Transcranial magnetic stimulation at the interface with other techniques: A powerful tool for studying the human cortex

Neuroscientist

Volumn 17, Issue 4, 2011, Pages 368-381

  Ziemann, Ulf ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

electroencephalography; functional magnetic resonance imaging; human cerebral cortex; magnetic resonance spectroscopy; near infrared spectroscopy; pharmacology; positron emission tomography; transcranial magnetic stimulation

Indexed keywords

ALCOHOL; ALPRAZOLAM; ATOMOXETINE; BACLOFEN; BENZODIAZEPINE; BROMOCRIPTINE; CABERGOLINE; CARBAMAZEPINE; DEXAMPHETAMINE; DEXTROMETHORPHAN; DIAZEPAM; FLUMAZENIL; HALOPERIDOL; KETAMINE; LAMOTRIGINE; LEVODOPA; LORAZEPAM; MEMANTINE; METHYLPHENIDATE; OXCARBAZEPINE; PERGOLIDE; PHENOBARBITAL; PHENYTOIN; PRAZOSIN; REBOXETINE; SULPIRIDE; THIOPENTAL; UNINDEXED DRUG; YOHIMBINE; ZOLPIDEM;

BRAIN BLOOD FLOW; BRAIN CORTEX; DRUG BINDING SITE; DRUG MECHANISM; DRUG RECEPTOR BINDING; ELECTROENCEPHALOGRAM; EVOKED MUSCLE RESPONSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; NEAR INFRARED SPECTROSCOPY; NEUROTRANSMISSION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; REVIEW; TRANSCRANIAL MAGNETIC STIMULATION;

BRAIN MAPPING; CEREBRAL CORTEX; DIAGNOSTIC IMAGING; ELECTROENCEPHALOGRAPHY; HUMANS; NERVE NET; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 79960496932     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858410390225     Document Type: Review

References (65)

1. Badawy RA, Macdonell RA, Berkovic SF, Newton MR, Jackson GD. Predicting seizure control: cortical excitability and antiepileptic medication. Ann Neurol. 2010 ; 67: 64-73
2. Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex [letter]. Lancet. 1985 ; 1: 1106-7 (Pubitemid 15075547)
3. Bestmann S, Baudewig J, Frahm J. On the synchronization of transcranial magnetic stimulation and functional echo-planar imaging. J Magn Reson Imaging. 2003a ; 17: 309-16 (Pubitemid 36259244)
4. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J. Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS. Neuroimage. 2003b ; 20: 1685-96 (Pubitemid 37468274)
5. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J. Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits. Eur J Neurosci. 2004 ; 19: 1950-62 (Pubitemid 38482583)
6. Bestmann S, Swayne O, Blankenburg F, Ruff CC, Haggard P, Weiskopf N. Dorsal premotor vortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. Cereb Cortex. 2008 ; 18: 1281-91 (Pubitemid 351769781)
7. Bohning DE, Shastri A, Nahas Z, Lorberbaum JP, Andersen SW, Dannels WR. Echoplanar BOLD fMRI of brain activation induced by concurrent transcranial magnetic stimulation. Invest Radiol. 1998 ; 33: 336-40 (Pubitemid 28299174)
8. Buzsaki G, Draguhn A. Neuronal oscillations in cortical networks. Science. 2004 ; 304: 1926-9
9. Chen R, Cros D, Curra A, Di Lazzaro V, Lefaucheur JP, Magistris MR. The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol. 2008 ; 119: 504-32
10. Chen R, Samii A, Canos M, Wassermann EM, Hallett M. Effects of phenytoin on cortical excitability in humans. Neurology. 1997 ; 49: 881-3 (Pubitemid 27428043)
11. Cho SS, Strafella AP. rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS One. 2009 ; 4: e6725
12. Cooke SF, Bliss TV. Plasticity in the human central nervous system. Brain. 2006 ; 129: 1659-73 (Pubitemid 43999401)
13. Cracco RQ, Amassian VE, Maccabee PJ, Cracco JB. Comparison of human transcallosal responses evoked by magnetic coil and electrical stimulation. Electroencephalogr Clin Neurophysiol. 1989 ; 74: 417-24 (Pubitemid 20000336)
14. Daskalakis ZJ, Farzan F, Barr MS, Maller JJ, Chen R, Fitzgerald PB. Long-interval cortical inhibition from the dorsolateral prefrontal cortex: a TMS-EEG study. Neuropsychopharmacology. 2008 ; 33: 2860-9
15. Di Lazzaro V, Pilato F, Dileone M, Profice P, Ranieri F, Ricci V. Segregating two inhibitory circuits in human motor cortex at the level of GABAA receptor subtypes: a TMS study. Clin Neurophysiol. 2007 ; 118: 2207-14 (Pubitemid 47385353)
16. Di Lazzaro V, Pilato F, Dileone M, Ranieri F, Ricci V, Profice P. GABAA receptor subtype specific enhancement of inhibition in human motor cortex. J Physiol. 2006 ; 575: 721-6 (Pubitemid 44323738)
17. Farzan F, Barr MS, Levinson AJ, Chen R, Wong W, Fitzgerald PB. Evidence for gamma inhibition deficits in the dorsolateral prefrontal cortex of patients with schizophrenia. Brain. 2010 ; 133: 1505-14
18. Farzan F, Barr MS, Wong W, Chen R, Fitzgerald PB, Daskalakis ZJ. Suppression of gamma-oscillations in the dorsolateral prefrontal cortex following long interval cortical inhibition: a TMS-EEG study. Neuropsychopharmacology. 2009 ; 34: 1543-51
19. Ferrarelli F, Massimini M, Peterson MJ, Riedner BA, Lazar M, Murphy MJ. Reduced evoked gamma oscillations in the frontal cortex in schizophrenia patients: a TMS/EEG study. Am J Psychiatry. 2008 ; 165: 996-1005
20. Floyer-Lea A, Wylezinska M, Kincses T, Matthews PM. Rapid modulation of GABA concentration in human sensorimotor cortex during motor learning. J Neurophysiol. 2006 ; 95: 1639-44
21. Fox P, Ingham R, George MS, Mayberg H, Ingham J, Roby J. Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport. 1997 ; 8: 2787-91 (Pubitemid 27373530)
22. Hada Y, Abo M, Kaminaga T, Mikami M. Detection of cerebral blood flow changes during repetitive transcranial magnetic stimulation by recording hemoglobin in the brain cortex, just beneath the stimulation coil, with near-infrared spectroscopy. Neuroimage. 2006 ; 32: 1226-30 (Pubitemid 44278670)
23. Hallett M. Transcranial magnetic stimulation: a primer. Neuron. 2007 ; 55: 187-99 (Pubitemid 47048907)
24. Huang Y-Z, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005 ; 45: 201-6 (Pubitemid 40128115)
25. Ilmoniemi RJ, Kicic D. Methodology for combined TMS and EEG. Brain Topogr. 2010 ; 22: 233-48
26. Ilmoniemi RJ, Virtanen J, Ruohonen J, Karhu J, Aronen HJ, Naatanen R. Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. NeuroReport. 1997 ; 8: 3537-40 (Pubitemid 27497479)
27. Kanai R, Chaieb L, Antal A, Walsh V, Paulus W. Frequency-dependent electrical stimulation of the visual cortex. Curr Biol. 2008 ; 18: 1839-43
28. Kawaguchi Y, Kondo S. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol. 2002 ; 31: 277-87 (Pubitemid 36877376)
29. Kozel FA, Tian F, Dhamne S, Croarkin PE, McClintock SM, Elliott A. Using simultaneous repetitive transcranial magnetic stimulation/functional near infrared spectroscopy (rTMS/fNIRS) to measure brain activation and connectivity. Neuroimage. 2009 ; 47: 1177-84
30. Li X, Teneback CC, Nahas Z, Kozel FA, Large C, Cohn J. Interleaved transcranial magnetic stimulation/functional MRI confirms that lamotrigine inhibits cortical excitability in healthy young men. Neuropsychopharmacology. 2004 ; 29: 1395-407 (Pubitemid 38780663)
31. Macdonald RL, Kang JQ, Gallagher MJ. Mutations in GABAA receptor subunits associated with genetic epilepsies. J Physiol. 2010 ; 588: 1861-9
32. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci. 2004 ; 5: 793-807 (Pubitemid 39336216)
33. Marshall L, Helgadottir H, Molle M, Born J. Boosting slow oscillations during sleep potentiates memory. Nature. 2006 ; 444: 610-3 (Pubitemid 44864437)
34. Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G. Breakdown of cortical effective connectivity during sleep. Science. 2005 ; 309: 2228-32 (Pubitemid 41396075)
35. McDonnell MN, Orekhov Y, Ziemann U. The role of GABA(B) receptors in intracortical inhibition in the human motor cortex. Exp Brain Res. 2006 ; 173: 86-93 (Pubitemid 44099702)
36. Mochizuki H, Furubayashi T, Hanajima R, Terao Y, Mizuno Y, Okabe S. Hemoglobin concentration changes in the contralateral hemisphere during and after theta burst stimulation of the human sensorimotor cortices. Exp Brain Res. 2007 ; 180: 667-75 (Pubitemid 46988108)
37. Mochizuki H, Ugawa Y, Terao Y, Sakai KL. Cortical hemoglobin- concentration changes under the coil induced by single-pulse TMS in humans: a simultaneous recording with near-infrared spectroscopy. Exp Brain Res. 2006 ; 169: 302-10 (Pubitemid 43356322)
38. Möhler H. GABA(A) receptor diversity and pharmacology. Cell Tissue Res. 2006 ; 326: 505-16
39. Moliadze V, Zhao Y, Funke K. Effect of transcranial magnetic stimulation on single unit activity in cat primary visual cortex. J Physiol. 2003 ; 553: 665-79 (Pubitemid 37527562)
40. Noguchi Y, Watanabe E, Sakai KL. An event-related optical topography study of cortical activation induced by single-pulse transcranial magnetic stimulation. Neuroimage. 2003 ; 19: 156-62 (Pubitemid 36627388)
41. Paulus W, Classen J, Cohen LG, Large CH, Di Lazzaro V, Nitsche M. State of the art: pharmacologic effects on cortical excitability measures tested by transcranial magnetic stimulation. Brain Stimulation. 2008 ; 1: 151-63
42. Paus T, Castro-Alamancos MA, Petrides M. Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation. Eur J Neurosci. 2001a ; 14: 1405-11 (Pubitemid 35463746)
43. Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans AC. Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J Neurosci. 1997 ; 17: 3178-84 (Pubitemid 27175830)
44. 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. 2001b ; 86: 1983-90 (Pubitemid 32953243)
45. Romei V, Brodbeck V, Michel C, Amedi A, Pascual-Leone A, Thut G. Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas. Cereb Cortex. 2008 ; 18: 2010-8
46. Rosanova M, Casali A, Bellina V, Resta F, Mariotti M, Massimini M. Natural frequencies of human corticothalamic circuits. J Neurosci. 2009 ; 29: 7679-85
47. Ruff CC, Blankenburg F, Bjoertomt O, Bestmann S, Freeman E, Haynes JD. Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Curr Biol. 2006 ; 16: 1479-88 (Pubitemid 44142983)
48. Sauseng P, Klimesch W, Gerloff C, Hummel FC. Spontaneous locally restricted EEG alpha activity determines cortical excitability in the motor cortex. Neuropsychologia. 2009 ; 47: 284-8
49. Sibon I, Strafella AP, Gravel P, Ko JH, Booij L, Soucy JP. Acute prefrontal cortex TMS in healthy volunteers: effects on brain (11)C-alphaMtrp trapping. Neuroimage. 2007 ; 34: 1658-64 (Pubitemid 46187059)
50. Siebner HR, Willoch F, Peller M, Auer C, Boecker H, Conrad B. Imaging brain activation induced by long trains of repetitive transcranial magnetic stimulation. Neuroreport. 1998 ; 9: 943-8 (Pubitemid 28179305)
51. Stagg CJ, Best JG, Stephenson MC, O'Shea J, Wylezinska M, Kincses ZT. Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci. 2009a ; 29: 5202-6
52. Stagg CJ, Wylezinska M, Matthews PM, Johansen-Berg H, Jezzard P, Rothwell JC. The neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. J Neurophysiol. 2009b ; 101: 2872-7
53. Stickgold R. Sleep-dependent memory consolidation. Nature. 2005 ; 437: 1272-8 (Pubitemid 41568667)
54. Strafella AP, Ko JH, Grant J, Fraraccio M, Monchi O. Corticostriatal functional interactions in Parkinson's disease: a rTMS/[11C]raclopride PET study. Eur J Neurosci. 2005 ; 22: 2946-52 (Pubitemid 41811290)
55. Strafella AP, Paus T, Barrett J, Dagher A. Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci. 2001 ; 21: RC157
56. Strafella AP, Paus T, Fraraccio M, Dagher A. Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain. 2003 ; 126: 2609-15 (Pubitemid 37463080)
57. Uhlhaas PJ, Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci. 2010 ; 11: 100-13
58. Valentin A, Arunachalam R, Mesquita-Rodrigues A, Garcia Seoane JJ, Richardson MP, Mills KR. Late EEG responses triggered by transcranial magnetic stimulation (TMS) in the evaluation of focal epilepsy. Epilepsia. 2008 ; 49: 470-80 (Pubitemid 351294537)
59. Valls-Sole J, Pascual-Leone A, Wassermann EM, Hallett M. Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol. 1992 ; 85: 355-64 (Pubitemid 23011246)
60. Villringer A, Planck J, Hock C, Schleinkofer L, Dirnagl U. Near infrared spectroscopy (NIRS): a new tool to study hemodynamic changes during activation of brain function in human adults. Neurosci Lett. 1993 ; 154: 101-4 (Pubitemid 23172331)
61. Wassermann E, Epstein CM, Ziemann U, Walsh V, Paus T, Lisanby SH The Oxford handbook of transcranial stimulation. Oxford: Oxford University Press ; 2008 :
62. Ziemann U. TMS and drugs. Clin Neurophysiol. 2004 ; 115: 1717-29 (Pubitemid 38952939)
63. Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res. 1996a ; 109: 127-35 (Pubitemid 26119972)
64. Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol. 1996b ; 40: 367-78 (Pubitemid 26304794)
65. Ziemann U, Rothwell JC, Ridding MC. Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol (Lond). 1996c ; 496: 873-81 (Pubitemid 26387868)