PubMed  Google Scholar 

  • Pfurtscheller G, Neuper C, Andrew C, Edlinger G (1997) Foot and hand area mu rhythms. Int J Psychophysiol 26:121–135

    Article  CAS  PubMed  Google Scholar 

  • Pfurtscheller G, Neuper C, Krausz G (2000) Functional dissociation of lower and upper mu rhythms in relation to voluntary limb movement. Clin Neurophysiol 111:1873–1879

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg JR, Amjad AM, Breeze P, Brillinger DR, Halliday DM (1989) The Fourier approach to the identification of functional coupling between neuronal spike trains: maximum likelihood analysis of spike trains of interacting nerve cells. Prog Biophys Mol Biol 53:1–31

    CAS  PubMed  Google Scholar 

  • Salmelin R, Hari R (1994) Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement. Neuroscience 60:537–550

    CAS  PubMed  Google Scholar 

  • Serrien DJ, Strens LHA, Oliviero A, Brown P (2002) Repetitive transcranial magnetic stimulation of the supplementary motor area (SMA) degrades bimanual movement control in humans. Neurosci Lett 328:89–92

    CAS  PubMed  Google Scholar 

  • Siebner HR, Auer C, Conrad B (1999) Abnormal increase in the corticomotor output to the affected hand during repetitive transcranial magnetic stimulation of the primary motor cortex in patients with writer's cramp. Neurosci Lett 262:133–136

    CAS  PubMed  Google Scholar 

  • Siebner HR, Peller M, Willoch F, Minoshima S, Boecker H, Auer C, Drzezga A, Conrad B, Bartstein P (2000) Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology 54:956–963

    CAS  PubMed  Google Scholar 

  • 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 sensorimotor cortex: a glucose PET study. Hum Brain Mapp 12:157–167

    CAS  PubMed  Google Scholar 

  • Stancak A Jr, Pfurtscheller G (1995) Desynchronisation and recovery of beta rhythms during brisk and slow self-paced finger movements in man. Neurosci Lett 196:21–24

    PubMed  Google Scholar 

  • Stancak A Jr, Pfurtscheller G (1996a) The effects of handedness and type of movement on the contralateral preponderance of mu-rhythm desynchronisation. Electroencephalogr Clin Neurophysiol 99:174–182

    Article  PubMed  Google Scholar 

  • Stancak A Jr, Pfurtscheller G (1996b) Mu-rhythm changes in brisk and slow self-paced finger movements. Neuroreport 7:1161–1164

    PubMed  Google Scholar 

  • Stancak A Jr, Pfurtscheller G (1996c) Event-related desynchronisation of central beta-rhythms during brisk and slow self-paced finger movements of dominant and non-dominant hand. Brain Res Cogn Brain Res 4:171–183

    PubMed  Google Scholar 

  • Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123:572–584

    Article  PubMed  Google Scholar 

  • Steinmetz H, Furst G, Meyer BU (1989) Craniocerebral topography within the international 10–20 system. Electroencephalogr Clin Neurophysiol 72:499–506

    CAS  PubMed  Google Scholar 

  • Strens LHA, Oliviero A, Bloem BR, Gerschlager W, Rothwell JC, Brown P (2002) The effects of subthreshold 1 Hz repetitive TMS on cortico-cortical and interhemispheric coherence. Clin Neurophysiol 113:1279–1285

    Article  PubMed  Google Scholar 

  • Thatcher RW, Krause PJ, Hrybyk M (1986) Cortico-cortical associations and EEG coherence: a two-compartmental model. Electroencephalogr Clin Neurophysiol 64:123–143

    CAS  PubMed  Google Scholar 

  • Toro C, Deuschl G, Thatcher R, Sato S, Kufta C, Hallett M (1994a) Event-related desynchronisation and movement-related cortical potentials on the ECoG and EEG. Electroencephalogr Clin Neurophysiol 93:380–390

    CAS  PubMed  Google Scholar 

  • Toro C, Cox C, Friehs G, Ojakangas C, Maxwell R, Gates JR, Gumnit RJ, Ebner TJ (1994b) 8–12 Hz rhythmic oscillations in human motor cortex during two-dimensional arm movements: evidence for representation of kinematic parameters. Electroencephalogr Clin Neurophysiol 93:390–403

    CAS  PubMed  Google Scholar 

  • 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 Neurophsiol 108:1–16

    Article  CAS  Google Scholar 

  • Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J (1999) Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol 517:591–597

    CAS  PubMed  Google Scholar 

  • Worden MS, Foxe JJ, Wang N, Simpson GV (2000) Anticipatory biasing of visuospatial attention indexed by retinotopically specific alpha-bank electroencephalography increases over occipital cortex. J Neurosci 20:RC63

    CAS  PubMed  Google Scholar 

  • Wu T, Sommer M, Tergau F, Paulus W (2000) Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci Lett 287:37–40

    CAS  PubMed  Google Scholar 

  • Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996a) Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:367–378

    CAS  PubMed  Google Scholar 

  • Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996b) The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 109:127–135

    CAS  PubMed  Google Scholar 

  • Ziemann U, Corwell B, Cohen LG (1998) Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci 18:1115–1123

    CAS  PubMed  Google Scholar 

  • Ziemann U, Muellbacher W, Hallett M, Cohen LG (2001) Modulation of practice-dependent plasticity in human motor cortex. Brain 124:1171–1181

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Istituto di Neurologia, Università Cattolica, L.go A. Gemelli 8, 00168, Rome, Italy

    Antonio Oliviero, Vincenzo Di Lazzaro & Pietro A. Tonali

  2. Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, London, UK

    Antonio Oliviero, Lucy H. A. Strens & Peter Brown

  3. IRCCS "Casa Sollievo della Sofferenza", San Giovanni Rotondo, Italy

    Pietro A. Tonali

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  1. Antonio Oliviero
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  2. Lucy H. A. Strens
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  3. Vincenzo Di Lazzaro
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  4. Pietro A. Tonali
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  5. Peter Brown
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Correspondence to Antonio Oliviero.

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Oliviero, A., Strens, L.H.A., Di Lazzaro, V. et al. Persistent effects of high frequency repetitive TMS on the coupling between motor areas in the human. Exp Brain Res 149, 107–113 (2003). https://doi.org/10.1007/s00221-002-1344-x

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  • DOI: https://doi.org/10.1007/s00221-002-1344-x

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