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Cited by 238Transcranial Magnetic Stimulation StudiesEEG and Brain-Computer InterfacesTraumatic Brain Injury Research

TMS combined with EEG: Recommendations and open issues for data collection and analysis

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Hernandez-Pavon, Julio C., Veniero, Domenica, Bergmann, Til Ole, Belardinelli, Paolo, Bortoletto, Marta, Casarotto, Silvia, Casula, Elias P., Farzan, Faranak +15 more·2023·Brain Stimulation
DOI 10.1016/j.brs.2023.02.009
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Abstract

Transcranial magnetic stimulation (TMS) evokes neuronal activity in the targeted cortex and connected brain regions. The evoked brain response can be measured with electroencephalography (EEG). TMS combined with simultaneous EEG (TMS-EEG) is widely used for studying cortical reactivity and connectivity at high spatiotemporal resolution. Methodologically, the combination of TMS with EEG is challenging, and there are many open questions in the field. Different TMS-EEG equipment and approaches for data collection and analysis are used. The lack of standardization may affect reproducibility and limit the comparability of results produced in different research laboratories. In addition, there is controversy about the extent to which auditory and somatosensory inputs contribute to transcranially evoked EEG. This review provides a guide for researchers who wish to use TMS-EEG to study the reactivity of the human cortex. A worldwide panel of experts working on TMS-EEG covered all aspects that should be considered in TMS-EEG experiments, providing methodological recommendations (when possible) for effective TMS-EEG recordings and analysis. The panel identified and discussed the challenges of the technique, particularly regarding recording procedures, artifact correction, analysis, and interpretation of the transcranial evoked potentials (TEPs). Therefore, this work offers an extensive overview of TMS-EEG methodology and thus may promote standardization of experimental and computational procedures across groups.

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  • TMS-EEG generates a TEP whose amplitude and spatio-temporal characteristics reflect activity of cortical circuits within the stimulated cortex and interconnected areas.

    “This generates a TMS-evoked EEG potential (TEP), the amplitude and spatio-temporal characteristics of which reflect activity of cortical circuits within the stimulated cortex and interconnected areas (HernandezPavon et al. 2023).”

    From Mild traumatic brain injury alters function in the dorsolateral prefrontal cortex: a TMS-EEG study (2025) · cites this paper as Hernandez-Pavon et al. 2023

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  1. [1][1] [Barker A, Jalinous R, Freeston I. Non-invasive magnetic stimulation of human motor cortex. Lancet 1985;1(8437):1106 e 7.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref1) -
  2. [2][2] [Cracco R, Amassian V, Maccabee P, Cracco J. Comparison of human transcallosal responses evoked by magnetic coil and electrical stimulation. Electroencephalogr Clin Neurophysiol 1989;74:417 e 24.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref2) -
  3. [3][3] [Amassian V, Cracco R, Maccabee P, Cracco J. Cerebello-frontal cortical projections in humans studied with the magnetic coil. Electroencephalogr Clin Neurophysiol 1992;85(4):265 e 72.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref3) -
  4. [4][4] [Ilmoniemi R, Virtanen J, Ruohonen J, Karhu J, Aronen H, N € a € at € anen R, et al. Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 1997;8:3537 e 40.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref4) -
  5. [5][5] [Tremblay S, Rogasch N, Premoli I, Blumberger D, Casarotto S, Chen R, et al. Clinical utility and prospective of TMS e EEG. Clin Neurophysiol 2019;130(5): 802 e 44.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref5) -
  6. [6][6] [Ridding M, Rothwell J. Is there a future for therapeutic use of transcranial magnetic stimulation? Nat Rev Neurosci 2007;8(7):559 e 67.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref6) -
  7. [7][7] [Ilmoniemi R, Ruohonen J, Virtanen J, Aronen H, Karhu J. EEG responses evoked by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol Suppl 1999;51:22 e 9.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref7) -
  8. [9][9] [Maccabee P, Amassian V, Eberle L, Cracco R. Magnetic coil stimulation of straight and bent amphibian and mammalian peripheral nerve in vitro: locus of excitation. J Physiol 1993;460:201 e 19.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref9) -
  9. [10][10] [Ruohonen J. Chapter 1 background physics for magnetic stimulation. Supplements to clinical neurophysiology transcranial magnetic stimulation and transcranial direct current stimulation, proceedings of the 2nd international transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS). Symposium 2003;56:3 e 12.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref10) -
  10. [11][11] [Deng Z, Lisanby S, Peterchev A. Electric fi eld depth-focality tradeoff in transcranial magnetic stimulation: simulation comparison of 50 coil designs. Brain Stimul 2013;6(1):1 e 13.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref11) -
  11. [12][12] [Ilmoniemi R, Ruohonen J, Karhu J. Transcranial magnetic stimulation -a new tool for functional imaging of the brain. Crit Rev Biomed Eng 1999;27(3 e 5): 241 e 84.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref12) -
  12. [13][13] [Romero M, Davare M, Armendariz M, Janssen P. Neural effects of transcranial magnetic stimulation at the single-cell level. Nat Commun 2019;10(2642): 1 e 11.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref13) -
  13. [14][14] [Di Lazzaro V, Ziemann U. The contribution of transcranial magnetic stimulation in the functional evaluation of microcircuits in human motor cortex. Front Neural Circ 2013;7:18.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref14) -
  14. [15][15] [Bergmann TO, Hartwigsen G. Inferring causality from noninvasive brain stimulation in cognitive neuroscience. J Cognit Neurosci 2021;33(2): 195 e 225.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref15) -
  15. [16][16] [Baillet S, Mosher J, Leahy R. Electromagnetic brain mapping. IEEE Signal Process Mag 2001;18(6):14 e 30.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref16) -
  16. [17][17] [Bergmann T, Karabanov A, Hartwigsen G, Thielscher A, Siebner H. Combining non-invasive transcranial brain stimulation with neuroimaging and electrophysiology: current approaches and future perspectives. Neuroimage 2016;140:4 e 19.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref17) -
  17. [18][18] [Hallett M, Di Iorio R, Rossini P, Park J, Chen R, Celnik P, et al. Contribution of transcranial magnetic stimulation to assessment of brain connectivity and networks. Clin Neurophysiol 2017;128(11):2125 e 39.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref18) -
  18. [19][19] [Siebner H, Bergmann T, Bestmann S, Massimini M, Johansen-Berg H, Mochizuki H, et al. Consensus paper: combining transcranial stimulation with neuroimaging. Brain Stimul 2009;2(2):58 e 80.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref19) -
  19. [20][20] [Berger H. Uber das Elektroenkephalogramm des Menschen (On the electroencephalogram of man). Arch Psychiatr Nervenkr 1929;87:527 e 70.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref20) -
  20. [22][22] [Schomer D, da Silva F. Niedermeyer's electroencephalography: basic principles, clinical applications, and related fi elds. 2018.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref22) -
  21. [23][23] [Ilmoniemi R, Sarvas J. Brain signals physics and mathematics of MEG and EEG. The MIT Press; 2019.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref23) -
  22. [25][25] [de Munck J, Vijn P, Lopez da Silva F. A random dipole model for spontaneous brain activity. IEEE Trans Biomed Eng 1992;39(8):791 e 804.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref25) -
  23. [26][26] [Ilmoniemi R. Neuromagnetism : theory, techniques, and measurements department of technical physics. Espoo, Finland: Helsinki University of Technology; 1985.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref26) -
  24. [27][27] [Miniussi C, Thut G. Combining TMS and EEG offers new prospects in cognitive neuroscience. Brain Topogr 2010;22(4):249 e 56.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref27) -
  25. [28][28] Ilmoniemi R, Kici c D. Methodology for combined TMS and EEG. Brain Topogr 2010;22(4):233 e 48. -
  26. [29][29] [Bortoletto M, Bonzano L, Zazio A, Ferrari C, Pedull a L, Gasparotti R, et al. Asymmetric transcallosal conduction delay leads to fi ner bimanual coordination. Brain Stimul 2021;14(2):379 e 88.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref29) -
  27. [30][30] [Kallioniemi E, Saari J, Ferreri F, M € a € att € a S. TMS-EEG responses across the lifespan: measurement, methods for characterisation and identi fi ed responses. J Neurosci Methods 2022;366(109430):1 e 19.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref30) -
  28. [31][31] [Luck S. An introduction to the event-related potential technique. second ed. 2014. Second Edition.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref31) -
  29. [32][32] [Lioumis P, Ki ci c D, Savolainen P, M € akel € a J, K € ahk € onen S. Reproducibility of TMS-Evoked EEG responses. Hum Brain Mapp 2009;30(4):1387 e 96.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref32) -
  30. [33][33] [Kerwin L, Keller C, Wu W, Narayan M, Etkin A. Test-retest reliability of transcranial magnetic stimulation EEG evoked potentials. Brain Stimul 2018;11(3):536 e 44.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref33) -
  31. [34][34] [Casarotto S, Fecchio M, Rosanova M, Varone G, D ' Ambrosio S, Sarasso S, et al. The rt-TEP tool: real-time visualization of TMS-Evoked Potential to maximize cortical activation and minimize artifacts. J Neurosci Methods 2022;370: 109486.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref34) -
  32. [35][35] [Komssi S, K € ahk € onen S, Ilmoniemi R. The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation. Hum Brain Mapp 2004;21:154 e 64.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref35) -
  33. [37][37] [Bonato C, Miniussi C, Rossini P. Transcranial magnetic stimulation and cortical evoked potentials: a TMS/EEG co-registration study. Clin Neurophysiol 2006;117(8):1699 e 707.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref37) -
  34. [38][38] [Rocchi L, Di Santo A, Brown K, Ib a ~ nez J, Casula E, Rawji V, et al. Disentangling EEG responses to TMS due to cortical and peripheral activations. Brain Stimul 2021;14(1):4 e 18.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref38) -
  35. [39][39] [Belardinelli P, K € onig F, Liang C, Premoli I, Desideri D, Müller-Dahlhaus F, et al. TMS-EEG signatures of glutamatergic neurotransmission in human cortex. Sci Rep 2021;11(1):1 e 14.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref39) -
  36. [40][40] [Nikulin V, Ki ci c D, K € ahk € onen S, Ilmoniemi R. Modulation of electroencephalographic responses to transcranial magnetic stimulation: evidence for changes in cortical excitability related to movement. Eur J Neurosci 2003;18(5):1206 e 12.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref40) -
  37. [42][42] [Sarasso S, Boly M, Napolitani M, Gosseries O, Charland-Verville V, Casarotto S, et al. Consciousness and complexity during unresponsiveness induced by propofol, xenon, and ketamine. Curr Biol 2015;25(23):3099 e 105.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref42) -
  38. [43][43] [Sha fi M, Vernet M, Klooster D, Chu C, Boric K, Barnard M, et al. Physiological consequences of abnormal connectivity in a developmental epilepsy. Ann Neurol 2015;77(3):487 e 503.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref43) -
  39. [44][44] [Fox P, Narayana S, Tandon N, Fox S, Sandoval H, Kochunov P, et al. Intensity modulation of TMS-induced cortical excitation: primary motor cortex. Hum Brain Mapp 2006;27:478 e 87.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref44) -
  40. [45][45] [Saari J, Kallioniemi E, Tarvainen M, Julkunen P. Oscillatory TMS-EEGresponses as a measure of the cortical excitability threshold. IEEE Trans Neural Syst Rehabil Eng 2018;26(2):383 e 91.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref45) -
  41. [46][46] [Rosanova M, Casali A, Bellina V, Resta F, Mariotti M, Massimini M. Natural frequencies of human corticothalamic circuits. J Neurosci 2009;29(24): 7679 e 85.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref46) -
  42. [47][47] [Thut G, Miniussi C, Gross J. The functional importance of rhythmic activity in the brain. Curr Biol 2012;22(16):R658 e 63.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref47) -
  43. [48][48] [Vallesi A, Del Felice A, Capizzi M, Tafuro A, Formaggio E, Bisiacchi P, et al. Natural oscillation frequencies in the two lateral prefrontal cortices induced by Transcranial Magnetic Stimulation. Neuroimage 2021;227:117655.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref48) -
  44. [49][49] [Herring JD, Thut G, Jensen O, Bergmann TO. Attention modulates TMS-locked alpha oscillations in the visual cortex. J Neurosci 2015;35(43):14435 e 47.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref49) -
  45. [50][50] [Veniero D, Gross J, Morand S, Duecker F, Sack AT, Thut G. Top-down control of visual cortex by the frontal eye fi elds through oscillatory realignment. Nat Commun 2021;12(1):1757.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref50) -
  46. [52][52] [Premoli I, Bergmann T, Fecchio M, Rosanova M, Biondi A, Belardinelli P, et al. The impact of GABAergic drugs on TMS-induced brain oscillations in human motor cortex. Neuroimage 2017;163:1 e 12.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref52) -
  47. [53][53] [Thut G, Bergmann TO, Frohlich F, Soekadar SR, Brittain JS, Valero-Cabre A, et al. Guiding transcranial brain stimulation by EEG/MEG to interact with ongoing brain activity and associated functions: a position paper. Clin Neurophysiol 2017;128(5):843 e 57.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref53) -
  48. [54][54] [Pellicciari MC, Veniero D, Miniussi C. Characterizing the cortical oscillatory response to TMS pulse. Front Cell Neurosci 2017;11:38.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref54) -
  49. [55][55] [Casarotto S, Romero Lauro L, Bellina V, Casali A, Rosanova M, Pigorini A, et al. EEG responses to TMS are sensitive to changes in the perturbation parameters and repeatable over time. PLoS One 2010;5(4):e10281.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref55) -
  50. [56][56] [Gosseries O, Sarasso S, Casarotto S, Boly M, Schnakers C, Napolitani M, et al. On the cerebral origin of EEG responses to TMS: insights from severe cortical lesions. Brain Stimul 2015;8(1):142 e 9.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref56) -
  51. [57][57] [Rossi S, Antal A, Bestmann S, Bikson M, Brewer C, Brockm € oller J, et al. Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: expert Guidelines. Clin Neurophysiol 2021;132(1):269 e 306.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref57) -
  52. [58][58] [Deng Z, Lisanby S, Peterchev A. Coil design considerations for deep transcranial magnetic stimulation. Clin Neurophysiol 2014;125(6):1202 e 12.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref58) -
  53. [59][59] [Ueno S, Tashiro T, Harada K. Localized stimulation of neural tissue in the brain by means of a paired con fi guration of time-varying magnetic fi elds. J App Phys 1988;64:5862 e 4.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref59) -
  54. [60][60] [Fernandez L, Biabani M, Do M, Opie G, Hill A, Barham M, et al. Assessing cerebellar-cortical connectivity using concurrent TMS-EEG: a feasibility study. J Neurophysiol 2021;125(5):1768 e 87.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref60) -
  55. [61][61] [Koponen L, Nieminen J, Ilmoniemi R. Multi-locus transcranial magnetic stimulation-theory and implementation. Brain Stimul 2018;11(4):849 e 55.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref61) -
  56. [62][62] [Nieminen JO, Sinisalo H, Souza VH, Malmi M, Yuryev M, Tervo AE, et al. Multi-locus transcranial magnetic stimulation system for electronically targeted brain stimulation. Brain Stimul 2022;15(1):116 e 24.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref62) -
  57. [63][63] [Souza VH, Nieminen JO, Tugin S, Koponen LM, Baffa O, Ilmoniemi RJ. TMS with fast and accurate electronic control: measuring the orientation sensitivity of corticomotor pathways. Brain Stimul 2022;15(2):306 e 15.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref63) -
  58. [64][64] [Tervo AE, Nieminen JO, Lioumis P, Metsomaa J, Souza VH, Sinisalo H, et al. Closed-loop optimization of transcranial magnetic stimulation with electroencephalography feedback. Brain Stimul 2022;15(2):523 e 31.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref64) -
  59. [65][65] [Sommer M, Alfaro A, Rummel M, Speck S, Lang N, Tings T, et al. Half sine, monophasic and biphasic transcranial magnetic stimulation of the human motor cortex. Clin Neurophysiol 2006;117(4):838 e 44.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref65) -
  60. [66][66] [Jung N, Delvendahl I, Pechmann A, Gleich B, Gattinger N, Siebner H, et al. Transcranial magnetic stimulation with a half-sine wave pulse elicits direction-speci fi c effects in human motor cortex. BMC Neurosci 2012;13(139):1 e 9.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref66) -
  61. [67][67] [Delvendahl I, Gattinger N, Berger T, Gleich B, Siebner H, Mall V. The role of pulse shape in motor cortex transcranial magnetic stimulation using full-sine stimuli. PLoS One 2014;9(12):e115247.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref67) -
  62. [68][68] [Delvendahl I, Lindemann H, Jung N, Pechmann A, Siebner H, Mall V. In fl uence of waveform and current direction on short-interval intracortical facilitation: a paired-pulse TMS study. Brain Stimul 2014;7(1):49 e 58.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref68) -
  63. [69][69] [Groppa S, Oliviero A, Eisen A, Quartarone A, Cohen L, Mall V, et al. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol 2012;23(5). 858-582.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref69) -
  64. [70][70] [Funke K. Transcranial magnetic stimulation of rodents: repetitive transcranial magnetic stimulation d a noninvasive way to induce neural plasticity in vivo and in vitro. In: Manahan-Vaughan D, editor. Handbook of behavioral neuroscience. Elsevier; 2018. p. 365 e 87.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref70) -
  65. [71][71] [Rossini P, Burke D, Chen R, Cohen L, Z D, Di Iorio R, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 2015;26(6):1071 e 107.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref71) -
  66. [72][72] [Kammer T, Beck S, Thielscher A, Laubis-Herrmann U, Topka H. Motor thresholds in humans: a transcranial magnetic stimulation study comparing](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref72) - [different pulse waveforms, current directions and stimulator types. Clin Neurophysiol 2001;112(2):250 e 8.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref72) -
  67. [73][73] [Mills K, Boniface S, Schubert M. Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr Clin Neurophysiol 1992;85:17 e 21.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref73) -
  68. [74][74] [Corthout E, Barker A, Cowey A. Transcranial magnetic stimulation: which part of the current waveform causes the stimulation? Exp Brain Res 2001;141(1):128 e 32.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref74) -
  69. [75][75] [Mutanen T, M € aki H, Ilmoniemi R. The effect of stimulus parameters on TMSEEG muscle artifacts. Brain Stimul 2013;6(3):371 e 6.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref75) -
  70. [76][76] [Rogasch NC, Thomson RH, Daskalakis ZJ, Fitzgerald PB. Short-latency artifacts associated with concurrent TMS-EEG. Brain Stimul 2013;6(6):868 e 76.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref76) -
  71. [77][77] [Veniero D, Bortoletto M, Miniussi C. TMS-EEG co-registration: on TMSinduced artifact. Clin Neurophysiol 2009;120(7):1392 e 9.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref77) -
  72. [78][78] [Casula E, Rocchi L, Hannah R, Rothwell J. Effects of pulse width, waveform and current direction in the cortex: a combined cTMS-EEG study. Brain Stimul 2018;11(5):1063 e 70.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref78) -
  73. [79][79] [Virtanen J, Ruohonen J, N € a € at € anen R, Ilmoniemi R. Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Med Biol Eng Comput 1999;37(3):322 e 6.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref79) -
  74. [80][80] [Iramina I, Maeno T, Nonaka Y, Ueno S. Measurement of evoked electroencephalography induced by transcranial magnetic stimulation. J Appl Phys 2003;93(10):6718 e 20.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref80) -
  75. [81][81] [Taylor J, Loo C. Stimulus waveform in fl uences the ef fi cacy of repetitive transcranial magnetic stimulation. J Affect Disord 2007;97(1 e 3):271 e 6.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref81) -
  76. [82][82] [Freche D, Naim-Feil J, Peled A, Levit-Binnun N, Moses E. A quantitative physical model of the TMS-induced discharge artifacts in EEG. PLoS Comput Biol 2018;14(7):1 e 35.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref82) -
  77. [83][83] [Bae J, MacFall J, Krishnan K, Payne M, Steffens D, Taylor W. Dorsolateral prefrontal cortex and anterior cingulate cortex white matter alterations in late-life depression. Biol Psychiatr 2006;60(12):1356 e 63.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref83) -
  78. [84][84] [Tanner D, Norton JJ, Morgan-Short K, Luck SJ. On high-pass fi lter artifacts (they're real) and baseline correction (it's a good idea) in ERP/ERMF analysis. J Neurosci Methods 2016;266:166 e 70.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref84) -
  79. [85][85] [Varone G, Hussain Z, Sheikh Z, Howard A, Boulila W, Mahmud M, et al. Realtime artifacts reduction during TMS-EEG Co-registration: a comprehensive review on technologies and procedures. Sensors (Basel) 2021;21(637):1 e 23.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref85) -
  80. [86][86] [Mancuso M, Sveva V, Cruciani A, Brown K, Ib a ~ nez J, Rawji V, et al. Transcranial evoked potentials can Be reliably recorded with active electrodes. Brain Sci 2021;11(145):1 e 16.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref86) -
  81. [87][87] [Ozdemir R, Tadayon E, Boucher P, Momi D, Karakhanyan K, Fox M, et al. Individualized perturbation of the human connectome reveals reproducible biomarkers of network dynamics relevant to cognition. Proc Natl Acad Sci U S A 2020;117(14):8115 e 25.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref87) -
  82. [88][88] [Rawji V, Kaczmarczyk I, Rocchi L, Fong PY, Rothwell JC, Sharma N. Preconditioning stimulus intensity alters paired-pulse TMS evoked potentials. Brain Sci 2021;11(3).](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref88) -
  83. [89][89] [Julkunen P, S € ais € anen L, Sarasti M, K € on € onen M. Effect of electrode cap on measured cortical motor threshold. J Neurosci Methods 2009;176(2):225 e 9.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref89) -
  84. [90][90] [Jasper H. The ten-twenty electrode system of the international federation. Electroencephalogr Clin Neurophysiol 1958;10:371 e 5.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref90) -
  85. [91][91] [Iivanainen J, Makinen AJ, Zetter R, Stenroos M, Ilmoniemi RJ, Parkkonen L. Spatial sampling of MEG and EEG based on generalized spatial-frequency analysis and optimal design. Neuroimage 2021;245:118747.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref91) -
  86. [92][92] [Ryynanen OR, Hyttinen JA, Laarne PH, Malmivuo JA. Effect of electrode density and measurement noise on the spatial resolution of cortical potential distribution. IEEE Trans Biomed Eng 2004;51(9):1547 e 54.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref92) -
  87. [93][93] [Michel CM, Brunet D. EEG source imaging: a practical review of the analysis steps. Front Neurol 2019;10:325.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref93) -
  88. [95][95] [Goldenholz DM, Ahlfors SP, Hamalainen MS, Sharon D, Ishitobi M, Vaina LM, et al. Mapping the signal-to-noise-ratios of cortical sources in magnetoencephalography and electroencephalography. Hum Brain Mapp 2009;30(4): 1077 e 86.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref95) -
  89. [96][96] [Sack A, Kadosh R, Schuhmann T, Moerel M, Walsh V, Goebel R. Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. J Cognit Neurosci 2009;21(2):207 e 21.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref96) -
  90. [97][97] [Lioumis P, Rosanova M. The role of neuronavigation in TMS-EEG studies: current applications and future perspectives. J Neurosci Methods 2022;380: 109677.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref97) -
  91. [98][98] [Ruohonen J, Karhu J. Navigated transcranial magnetic stimulation. Neurophysiol Clin 2010;40(1):7 e 17.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref98) -
  92. [99][99] [Hannula H, Ilmoniemi R. Basic principles of navigated TMS. In: Krieg S, editor. Navigated transcranial magnetic stimulation in neurosurgery. Springer; 2017.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref99) -
  93. [100][100] [Bashir S, Edwards D, Pascual-Leone A. Neuronavigation increases the physiologic and behavioral effects of low-frequency rTMS of primary motor cortex in healthy subjects. Brain Topogr 2011;24(1):54 e 64.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref100) -
  94. [101][101] [Cincotta M, Giovannelli F, Borgheresi A, Balestrieri F, Toscani L, Zaccara G, et al. Optically tracked neuronavigation increases the stability of hand-held focal coil positioning: evidence from "transcranial" magnetic stimulationinduced electrical fi eld measurements. Brain Stimul 2010;3(2):119 e 23.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref101) -
  95. [102][102] [Julkunen P, S € ais € anen L, Danner N, Niskanen E, Hukkanen T, Mervaala E, et al. Comparison of navigated and non-navigated transcranial magnetic stimulation for motor cortex mapping, motor threshold and motor evoked potentials. Neuroimage 2009;44(3):790 e 5.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref102) -
  96. [103][103] [Thielscher A, Opitz A, Windhoff M. Impact of the gyral geometry on the electric fi eld induced by transcranial magnetic stimulation. Neuroimage 2011;54(1):234 e 43.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref103) -
  97. [104][104] [Thut G, Veniero D, Romei V, Miniussi C, Schyns P, Gross J. Rhythmic TMS causes local entrainment of natural oscillatory signatures. Curr Biol 2011;21(14):1176 e 85.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref104) -
  98. [105][105] [Sarvas J. Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. Phys Med Biol 1987;32(1):11 e 22.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref105) -
  99. [106][106] [Nummenmaa A, Stenroos M, Ilmoniemi R, Okada Y, H € am € al € ainen M, Raij T. Comparison of spherical and anatomically realistic boundary element head models for transcranial magnetic stimulation navigation. Clin Neurophysiol 2013;124(10):1995 e 2007.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref106) -
  100. [107][107] [Thielscher A, Antunes A, Saturnino G. Field modeling for transcranial magnetic stimulation: a useful tool to understand the physiological effects of TMS? Annu Int Conf IEEE Eng Med Biol Soc 2015:222 e 5.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref107) -
  101. [108][108] [de Goede A, Ter Braack E, van Putten M. Accurate coil positioning is important for single and paired pulse TMS on the subject level. Brain Topogr 2018;31(6):917 e 30.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref108) -
  102. [109][109] [Harquel S, Bacle T, Beynel L, Marendaz C, Chauvin A, David O. Mapping dynamical properties of cortical microcircuits using robotized TMS and EEG: towards functional cytoarchitectonics. Neuroimage 2016;135:115 e 24.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref109) -
  103. [110][110] [Goldenholz D, Ahlfors S, H € am € al € ainen M, Sharon D, Ishitobi M, Vaina L, et al. Mapping the signal-to-noise-ratios of cortical sources in magnetoencephalography and electroencephalography. Hum Brain Mapp 2009;30(4): 1077 e 86.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref110) -
  104. [111][111] [Hui J, Zomorrodi R, Lioumis P, Salavati B, Rajji TK, Chen R, et al. Pharmacological mechanisms of interhemispheric signal propagation: a TMS-EEG study. Neuropsychopharmacology 2020;45(6):932 e 9.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref111) -
  105. [112][112] [Bertazzoli G, Esposito R, Mutanen T, Ferrari C, Ilmoniemi R, Miniussi C, et al. The impact of artifact removal approaches on TMS e EEG signal. Neuroimage 2021;239(118272):1 e 15.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref112) -
  106. [113][113] [Rosanova M, Casarotto S, Pigorini A, Canali P, Casali AG, Massimini M. Combining transcranial magnetic stimulation with electroencephalography to study human cortical excitability and effective connectivity. Neuronal Network Anal: Concepts and Experiment Approach 2012;67:435 e 57.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref113) -
  107. [114][114] [Komssi S, Huttunen J, Aronen H, Ilmoniemi R. EEG minimum-norm estimation compared with MEG dipole fi tting in the localization of somatosensory sources at S1. Clin Neurophysiol 2004;115(3):534 e 42.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref114) -
  108. [115][115] [VanRullen R. How to evaluate phase differences between trial groups in ongoing electrophysiological signals. Front Neurosci 2016;10(426):1 e 22.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref115) -
  109. [116][116] [Schaworonkow N, Caldana Gordon P, Belardinelli P, Ziemann U, Bergmann T, Zrenner C. m -Rhythm extracted with personalized EEG fi lters correlates with corticospinal excitability in real-time phase-triggered EEG-TMS. Front Neurosci 2018;12(954):1 e 6.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref116) -
  110. [117][117] [Rossini P, Barker A, Berardelli A, Caramia M, Caruso G, Cracco R, et al. Noninvasive 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 1994;91(2): 79 e 92.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref117) -
  111. [118][118] [Rothwell J, Hallett M, Berardelli A, Eisen A, Rossini P, Paulus W. Magnetic stimulation: motor evoked potentials. The international federation of clinical neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999;52: 97 e 103.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref118) -
  112. [119][119] [Reijonen J, Pitk € anen M, Kallioniemi E, Mohammadi A, Ilmoniemi R, Julkunen P. Spatial extent of cortical motor hotspot in navigated transcranial magnetic stimulation. J Neurosci Methods 2020;346(108893):1 e 9.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref119) -
  113. [120][120] [Julkunen P, S € ais € anen L, Hukkanen T, Danner N, K € on € onen M. Does secondscale intertrial interval affect motor evoked potentials induced by singlepulse transcranial magnetic stimulation? Brain Stimul 2012;5(4):526 e 32.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref120) -
  114. [121][121] [Pellicciari M, Miniussi C, Ferrari C, Koch G, Bortoletto M. Ongoing cumulative effects of single TMS pulses on corticospinal excitability: an intra- and interblock investigation. Clin Neurophysiol 2016;127(1):621 e 8.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref121) -
  115. [122][122] [Hassanzahraee M, Zoghi M, Jaberzadeh S. Longer transcranial magnetic stimulation intertrial interval increases size, reduces variability, and improves the reliability of motor evoked potentials. Brain Connect 2019;9(10): 770 e 6.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref122) -
  116. [123][123] [Pitk € anen M, Kallioniemi E, Julkunen P. Effect of inter-train interval on the induction of repetition suppression of motor-evoked potentials using transcranial magnetic stimulation. PLoS One 2017;12(7):1 e 10.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref123) -
  117. [124][124] [Tran D, McNair N, Harris J, Livesey E. Expected TMS excites the motor system less effectively than unexpected stimulation. Neuroimage 2021;226(117541):1 e 10.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref124) -
  118. [125][125] [Awiszus F. Fast estimation of transcranial magnetic stimulation motor threshold: is it safe? Brain Stimul 2011;4(1):58 e 9.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref125) -
  119. [126][126] [Capozio A, Chakrabarty S, Astill S. The effect of sound and stimulus expectation on transcranial magnetic stimulation-elicited motor evoked potentials. Brain Topogr 2021;34(6):720 e 30.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref126) -
  120. [127][127] [Brown KE, Lohse KR, Mayer IMS, Strigaro G, Desikan M, Casula EP, et al. The reliability of commonly used electrophysiology measures. Brain Stimul 2017;10(6):1102 e 11.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref127) -
  121. [128][128] [Stewart L, Walsh V, Rothwell J. Motor and phosphene thresholds: a transcranial magnetic stimulation correlation study. Neuropschologia 2001;39(4): 415 e 9.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref128) -
  122. [129][129] [Deblieck C, Thompson B, Iacoboni M, Wu AD. Correlation between motor and phosphene thresholds: a transcranial magnetic stimulation study. Hum Brain Mapp 2008;29(6):662 e 70.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref129) -
  123. [130][130] [Stokes M, Chambers C, Gould I, Henderson T, Janko N, Allen N, et al. Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. J Neurophysiol 2005;94(6):4520 e 7.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref130) -
  124. [131][131] [Westin G, Bassi B, Lisanby S, Luber B. Determination of motor threshold using visual observation overestimates transcranial magnetic stimulation dosage: safety implications. Clin Neurophysiol 2014;125(1):142 e 7.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref131) -
  125. [132][132] [Kammer T, Puls K, Strasburger H, Hill N, Wichmann F. Transcranial magnetic stimulation in the visual system. I. The psychophysics of visual suppression. Exp Brain Res 2005;160(1):118 e 28.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref132) -
  126. [133][133] [Kammer T, Puls K, Erb M, Grodd W. Transcranial magnetic stimulation in the visual system. II. Characterization of induced phosphenes and scotomas. Exp Brain Res 2005;160(1):129 e 40.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref133) -
  127. [134][134] [Taylor P, Walsh V, Eimer M. The neural signature of phosphene perception. Hum Brain Mapp 2010;31(9):1408 e 17.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref134) -
  128. [135][135] [Marg E, Rudiak D. Phosphenes induced by magnetic stimulation over the occipital brain: description and probable site of stimulation. Optom Vis Sci 1994;71(5):301 e 11.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref135) -
  129. [136][136] [Antal A, Nitsche M, Kincses T, Lampe C, Paulus W. No correlation between moving phosphene and motor thresholds: a transcranial magnetic stimulation study. Neuroreport 2004;15(2):297 e 302.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref136) -
  130. [137][137] [Romei V, Gross J, Thut G. On the role of prestimulus alpha rhythms over occipito-parietal areas in visual input regulation: correlation or causation? J Neurosci 2010;30(25):8692 e 7.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref137) -
  131. [138][138] [Zazio A, Bortoletto M, Ruzzoli M, Miniussi C, Veniero D. Perceptual and physiological consequences of dark adaptation: a TMS-EEG study. Brain Topogr 2019;32(5):773 e 82.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref138) -
  132. [139][139] [Janssen A, Oostendorp T, Stegeman D. The coil orientation dependency of the electric fi eld induced by TMS for M1 and other brain areas. J NeuroEng Rehabil 2015;12(47):1 e 13.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref139) -
  133. [140][140] [Janssen A, Oostendorp T, Stegeman D. The effect of local anatomy on the electric fi eld induced by TMS: evaluation at 14 different target sites. Med Biol Eng Comput 2014;52(10):873 e 83.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref140) -
  134. [141][141] [Julkunen P, Saisanen L, Danner N, Awiszus F, Kononen M. Within-subject effect of coil-to-cortex distance on cortical electric fi eld threshold and motor evoked potentials in transcranial magnetic stimulation. J Neurosci Methods 2012;206(2):158 e 64.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref141) -
  135. [142][142] [Casali AG, Casarotto S, Rosanova M, Mariotti M, Massimini M. General indices to characterize the electrical response of the cerebral cortex to TMS. Neuroimage 2010;49(2):1459 e 68.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref142) -
  136. [143][143] [K € ahk € onen S, Wilenius J, Komssi S, Ilmoniemi R. Distinct differences in cortical reactivity of motor and prefrontal cortices to magnetic stimulation. Clin Neurophysiol 2004;115(3):583 e 8.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref143) -
  137. [144][144] [Komssi S, Savolainen P, Heiskala J, K € ahk € onen S. Excitation threshold of the motor cortex estimated with transcranial magnetic stimulation electroencephalography. Neuroreport 2007;18(1):13 e 6.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref144) -
  138. [145][145] [Raf fi n E, Harquel S, Passera B, Chauvin A, Bougerol T, David O. Probing regional cortical excitability via input-output properties using transcranial magnetic stimulation and electroencephalography coupling. Hum Brain Mapp 2020;41(10):2741 e 61.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref145) -
  139. [146][146] [Schaworonkow N, Triesch J, Ziemann U, Zrenner C. EEG-triggered TMS reveals stronger brain state-dependent modulation of motor evoked potentials at weaker stimulation intensities. Brain Stimul 2019;12(1):110 e 8.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref146) -
  140. [147][147] [Zmeykina E, Mittner M, Paulus W, Turi Z. Weak rTMS-induced electric fi elds produce neural entrainment in humans. Sci Rep 2020;10(1):1 e 16. 11994.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref147) -
  141. [148][148] [K € ahk € onen S, Komssi S, Wilenius J, Ilmoniemi R. Prefrontal transcranial magnetic stimulation produces intensity-dependent EEG responses in humans. Neuroimage 2005;24(4):955 e 60.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref148) -
  142. [149][149] [Muggleton NG, Juan CH, Cowey A, Walsh V. Human frontal eye fi elds and visual search. J Neurophysiol 2003;89(6):3340 e 3.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref149) -
  143. [150][150] [O'Shea J, Muggleton NG, Cowey A, Walsh V. Timing of target discrimination in human frontal eye fi elds. J Cognit Neurosci 2004;16(6):1060 e 7.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref150) -
  144. [151][151] [Juan CH, Muggleton NG, Tzeng OJ, Hung DL, Cowey A, Walsh V. Segregation of visual selection and saccades in human frontal eye fi elds. Cerebr Cortex 2008;18(10):2410 e 5.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref151) -
  145. [152][152] [Silvanto J, Lavie N, Walsh V. Stimulation of the human frontal eye fi elds modulates sensitivity of extrastriate visual cortex. J Neurophysiol 2006;96(2):941 e 5.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref152) -
  146. [153][153] [Voineskos A, Farzan F, Barr M, Lobaugh N, Mulsant B, Chen R, et al. The role of the corpus callosum in transcranial magnetic stimulation induced interhemispheric signal propagation. Biol Psychiatr 2010;68(9):825 e 31.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref153) -
  147. [154][154] [Kallioniemi E, K € on € onen M, Julkunen P. Repeatability of functional anisotropy in navigated transcranial magnetic stimulation -coil-orientation versus response. Neuroreport 2015;26(9):515 e 21.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref154) -
  148. [155][155] [Belardinelli P, Biabani M, Blumberger D, Bortoletto M, Casarotto S, David O, et al. Reproducibility in TMS-EEG studies: a call for data sharing, standard procedures and effective experimental control. Brain Stimul 2019;12(3): 787 e 90.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref155) -
  149. [156][156] [Conde V, Tomasevic L, Akopian I, Stanek K, Saturnino G, Thielscher A, et al. The non-transcranial TMS-evoked potential is an inherent source of ambiguity in TMS-EEG studies. Neuroimage 2019;85:300 e 12.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref156) -
  150. [157][157] [Siebner H, Conde V, Tomasevic L, Thielscher A, Bergmann T. Distilling the essence of TMS-evoked EEG potentials (TEPs): a call for securing mechanistic speci fi city and experimental rigor. Brain Stimul 2019;12(4):1051 e 4.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref157) -
  151. [158][158] [de Graaf T, Sack A. Null results in TMS: from absence of evidence to evidence of absence. Neurosci Biobehav Rev 2011;35(3):871 e 7.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref158) -
  152. [159][159] [Russo S, Sarasso S, Puglisi GE, Dal Palù D, Pigorini A, Casarotto S, et al. TAAC TMS Adaptable Auditory Control: a universal tool to mask TMS clicks. J Neurosci Methods 2022;370:109491.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref159) -
  153. [160][160] [Pellegrino G, Schuler AL, Arcara G, Di Pino G, Piccione F, Kobayashi E. Resting state network connectivity is attenuated by fMRI acoustic noise. Neuroimage 2022;247:118791.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref160) -
  154. [161][161] [Sarasso S, D'Ambrosio S, Fecchio M, Casarotto S, Vigan o A, Landi C, et al. Local sleep-like cortical reactivity in the awake brain after focal injury. Brain 2020;143(12):3672 e 84.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref161) -
  155. [162][162] [ter Braack E, de Vos C, van Putten M. Masking the auditory evoked potential in TMS-EEG: a comparison of various methods. Brain Topogr 2015;28(3): 520 e 8.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref162) -
  156. [164][164] [Ohbayashi W, Kakigi R, Nakata H. Effects of white noise on event-related potentials in somatosensory Go/No-go paradigms. Neuroreport 2017;28(13):788 e 92.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref164) -
  157. [165][165] [Koponen LM, Goetz SM, Tucci DL, Peterchev AV. Sound comparison of seven TMS coils at matched stimulation strength. Brain Stimul 2020;13(3):873 e 80.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref165) -
  158. [166][166] [Ruohonen J, Ollikainen M, Nikouline V, Virtanen J, Ilmoniemi R. Coil design for real and sham transcranial magnetic stimulation. IEEE Trans Biomed Eng 2000;47(2):145 e 8.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref166) -
  159. [167][167] [Gordon PC, Jovellar DB, Song Y, Zrenner C, Belardinelli P, Siebner HR, et al. Recording brain responses to TMS of primary motor cortex by EEG - utility of an optimized sham procedure. Neuroimage 2021;245:118708.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref167) -
  160. [168][168] [Rossi S, Ferro M, Cincotta M, Ulivelli M, Bartalini S, Miniussi C, et al. A real electro-magnetic placebo (REMP) device for sham transcranial magnetic stimulation (TMS). Clin Neurophysiol 2007;118(3):709 e 16.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref168) -
  161. [169][169] [Amaro Jr E, Barker GJ. Study design in fMRI: basic principles. Brain Cognit 2006;60(3):220 e 32.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref169) -
  162. [170][170] [Premoli I, Castellanos N, Rivolta D, Belardinelli P, Bajo R, Zipser C, et al. TMSEEG signatures of GABAergic neurotransmission in the human cortex. J Neurosci 2014;34(16):5603 e 12.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref170) -
  163. [172][172] [Vernet M, Bashir S, Yoo W, Perez J, Najib U, Pascual-Leone A. Insights on the neural basis of motor plasticity induced by theta burst stimulation from TMS-EEG. Eur J Neurosci 2013;37(4):598 e 606.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref172) -
  164. [173][173] [Leodori G, Fabbrini A, De Bartolo MI, Costanzo M, Asci F, Palma V, et al. Cortical mechanisms underlying variability in intermittent theta-burst stimulation-induced plasticity: a TMS-EEG study. Clin Neurophysiol 2021;132(10):2519 e 31.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref173) -
  165. [174][174] [Rocchi L, Ibanez J, Benussi A, Hannah R, Rawji V, Casula E, et al. Variability and predictors of response to continuous theta burst stimulation: a TMS-EEG study. Front Neurosci 2018;12:400.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref174) -
  166. [175][175] [Morishima Y, Akaishi R, Yamada Y, Okuda J, Toma K, Sakai K. Task-speci fi c signal transmission from prefrontal cortex in visual selective attention. Nat Neurosci 2009;12(1):85 e 91.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref175) -
  167. [176][176] [Meteyard L, Holmes N. Tms smart - scalp mapping of annoyance ratings and twitches caused by Transcranial Magnetic Stimulation. J Neurosci Methods 2018;299:34 e 44.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref176) -
  168. [177][177] [Bergmann T. Brain state-dependent brain stimulation. Front Psychol 2018;9(2108):1 e 4.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref177) -
  169. [178][178] [Karabanov A, Thielscher A, Siebner HR. Transcranial brain stimulation: closing the loop between brain and stimulation. Curr Opin Neurol 2016;29(4):397 e 404.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref178) -
  170. [179][179] [Esposito R, Bortoletto M, Miniussi C. Integrating TMS, EEG, and MRI as an approach for studying brain connectivity. Neuroscientist 2020;26(5 e 6): 471 e 86.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref179) -
  171. [180][180] [Bergmann TO, Lieb A, Zrenner C, Ziemann U. Pulsed facilitation of corticospinal excitability by the sensorimotor mu-alpha rhythm. J Neurosci 2019;39(50):10034 e 43.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref180) -
  172. [181][181] [Zrenner C, Desideri D, Belardinelli P, Ziemann U. Real-time EEG-de fi ned excitability states determine ef fi cacy of TMS-induced plasticity in human motor cortex. Brain Stimul 2018;11(2):374 e 89.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref181) -
  173. [182][182] [Karabanov AN, Madsen KH, Krohne LG, Siebner HR. Does pericentral murhythm "power" corticomotor excitability? - a matter of EEG perspective. Brain Stimul 2021;14(3):713 e 22.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref182) -
  174. [183][183] [Madsen KH, Karabanov AN, Krohne LG, Safeldt MG, Tomasevic L, Siebner HR. No trace of phase: corticomotor excitability is not tuned by phase of pericentral mu-rhythm. Brain Stimul 2019;12(5):1261 e 70.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref183) -
  175. [184][184] [Bergmann TO, Born J. Phase-amplitude coupling: a general mechanism for memory processing and synaptic plasticity? Neuron 2018;97(1):10 e 3.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref184) -
  176. [185][185] [Schaworonkow N, Nikulin VV. Is sensor space analysis good enough? Spatial patterns as a tool for assessing spatial mixing of EEG/MEG rhythms. Neuroimage 2022;253:119093.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref185) -
  177. [186][186] [Ilmoniemi RJ, Hernandez-Pavon JC, Makela NN, Metsomaa J, Mutanen TP, Stenroos M, et al. Dealing with artifacts in TMS-evoked EEG. Conf Proc IEEE Eng Med Biol Soc 2015;2015:230 e 3.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref186) -
  178. [187][187] [Rogasch N, Sullivan C, Thomson R, Rose N, Bailey N, Fitzgerald P, et al. Analysing concurrent transcranial magnetic stimulation and electroencephalographic data: a review and introduction to the open-source TESA software. Neuroimage 2017;147:934 e 51.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref187) -
  179. [188][188] [Vernet M, Thut G. Electroencephalography during transcranial magnetic stimulation: current modus operandi. In: Rotenberg A, Horvath J, PascualLeone A, editors. Transcranial magnetic stimulation. Neuromethods. New York, NY: Humana Press; 2014.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref188) -
  180. [189][189] [Litvak V, Komssi S, Scherg M, Hoechstetter K, Classen J, Zaaroor M, et al. Artifact correction and source analysis of early electroencephalographic responses evoked by transcranial magnetic stimulation over primary motor cortex. Neuroimage 2007;37(1):56 e 70.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref189) -
  181. [190][190] [Julkunen P, P € a € akk € onen A, Hukkanen T, K € on € onen M, Tiihonen P, Vanhatalo S, et al. Ef fi cient reduction of stimulus artefact in TMS-EEG by epithelial shortcircuiting by mini-punctures. Clin Neurophysiol 2008;119(2):475 e 81.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref190) -
  182. [191][191] [Picton T, Hillyard S. Cephalic skin potentials in electroencephalography. Electroencephalogr Clin Neurophysiol 1972;33(4):419 e 24.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref191) -
  183. [192][192] Johnson J. Thermal agitation of electricity in conductors. Nature 1927;119: 50 e 1. -
  184. [194][194] [Burbank D, Webster J. Reducing skin potential motion artefact by skin abrasion. Med Biol Eng Comput 1978;16(1):31 e 8.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref194) -
  185. [195][195] [Li B, Virtanen J, Oeltermann A, Schwarz C, Giese M, Ziemann U, et al. Lifting the veil on the dynamics of neuronal activities evoked by transcranial magnetic stimulation. Elife 2017;6(e30552):1 e 22.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref195) -
  186. [196][196] [de Talhouet H, Webster J. The origin of skin-stretch-caused motion artifacts under electrodes. Physiol Meas 1996;17(2):81 e 93.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref196) -
  187. [197][197] [Ruddy K, Woolley D, Mantini D, Balsters J, Enz N, Wenderoth N. Improving the quality of combined EEG-TMS neural recordings: introducing the coil spacer. J Neurosci Methods 2018;294:34 e 9.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref197) -
  188. [198][198] [Berg P, Scherg M. Dipole models of eye movements and blinks. Electroencephalogr Clin Neurophysiol 1991;79(1):36 e 44.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref198) -
  189. [199][199] [Lins O, Picton T, Berg P, Scherg M. Ocular artifacts in recording EEGs and event-related potentials. II: source dipoles and source components. Brain Topogr 1993;6(1):65 e 78.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref199) -
  190. [200][200] [Korhonen RJ, Hernandez-Pavon JC, Metsomaa J, M € aki H, Ilmoniemi RJ, Sarvas J. Removal of large muscle artifacts from transcranial magnetic stimulation-evoked EEG by independent component analysis. Med Biol Eng Comput 2011;49(4):397 e 407.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref200) -
  191. [201][201] [Paus T, Sipila P, Strafella A. Synchronization of neuronal activity in the human primary motor cortex by transcranial magnetic stimulation: an EEG study. J Neurophysiol 2001;86(4):1983 e 90.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref201) -
  192. [202][202] [Friedman B, Thayer J. Facial muscle activity and EEG recordings: redundancy analysis. Electroencephalogr Clin Neurophysiol 1991;79(5):358 e 60.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref202) -
  193. [203][203] [Hernandez-Pavon JC, Metsomaa J, Mutanen T, Stenroos M, M € aki H, Ilmoniemi RJ, et al. Uncovering neural independent components from highly artifactual TMS-evoked EEG data. J Neurosci Methods 2012;209(1):144 e 57.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref203) -
  194. [204][204] [Tiitinen H, Virtanen J, Ilmoniemi R, Kamppuri J, Ollikainen M, Ruohonen J, et al. Separation of contamination caused by coil clicks from responses elicited by transcranial magnetic stimulation. Clin Neurophysiol 1999;110(5): 982 e 5.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref204) -
  195. [205][205] [Ross JM, Sarkar M, Keller CJ. Experimental suppression of transcranial magnetic stimulation-electroencephalography sensory potentials. Hum Brain Mapp 2022;43(17):5141 e 53.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref205) -
  196. [206][206] [Massimini M, Ferrarelli F, Esser SK, Riedner BA, Huber R, Murphy M, et al. Triggering sleep slow waves by transcranial magnetic stimulation. Proc Natl Acad Sci U S A 2007;104(20):8496 e 501.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref206) -
  197. [207][207] [Mizukami H, Kakigi R, Nakata H. Effects of stimulus intensity and auditory white noise on human somatosensory cognitive processing: a study using event-related potentials. Exp Brain Res 2019;237(2):521 e 30.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref207) -
  198. [208][208] [Koponen LM, Goetz SM, Peterchev AV. Double-containment coil with enhanced winding mounting for transcranial magnetic stimulation with reduced acoustic noise. IEEE Trans Biomed Eng 2021;68(7):2233 e 40.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref208) -
  199. [209][209] [Gordon P, Desideri D, Belardinelli P, Zrenner C, Ziemann U. Comparison of cortical EEG responses to realistic sham versus real TMS of human motor cortex. Brain Stimul 2018;11(6):1322 e 30.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref209) -
  200. [210][210] [Kappenman ES, Luck SJ. The effects of electrode impedance on data quality and statistical signi fi cance in ERP recordings. Psychophysiology 2010;47(5): 888 e 904.](http://refhub.elsevier.com/S1935-861X(23)01696-0/sref210) -

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Authors
Hernandez-Pavon, J. C., Veniero, D., Bergmann, T. O., Belardinelli, P., Bortoletto, M., Casarotto, S., Casula, E. P., Farzan, F., Fecchio, M., Julkunen, P., Kallioniemi, E., Lioumis, P., Metsomaa, J., Miniussi, C., Mutanen, T. P., Rocchi, L., Rogasch, N. C., Shafi, M. M., Siebner, H. R., Thut, G., Zrenner, C., Ziemann, U., & Ilmoniemi, R. J.
Affiliations
  • Northwestern University (US)
  • University of Nottingham (GB)
  • Leibniz Institute for Resilience Research (DE)
  • University of Trento (IT)
  • Centro San Giovanni di Dio Fatebenefratelli (IT)
  • University of Milan (IT)
  • University of Rome Tor Vergata (IT)
  • Simon Fraser University (CA)
  • Massachusetts General Hospital (US)
  • University of Eastern Finland (FI)
  • New Jersey Institute of Technology (US)
  • University of Helsinki (FI)
  • University of Copenhagen (DK)
  • University of Cagliari (IT)
  • South Australian Health and Medical Research Institute (AU)
  • Beth Israel Deaconess Medical Center (US)
  • University of Glasgow (GB)
  • Centre for Addiction and Mental Health (CA)
  • Hertie Institute for Clinical Brain Research (DE)
Corresponding author
Veniero, Domenica
ORCID
Venue
Brain Stimulation
Publisher
Elsevier BV
Published
2023-03
Volume
16
Issue
2
Pages
567-593
ISSN
  • 1876-4754 (ISSN-L)
  • 1935-861X
DOI
10.1016/j.brs.2023.02.009
OpenAlex
W4321487178
Cited by
238
References
12
Citations by year
2026: 72 · 2025: 74 · 2024: 64 · 2023: 28
FWCI
6.21
Type
journal article
Language
en
Open access
Licence
Locations
  • Brain stimulation (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by-nc-nd)
  • ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion, other-oa)
  • Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
  • Informationszentrum Lebenswissenschaften (ZB MED) (submittedVersion, cc-by-nc-nd)
  • UNICA IRIS Institutional Research Information System (University of Cagliari) (submittedVersion, other-oa)
  • Institutional Research Information System (Università degli Studi di Trento) (submittedVersion, cc-by-nc-nd)
  • Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by-nc-nd)
  • Aaltodoc (Aalto University) (submittedVersion, cc-by-nc-nd)
  • Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Työväentutkimus Vuosikirja (submittedVersion)
  • Repository@Nottingham (University of Nottingham) (submittedVersion)
Funders
  • Academy of Finland (321631)
  • Lundbeckfonden (R186-2015-2138)
  • H. Lundbeck A/S (R186-2015-2138)
Topics
  • Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › EEG and Brain-Computer Interfaces
  • Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
Keywords
TMS-EEG, transcranial magnetic stimulation, EEG, method standardization, artifact removal, auditory input, somatosensory input, cortical reactivity, cortical connectivity, reproducibility
MeSH terms
Data Collection, Electroencephalography, Evoked Potentials, Humans, Reproducibility of Results, Transcranial Magnetic Stimulation

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