Insights on the neural basis of motor plasticity induced by theta burst stimulation from TMS-EEG

European Journal of Neuroscience

Volumn 37, Issue 4, 2013, Pages 598-606

  Vernet, Marine ^a   Bashir, Shahid ^a,b   Yoo, Woo Kyoung ^a   Perez, Jennifer M ^a   Najib, Umer ^a   Pascual Leone, Alvaro ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

^c University Institute affiliated with the Autonomous University of Barcelona   (Spain)

Author keywords

Cortico spinal excitability; CTBS; Human; Oscillations; TMS evoked potentials

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; EVOKED MUSCLE RESPONSE; EVOKED RESPONSE; FEMALE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; MALE; MOTOR PERFORMANCE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL PLASTICITY; NORMAL HUMAN; OSCILLATORY POTENTIAL; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; THETA BURST STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION;

ADOLESCENT; CORTICAL SYNCHRONIZATION; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; MALE; MOTOR CORTEX; NEURONAL PLASTICITY; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84873991084     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12069     Document Type: Article

References (37)

1. Benali, A., Trippe, J., Weiler, E., Mix, A., Petrasch-Parwez, E., Girzalsky, W., Eysel, U.T., Erdmann, R. & Funke, K. (2011) Theta-burst transcranial magnetic stimulation alters cortical inhibition. J. Neurosci., 31, 1193-1203.
2. Bender, S., Basseler, K., Sebastian, I., Resch, F., Kammer, T., Oelkers-Ax, R. & Weisbrod, M. (2005) Electroencephalographic response to transcranial magnetic stimulation in children: evidence for giant inhibitory potentials. Ann. Neurol., 58, 58-67.
3. Bonato, C., Miniussi, C. & Rossini, P.M. (2006) Transcranial magnetic stimulation and cortical evoked potentials: a TMS/EEG co-registration study. Clin. Neurophysiol., 117, 1699-1707.
4. Bonnard, M., Spieser, L., Meziane, H.B., de Graaf, J.B. & Pailhous, J. (2009) Prior intention can locally tune inhibitory processes in the primary motor cortex: direct evidence from combined TMS-EEG. Eur. J. Neurosci., 30, 913-923.
5. Brignani, D., Manganotti, P., Rossini, P.M. & Miniussi, C. (2008) Modulation of cortical oscillatory activity during transcranial magnetic stimulation. Hum. Brain Mapp., 29, 603-612.
6. Cardenas-Morales, L., Nowak, D.A., Kammer, T., Wolf, R.C. & Schonfeldt-Lecuona, C. (2010) Mechanisms and applications of theta-burst rTMS on the human motor cortex. Brain Topogr., 22, 294-306.
7. Chen, R., Cros, D., Curra, A., Di Lazzaro, V., Lefaucheur, J.P., Magistris, M.R., Mills, K., Rosler, K.M., Triggs, W.J., Ugawa, Y. & Ziemann, U. (2008) The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin. Neurophysiol., 119, 504-532.
8. Delorme, A. & Makeig, S. (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods, 134, 9-21.
9. Di Lazzaro, V., Pilato, F., Saturno, E., Oliviero, A., Dileone, M., Mazzone, P., Insola, A., Tonali, P.A., Ranieri, F., Huang, Y.Z. & Rothwell, J.C. (2005) Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J. Physiol., 565, 945-950.
10. Esser, S.K., Huber, R., Massimini, M., Peterson, M.J., Ferrarelli, F. & Tononi, G. (2006) A direct demonstration of cortical LTP in humans: a combined TMS/EEG study. Brain Res. Bull., 69, 86-94.
11. Ferreri, F., Pasqualetti, P., Maatta, S., Ponzo, D., Ferrarelli, F., Tononi, G., Mervaala, E., Miniussi, C. & Rossini, P.M. (2011) Human brain connectivity during single and paired pulse transcranial magnetic stimulation. Neuroimage, 54, 90-102.
12. Fitzgerald, P.B. (2010) TMS-EEG: a technique that has come of age? Clin. Neurophysiol., 121, 265-267.
13. Fuggetta, G., Fiaschi, A. & Manganotti, P. (2005) Modulation of cortical oscillatory activities induced by varying single-pulse transcranial magnetic stimulation intensity over the left primary motor area: a combined EEG and TMS study. Neuroimage, 27, 896-908.
14. Gentner, R., Wankerl, K., Reinsberger, C., Zeller, D. & Classen, J. (2008) Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb. Cortex, 18, 2046-2053.
15. Goldsworthy, M.R., Pitcher, J.B. & Ridding, M.C. (2012) A comparison of two different continuous theta burst stimulation paradigms applied to the human primary motor cortex. Clin. Neurophysiol., 123, 2256-2263.
16. Huang, Y.Z., Edwards, M.J., Rounis, E., Bhatia, K.P. & Rothwell, J.C. (2005) Theta burst stimulation of the human motor cortex. Neuron, 45, 201-206.
17. Huang, Y.Z., Chen, R.S., Rothwell, J.C. & Wen, H.Y. (2007) The after-effect of human theta burst stimulation is NMDA receptor dependent. Clin. Neurophysiol., 118, 1028-1032.
18. Huber, R., Maatta, S., Esser, S.K., Sarasso, S., Ferrarelli, F., Watson, A., Ferreri, F., Peterson, M.J. & Tononi, G. (2008) Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep. J. Neurosci., 28, 7911-7918.
19. Komssi, S. & Kahkonen, S. (2006) The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research. Brain Res. Rev., 52, 183-192.
20. Komssi, S., Kahkonen, S. & Ilmoniemi, R.J. (2004) The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation. Hum. Brain Mapp., 21, 154-164.
21. Maeda, F., Keenan, J.P., Tormos, J.M., Topka, H. & Pascual-Leone, A. (2000) Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp. Brain Res., 133, 425-430.
22. Maki, H. & Ilmoniemi, R.J. (2010) The relationship between peripheral and early cortical activation induced by transcranial magnetic stimulation. Neurosci. Lett., 478, 24-28.
23. McAllister, S.M., Rothwell, J.C. & Ridding, M.C. (2009) Selective modulation of intracortical inhibition by low-intensity theta burst stimulation. Clin. Neurophysiol., 120, 820-826.
24. McAllister, S.M., Rothwell, J.C. & Ridding, M.C. (2011) Cortical oscillatory activity and the induction of plasticity in the human motor cortex. Eur. J. Neurosci., 33, 1916-1924.
25. Miniussi, C. & Thut, G. (2010) Combining TMS and EEG offers new prospects in cognitive neuroscience. Brain Topogr., 22, 249-256.
26. Nikouline, V., Ruohonen, J. & Ilmoniemi, R.J. (1999) The role of the coil click in TMS assessed with simultaneous EEG. Clin. Neurophysiol., 110, 1325-1328.
27. Noh, N.A., Fuggetta, G., Manganotti, P. & Fiaschi, A. (2012) Long lasting modulation of cortical oscillations after continuous theta burst transcranial magnetic stimulation. PLoS ONE, 7, e35080.
28. Pascual-Leone, A., Freitas, C., Oberman, L., Horvath, J.C., Halko, M., Eldaief, M., Bashir, S., Vernet, M., Shafi, M., Westover, B., Vahabzadeh-Hagh, A.M. & Rotenberg, A. (2011) Characterizing brain cortical plasticity and network dynamics across the age-span in health and disease with TMS-EEG and TMS-fMRI. Brain Topogr., 24, 302-315.
29. Paus, T., Sipila, P.K. & Strafella, A.P. (2001) Synchronization of neuronal activity in the human primary motor cortex by transcranial magnetic stimulation: an EEG study. J. Neurophysiol., 86, 1983-1990.
30. Ridding, M.C. & Ziemann, U. (2010) Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J. Physiol., 588, 2291-2304.
31. Rosanova, M., Casali, A., Bellina, V., Resta, F., Mariotti, M. & Massimini, M. (2009) Natural frequencies of human corticothalamic circuits. J. Neurosci., 29, 7679-7685.
32. Rossi, S., Hallett, M., Rossini, P.M. & Pascual-Leone, A. (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol., 120, 2008-2039.
33. Rossini, P.M., Barker, A.T., Berardelli, A., Caramia, M.D., Caruso, G., Cracco, R.Q., Dimitrijevic, M.R., Hallett, M., Katayama, Y., Lucking, C.H., Maertens de Noordhout, A.L., Marsden, C.D., Murray, N.M.F., Rothwell, J.C., Swash, M. & Tomberg, C. (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr. Clin. Neurophysiol., 91, 79-92.
34. Silva, L.R., Amitai, Y. & Connors, B. W. (1991) Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science, 251, 432-435.
35. Spieser, L., Meziane, H.B. & Bonnard, M. (2010) Cortical mechanisms underlying stretch reflex adaptation to intention: a combined EEG-TMS study. Neuroimage, 52, 316-325.
36. Van Der Werf, Y.D. & Paus, T. (2006) The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions. Exp. Brain Res., 175, 231-245.
37. Virtanen, J., Ruohonen, J., Naatanen, R. & Ilmoniemi, R.J. (1999) Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Med. Biol. Eng. Comput., 37, 322-326.