Potentiation of short-latency cortical responses by high-frequency repetitive transcranial magnetic stimulation

Journal of Neurophysiology

Volumn 104, Issue 3, 2010, Pages 1578-1588

  Veniero, Domenica ^a,b   Maioli, Claudio ^a   Miniussi, Carlo ^a,b  

^a UNIVERSITY OF BRESCIA   (Italy)

^b IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AMPLITUDE MODULATION; ARTICLE; ELECTRODE; ELECTROENCEPHALOGRAPHY; EVOKED CORTICAL RESPONSE; EVOKED RESPONSE; FEMALE; HUMAN; HUMAN EXPERIMENT; LATENT PERIOD; MALE; MODULATION; MOTOR CORTEX; NORMAL HUMAN; PRIORITY JOURNAL; TRANSCRANIAL MAGNETIC STIMULATION;

ADOLESCENT; ADULT; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; MALE; MOTOR CORTEX; REACTION TIME; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 77957195817     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00172.2010     Document Type: Article

References (57)

1. Allen EA, Pasley BN, Duong T, Freeman RD. Transcranial magnetic stimulation elicits coupled neural and hemodynamic consequences. Science 317: 1918-1921, 2007.
2. Bender S, Basseler K, Sebastian I, Resch F, Kammer T, Oelkers-Ax R, Weisbrod M. Electroencephalographic response to transcranial magnetic stimulation in children: evidence for giant inhibitory potentials. Ann Neurol 58: 58-67, 2005.
3. Bestmann S, Ruff CC, Blankenburg F, Weiskopf N, Driver J, Rothwell JC. Mapping causal interregional influences with concurrent TMS-fMRI. Exp Brain Res 191: 383-402, 2008.
4. Bohning DE, Shastri A, McConnell KA, Nahas Z, Lorberbaum JP, Roberts DR, Teneback C, Vincent DJ, George MS. A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol Psychiatry 45: 385-394, 1999. (Pubitemid 29130434)
5. Bonato C, Miniussi C, Rossini PM. Transcranial magnetic stimulation and cortical evoked potentials: a TMS/EEG co-registration study. Clin Neurophysiol 117: 1699-1707, 2006. (Pubitemid 44160504)
6. Brignani D, Manganotti P, Rossini PM, Miniussi C. Modulation of cortical oscillatory activity during transcranial magnetic stimulation. Hum Brain Mapp 29: 603-612, 2008. (Pubitemid 351706808)
7. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48: 1398-1403, 1997. (Pubitemid 27240571)
8. Cruccu G, Berardelli A, Inghilleri M, Manfredi M. Functional organization of the trigeminal motor system in man. A neurophysiological study. Brain 112: 1333-1350, 1989.
9. Cruccu G, Inghilleri M, Berardelli A, Romaniello A, Manfredi M. Cortical mechanisms mediating the inhibitory period after magnetic stimulation of the facial motor area. Muscle Nerve 20: 418-424, 1997. (Pubitemid 27154631)
10. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Mazzone P, Insola A, Tonali PA, Rothwell JC. The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115: 255-266, 2004. (Pubitemid 38117244)
11. Di Lazzaro V, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC. Direct recordings of descending volleys after transcranial magnetic and electric motor cortex stimulation in conscious humans. Electroencephalogr Clin Neurophysiol Suppl 51: 120-126, 1999.
12. Di Lazzaro V, Thickbroom GW, Pilato F, Profice P, Dileone M, Mazzone P, Insola A, Ranieri F, Tonali PA, Rothwell JC. Direct demonstration of the effects of repetitive paired-pulse transcranial magnetic stimulation at I-wave periodicity. Clin Neurophysiol 118: 1193-1197, 2007. (Pubitemid 46727100)
13. Dubach P, Guggisberg AG, Rosler KM, Hess CW, Mathis J. Significance of coil orientation for motor evoked potentials from nasalis muscle elicited by transcranial magnetic stimulation. Clin Neurophysiol 115: 862-870, 2004. (Pubitemid 38293483)
14. Esser SK, Huber R, Massimini M, Peterson MJ, Ferrarelli F, Tononi G. A direct demonstration of cortical LTP in humans: a combined TMS/EEG study. Brain Res Bull 69: 86-94, 2006. (Pubitemid 43185348)
15. Fitzgerald PB, Fountain S, Daskalakis ZJ. A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol 117: 2584-2596, 2006. (Pubitemid 44781313)
16. Gooden BR, Ridding MC, Miles TS, Nordstrom MA, Thompson PD. Bilateral cortical control of the human anterior digastric muscles. Exp Brain Res 129: 582-591, 1999.
17. Hamidi M, Slagter HA, Tononi G, Postle BR. Brain responses evoked by high-frequency repetitive transcranial magnetic stimulation: an event-related potential study. Brain Stimulation 3: 2-14, 2010.
18. Harris IM, Miniussi C. Parietal lobe contribution to mental rotation demonstrated with rTMS. J Cogn Neurosci 15: 315-323, 2003. (Pubitemid 36438943)
19. 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 187: 207-217, 2008.
20. Ilmoniemi RJ, Kicic D. Methodology for combined TMS and EEG. Brain Topogr 22: 233-248, 2010.
21. Ilmoniemi RJ, Virtanen J, Ruohonen J, Karhu J, Aronen HJ, Naatanen R, Katila T. Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 8: 3537-3540, 1997. (Pubitemid 27497479)
22. Jaberzadeh S, Sakuma S, Zoghi M, Miles TS, Nordstrom MA. Focal transcranial magnetic stimulation of motor cortex evokes bilateral and symmetrical silent periods in human masseter muscles. Clin Neurophysiol 119: 693-703, 2008.
23. Kahkonen S, Komssi S, Wilenius J, Ilmoniemi RJ. Prefrontal transcranial magnetic stimulation produces intensity-dependent EEG responses in humans. Neuroimage 24: 955-960, 2005. (Pubitemid 40164497)
24. Kahkonen S, Wilenius J, Komssi S, Ilmoniemi RJ. Distinct differences in cortical reactivity of motor and prefrontal cortices to magnetic stimulation. Clin Neurophysiol 115: 583-588, 2004. (Pubitemid 38230985)
25. Komssi S, Aronen HJ, Huttunen J, Kesaniemi M, Soinne L, Nikouline VV, Ollikainen M, Roine RO, Karhu J, Savolainen S, Ilmoniemi RJ. Ipsi- and contralateral EEG reactions to transcranial magnetic stimulation. Clin Neurophysiol 113: 175-184, 2002. (Pubitemid 34164705)
26. Komssi S, Kahkonen S. The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research. Brain Res Rev 52: 183-192, 2006. (Pubitemid 44051536)
27. Komssi S, Kahkonen S, Ilmoniemi RJ. The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation. Hum Brain Mapp 21: 154-164, 2004. (Pubitemid 38295899)
28. Komssi S, Savolainen P, Heiskala J, Kahkonen S. Excitation threshold of the motor cortex estimated with transcranial magnetic stimulation electroencephalography. Neuroreport 18: 13-16, 2007. (Pubitemid 46183382)
29. Krnjevic K, Randic M, Straughan DW. An inhibitory process in the cerebral cortex. J Physiol 184: 16-48, 1966.
30. Lemon R. Basic physiology of transcranial magnetic stimulation. In: Handbook of Trascranial Magnetic Stimulation, edited by Pascual-Leone A, Davey N, Rothwell J, Wasserman E, Puri BK. London: Arnold, 2002, p. 61-77.
31. Lioumis P, Kicic D, Savolainen P, Makela JP, Kahkonen S. Reproducibility of TMS-evoked EEG responses. Hum Brain Mapp 30: 1387-1396, 2009.
32. Litvak V, Komssi S, Scherg M, Hoechstetter K, Classen J, Zaaroor M, Pratt H, Kahkonen S. Artifact correction and source analysis of early electroencephalographic responses evoked by transcranial magnetic stimulation over primary motor cortex. Neuroimage 37: 56-70, 2007. (Pubitemid 47068999)
33. Lorenzano C, Gilio F, Inghilleri M, Conte A, Fofi L, Manfredi M, Berardelli A. Spread of electrical activity at cortical level after repetitive magnetic stimulation in normal subjects. Exp Brain Res 147: 186-192, 2002. (Pubitemid 35471798)
34. Macaluso GM, Pavesi G, Bonanini M, Mancia D, Gennari PU. Magnetic stimulation of the scalp: the responses of the masseter muscles. I. Minerva Stomatol 39: 337-341, 1990.
35. Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 111: 800-805, 2000. (Pubitemid 30236424)
36. Maki H, Ilmoniemi RJ. The relationship between peripheral and early cortical activation induced by transcranial magnetic stimulation. Neurosci Lett 2010.
37. Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G. Breakdown of cortical effective connectivity during sleep. Science 309: 2228-2232, 2005. (Pubitemid 41396075)
38. McMillan AS, Graven-Nielsen T, Romaniello A, Svensson P. Motor potentials evoked by transcranial magnetic stimulation during isometric and dynamic masseter muscle contraction in humans. Arch Oral Biol 46: 381-386, 2001. (Pubitemid 32183534)
39. Miller MN, Okaty BW, Nelson SB. Region-specific spike-frequency acceleration in layer 5 pyramidal neurons mediated by Kv1 subunits. J Neurosci 28: 13716-13726, 2008.
40. Miniussi C, Bortoletto M, Veniero D. Low-frequency transcranial magnetic stimulation (TMS) over premotor area modulates short-latency TMS-evoked potentials (TEPs). 29th International Congress of Clinical Neurophysiology, Kobe, Japan, 2010.
41. Miniussi C, Thut G. Combining TMS and EEG offers new prospects in cognitive neuroscience. Brain Topogr 4: 249-256, 2010.
42. Mochizuki H, Huang YZ, Rothwell JC. Interhemispheric interaction between human dorsal premotor and contralateral primary motor cortex. J Physiol 561: 331-338, 2004. (Pubitemid 39549488)
43. Moliadze V, Giannikopoulos D, Eysel UT, Funke K. Paired-pulse transcranial magnetic stimulation protocol applied to visual cortex of anesthetized cat: effects on visually evoked single-unit activity. J Physiol 566: 955-965, 2005. (Pubitemid 41122674)
44. Moliadze V, Zhao Y, Eysel U, Funke K. Effect of transcranial magnetic stimulation on single-unit activity in the cat primary visual cortex. J Physiol 553: 665-679, 2003. (Pubitemid 37527562)
45. Munchau A, Bloem BR, Irlbacher K, Trimble MR, Rothwell JC. Functional connectivity of human premotor and motor cortex explored with repetitive transcranial magnetic stimulation. J Neurosci 22: 554-561, 2002. (Pubitemid 34049095)
46. Nordstrom MA. Insights into the bilateral cortical control of human masticatory muscles revealed by transcranial magnetic stimulation. Arch Oral Biol 52: 338-342, 2007.
47. Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117: 847-858, 1994. (Pubitemid 24281845)
48. Paus T, Sipila PK, Strafella AP. Synchronization of neuronal activity in the human primary motor cortex by transcranial magnetic stimulation: an EEG study. J Neurophysiol 86: 1983-1990, 2001.
49. Quartarone A, Bagnato S, Rizzo V, Morgante F, Sant'angelo A, Battaglia F, Messina C, Siebner HR, Girlanda P. Distinct changes in cortical and spinal excitability following high-frequency repetitive TMS to the human motor cortex. Exp Brain Res 161: 114-124, 2005.
50. Rossi S, Ferro M, Cincotta M, Ulivelli M, Bartalini S, Miniussi C, Giovannelli F, Passero S. A real electro-magnetic placebo (REMP) device for sham transcranial magnetic stimulation (TMS). Clin Neurophysiol 118: 709-716, 2007.
51. Rossi S, Hallett M, Rossini PM, Pascual-Leone A, Group. SoTC. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120: 2008-2039, 2009.
52. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic MR, Hallett M, Katayama Y, Lucking CH, Maertens de Noordhout AL, Mardsen CD, Murray NMF, Rothwell JC, Swash M, Tomberg C. 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, 1994.
53. Siebner HR, Bergmann TO, Bestmann S, Johansen-Berg H, Mochizuki H, Bohning DE, Boorman ED, Groppa S, Miniussi C, Pascual-Leone A, Huber R, Taylor PC, Ilmoniemi RJ, DE Gennaro L, Strafell AP, Kahkonen S, Koppler S, Frisoni G, George MS, Hallett M, Brandt SA, Rushworth MF, Ziemann U, Rothwell J, Ward N, Cohen L, Baudewig J, Paus T, Ugawa Y, Rossini P. Consensus paper: combining transcranial stimulation with neuroimaging. Brain Stimulation 2: 58-80, 2009.
54. Siebner HR, Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148: 1-16, 2003. (Pubitemid 35435791)
55. 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 22: 219-232, 2010.
56. Van Der Werf YD, Paus T. The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions. Exp Brain Res 175: 231-245, 2006.
57. Veniero D, Bortoletto M, Miniussi C. TMS-EEG co-registration: on TMS-induced artifact. Clin Neurophysiol 120: 1392-1399, 2009.