Changes of oscillatory brain activity induced by repetitive transcranial magnetic stimulation of the left dorsolateral prefrontal cortex in healthy subjects

NeuroImage

Volumn 88, Issue , 2014, Pages 91-99

  Woźniak Kwaśniewska, Agata ^a   Szekely, David ^a,b   Aussedat, Pierre ^a   Bougerol, Thierry ^b   David, Olivier ^a,b  

^a GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^b GRENOBLE UNIVERSITY HOSPITAL   (France)

Author keywords

Dorsolateral prefrontal cortex; EEG; Methods; RTMS

Indexed keywords

ADULT; ALPHA RHYTHM; ARTICLE; BETA RHYTHM; CONTROLLED STUDY; DELTA RHYTHM; ELECTRODE; ELECTROENCEPHALOGRAM; FEMALE; FOURIER TRANSFORMATION; GAMMA RHYTHM; HUMAN; HUMAN EXPERIMENT; MALE; MOOD CHANGE; NORMAL HUMAN; OSCILLATION; PARAMETRIC TEST; PREFRONTAL CORTEX; PRIORITY JOURNAL; REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION; SCALP; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION; ELECTROENCEPHALOGRAPHY; MIDDLE AGED; PHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADULT; ELECTROENCEPHALOGRAPHY; FEMALE; HEALTHY VOLUNTEERS; HUMANS; MALE; MIDDLE AGED; PREFRONTAL CORTEX; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84892898987     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.11.029     Document Type: Article

References (58)

1. Angrilli A., Spironelli C., Elbert T., Crow T.J., Marano G., Stegagno L. Schizophrenia as failure of left hemispheric dominance for the phonological component of language. PLoS ONE 2009, 4:e4507.
2. Arai N., Okabe S., Furubayashi T., Terao Y., Yuasa K., Ugawa Y. Comparison between short train, monophasic and biphasic repetitive transcranial magnetic stimulation (rTMS) of the human motor cortex. Clin. Neurophysiol. 2005, 116:605-613.
3. Arai N., Okabe S., Furubayashi T., Mochizuki H., Iwata N.K., Hanajima R., Terao Y., Ugawa Y. Differences in after-effect between monophasic and biphasic high-frequency rTMS of the human motor cortex. Clin. Neurophysiol. 2007, 118:2227-2233.
4. Avery D.H., Holtzheimer P.E., Fawaz W., Russo J., Neumaier J., Dunner D.L., Haynor D.R., Claypoole K.H., Wajdik C., Roy-Byrne P. A controlled study of repetitive transcranial magnetic stimulation in medication-resistant major depression. Biol. Psychiatry 2006, 59:187-194.
5. Benali A., Trippe J., Weiler E., Mix A., Petrasch-Parwez E., Girzalsky W., Eysel U.T., Erdmann R., Funke K. Theta-burst transcranial magnetic stimulation alters cortical inhibition. J. Neurosci. 2011, 31:1193-1203.
6. Bey A., Leue S., Wienbruch C. A neuronal network model for simulating the effects of repetitive transcranial magnetic stimulation on local field potential power spectra. PLoS ONE 2012, 7:e49097.
7. Brignani D., Manganotti P., Rossini P.M., Miniussi C. Modulation of cortical oscillatory activity during transcranial magnetic stimulation. Hum. Brain Mapp. 2008, 29:603-612.
8. Brigo F., Storti M., Nardone R., Fiaschi A., Bongiovanni L.G., Tezzon F., Manganotti P. Transcranial magnetic stimulation of visual cortex in migraine patients: a systematic review with meta-analysis. J. Headache Pain 2012, 13:339-349.
9. Buzsáki G. Rhythms of the Brain 2006, Oxford University Press, New York.
10. Buzsáki G., Wang X.-J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 2012, 35:203-225.
11. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.-H., Moore C.I. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 2009, 459:663-667.
12. Chen R., Yung D., Li J.-Y. Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. J. Neurophysiol. 2003, 89:1256-1264.
13. Classen J., Stefan K. Changes in TMS measures induced by repetitive TMS. The Oxford Handbook of Transcranial Stimulation 2008, 185-200. Oxford University Press, New York. E.M. Wassermann, C. Epstein, U. Ziemann, V. Walsh, T. Paus, S.H. Lisanby (Eds.).
14. Contreras D., Steriade M. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J. Neurosci. 1995, 15:604-622.
15. Dell'Osso B., Mundo E., D'Urso N., Pozzoli S., Buoli M., Ciabatti M., Rosanova M., Massimini M., Bellina V., Mariotti M., Carlo Altamura A. Augmentative repetitive navigated transcranial magnetic stimulation (rTMS) in drug-resistant bipolar depression. Bipolar Disord. 2009, 11:76-81.
16. Delorme A., Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 2004, 134:9-21.
17. Di Lazzaro V., Dileone M., Pilato F., Capone F., Musumeci G., Ranieri F., Ricci V., Bria P., Di Iorio R., de Waure C., Pasqualetti P., Profice P. Modulation of motor cortex neuronal networks by rTMS: comparison of local and remote effects of six different protocols of stimulation. J. Neurophysiol. 2011, 105:2150-2156.
18. Farzan F., Barr M.S., Wong W., Chen R., Fitzgerald P.B., Daskalakis Z.J. Suppression of gamma-oscillations in the dorsolateral prefrontal cortex following long interval cortical inhibition: a TMS-EEG study. Neuropsychopharmacology 2009, 34:1543-1551.
19. Fitzgerald P.B., Brown T.L., Marston N.A.U., Daskalakis Z.J., de Castella A., Kulkarni J. Transcranial magnetic stimulation in the treatment of depression: a double-blind, placebo-controlled trial. Arch. Gen. Psychiatry 2003, 60:1002-1008.
20. Fitzgerald P.B., McQueen S., Herring S., Hoy K., Segrave R., Kulkarni J., Daskalakis Z.J. A study of the effectiveness of high-frequency left prefrontal cortex transcranial magnetic stimulation in major depression in patients who have not responded to right-sided stimulation. Psychiatry Res. 2009, 169:12-15.
21. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 2005, 9:474-480.
22. Friston K., Harrison L., Daunizeau J., Kiebel S., Phillips C., Trujillo-Barreto N., Henson R., Flandin G., Mattout J. Multiple sparse priors for the M/EEG inverse problem. NeuroImage 2008, 39:1104-1120.
23. Fuggetta G., Pavone E.F., Fiaschi A., Manganotti P. Acute modulation of cortical oscillatory activities during short trains of high-frequency repetitive transcranial magnetic stimulation of the human motor cortex: a combined EEG and TMS study. Hum. Brain Mapp. 2008, 29:1-13.
24. Gasser T., Verleger R., Bächer P., Sroka L. Development of the EEG of school-age children and adolescents. I. Analysis of band power. Electroencephalogr. Clin. Neurophysiol. 1988, 69:91-99.
25. George M.S. Transcranial magnetic stimulation for the treatment of depression. Expert Rev. Neurother. 2010, 10:1761-1772.
26. George M.S., Wassermann E.M., Williams W.A., Callahan A., Ketter T.A., Basser P., Hallett M., Post R.M. Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression. Neuroreport 1995, 6:1853-1856.
27. Graf T., Engeler J., Achermann P., Mosimann U.P., Noss R., Fisch H.U., Schlaepfer T.E. High frequency repetitive transcranial magnetic stimulation (rTMS) of the left dorsolateral cortex: EEG topography during waking and subsequent sleep. Psychiatry Res. 2001, 107:1-9.
28. Griskova I., Ruksenas O., Dapsys K., Herpertz S., Höppner J. The effects of 10Hz repetitive transcranial magnetic stimulation on resting EEG power spectrum in healthy subjects. Neurosci. Lett. 2007, 419:162-167.
29. Grossheinrich N., Rau A., Pogarell O., Hennig-Fast K., Reinl M., Karch S., Dieler A., Leicht G., Mulert C., Sterr A., Padberg F. Theta burst stimulation of the prefrontal cortex: safety and impact on cognition, mood, and resting electroencephalogram. Biol. Psychiatry 2009, 65:778-784.
30. Hallett M. Transcranial magnetic stimulation: a primer. Neuron 2007, 55:187-199.
31. Hasan A., Falkai P., Wobrock T. Transcranial brain stimulation in schizophrenia: targeting cortical excitability, connectivity and plasticity. Curr. Med. Chem. 2013, 20:405-413.
32. Hayashi T., Ohnishi T., Okabe S., Teramoto N., Nonaka Y., Watabe H., Imabayashi E., Ohta Y., Jino H., Ejima N., Sawada T., Iida H., Matsuda H., Ugawa Y. Long-term effect of motor cortical repetitive transcranial magnetic stimulation induces. Ann. Neurol. 2004, 56:77-85.
33. Herwig U., Padberg F., Unger J., Spitzer M., Schönfeldt-Lecuona C. Transcranial magnetic stimulation in therapy studies: examination of the reliability of "standard" coil positioning by neuronavigation. Biol. Psychiatry 2001, 50:58-61.
34. Homan P., Kindler J., Hauf M., Hubl D., Dierks T. Cerebral blood flow identifies responders to transcranial magnetic stimulation in auditory verbal hallucinations. Transl. Psychiatry 2012, 2:e189.
35. Hoogendam J.M., Ramakers G.M.J., Di Lazzaro V. Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul. 2010, 3:95-118.
36. Houdayer E., Degardin A., Cassim F., Bocquillon P., Derambure P., Devanne H. The effects of low- and high-frequency repetitive TMS on the input/output properties of the human corticospinal pathway. Exp. Brain Res. 2008, 187:207-217.
37. Huang Y.-Z., Edwards M.J., Rounis E., Bhatia K.P., Rothwell J.C. Theta burst stimulation of the human motor cortex. Neuron 2005, 45:201-206.
38. Hummel F.C., Celnik P., Pascual-Leone A., Fregni F., Byblow W.D., Buetefisch C.M., Rothwell J., Cohen L.G., Gerloff C. Controversy: Noninvasive and invasive cortical stimulation show efficacy in treating stroke patients. Brain Stimul. 2008, 1:370-382.
39. Ilmoniemi R.J., Virtanen J., Ruohonen J., Karhu J., Aronen H.J., Näätänen R., Katila T. Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 1997, 8:3537-3540.
40. Jung S.H., Kim Y.K., Kim S.E., Paik N.-J. Prediction of motor function recovery after subcortical stroke: case series of activation PET and TMS studies. Ann. Rehabil. Med. 2012, 36:501.
41. Litvak V., Friston K. Electromagnetic source reconstruction for group studies. NeuroImage 2008, 42:1490-1498.
42. Magis D., Jensen R., Schoenen J. Neurostimulation therapies for primary headache disorders: present and future. Curr. Opin. Neurol. 2012, 25:269-276.
43. Mattout J., Henson R.N., Friston K.J. Canonical source reconstruction for MEG. Comput. Intell. Neurosci. 2007, 67613.
44. Noh N.A., Fuggetta G., Manganotti P., Fiaschi A. Long lasting modulation of cortical oscillations after continuous theta burst transcranial magnetic stimulation. PLoS ONE 2012, 7:e35080.
45. Okamura H., Jing H., Takigawa M. EEG modification induced by repetitive transcranial magnetic stimulation. J. Clin. Neurophysiol. 2001, 18:318-325.
46. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
47. Onton J., Westerfield M., Townsend J., Makeig S. Imaging human EEG dynamics using independent component analysis. Neurosci. Biobehav. Rev. 2006, 30:808-822.
48. Pascual-Leone A., Rubio B., Pallardó F., Catalá M.D. Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. Lancet 1996, 348:233-237.
49. Richieri R., Boyer L., Farisse J., Colavolpe C., Mundler O., Lancon C., Guedj E. Predictive value of brain perfusion SPECT for rTMS response in pharmacoresistant depression. Eur. J. Nucl. Med. Mol. Imaging 2011, 38:1715-1722.
50. Romero J.R., Anschel D., Sparing R., Gangitano M., Pascual-Leone A. Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex. Clin. Neurophysiol. 2002, 113:101-107.
51. Rosanova M., Casali A., Bellina V., Resta F., Mariotti M., Massimini M. Natural frequencies of human corticothalamic circuits. J. Neurosci. 2009, 29:7679-7685.
52. Rossi S., Hallett M., Rossini P.M., Pascual-Leone A., Safety of TMS Consensus Group Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Presented at the Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology 2009, 2008-2039.
53. Schutter D.J., van Honk J., d'Alfonso A.A., Postma A., de Haan E.H. Effects of slow rTMS at the right dorsolateral prefrontal cortex on EEG asymmetry and mood. Neuroreport 2001, 12:445-447.
54. Spironelli C., Angrilli A., Calogero A., Stegagno L. Delta EEG band as a marker of left hypofrontality for language in schizophrenia patients. Schizophr. Bull. 2011, 37:757-767.
55. Taylor J.L., Loo C.K. Stimulus waveform influences the efficacy of repetitive transcranial magnetic stimulation. J. Affect. Disord. 2007, 97:271-276.
56. Thielscher A., Reichenbach A., Uǧurbil K., Uludaǧ K. The cortical site of visual suppression by transcranial magnetic stimulation. Cereb. Cortex 2010, 20:328-338.
57. Thut G., Pascual-Leone A. A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience. Brain Topogr. 2010, 22:219-232.
58. Veniero D., Brignani D., Thut G., Miniussi C. Alpha-generation as basic response-signature to transcranial magnetic stimulation (TMS) targeting the human resting motor cortex: a TMS/EEG co-registration study. Psychophysiology 2011, 48:1381-1389.