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Mapping causal interregional influences with concurrent TMS–fMRI

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Abstract

Transcranial magnetic stimulation (TMS) produces a direct causal effect on brain activity that can now be studied by new approaches that simultaneously combine TMS with neuroimaging methods, such as functional magnetic resonance imaging (fMRI). In this review we highlight recent concurrent TMS–fMRI studies that illustrate how this novel combined technique may provide unique insights into causal interactions among brain regions in humans. We show how fMRI can detect the spatial topography of local and remote TMS effects and how these may vary with psychological factors such as task-state. Concurrent TMS–fMRI may furthermore reveal how the brain adapts to so-called virtual lesions induced by TMS, and the distributed activity changes that may underlie the behavioural consequences often observed during cortical stimulation with TMS. We argue that combining TMS with neuroimaging techniques allows a further step in understanding the physiological underpinnings of TMS, as well as the neural correlated of TMS-evoked consequences on perception and behaviour. This can provide powerful new insights about causal interactions among brain regions in both health and disease that may ultimately lead to developing more efficient protocols for basic research and therapeutic TMS applications.

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Abbreviations

BOLD:

Blood-oxygenation-level-dependent

DCM:

Dynamic causal modelling

EEG:

Electroencephalography

EPI:

Echo-planar imaging

FEF:

Frontal eye fields

fMRI:

Functional magnetic resonance imaging

M1:

Primary motor cortex

NIRS:

Near-infrared spectroscopy

PET:

Positron emission tomography

PMd:

Dorsal premotor cortex

IPS:

Intraparietal sulcus

TES:

Transcranial electrical stimulation

tDCS:

Transcranial direct current stimulation

TMS:

Transcranial magnetic stimulation

SoM:

Sense of movement

References

  • Allen EA, Pasley BN, Duong T, Freeman RD (2007) Transcranial magnetic stimulation elicits coupled neural and hemodynamic consequences. Science 317:1918–1921

    Article  PubMed  CAS  Google Scholar 

  • Armstrong KM, Fitzgerald JK, Moore T (2006) Changes in visual receptive fields with microstimulation of frontal cortex. Neuron 50:791–798

    Article  PubMed  CAS  Google Scholar 

  • Astafiev SV, Shulman GL, Stanley CM, Snyder AZ, Van Essen DC, Corbetta M (2003) Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing. J Neurosci 23:4689–4699

    PubMed  CAS  Google Scholar 

  • Attwell D, Iadecola C (2002) The neural basis of functional brain imaging signals. Trends Neurosci 25:621–625

    Article  PubMed  CAS  Google Scholar 

  • Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133–1145

    Article  PubMed  CAS  Google Scholar 

  • Aurora SK, Ahmad BK, Welch KM, Bhardhwaj P, Ramadan NM (1998) Transcranial magnetic stimulation confirms hyperexcitability of occipital cortex in migraine. Neurology 50:1111–1114

    PubMed  CAS  Google Scholar 

  • Aydin-Abidin S, Moliadze V, Eysel UT, Funke K (2006) Effects of repetitive TMS on visually evoked potentials and EEG in the anaesthetized cat: dependence on stimulus frequency and train duration. J Physiol 574:443–455

    Article  PubMed  CAS  Google Scholar 

  • Balslev D, Nielsen FA, Lund TE, Law I, Paulson OB (2006) Similar brain networks for detecting visuo-motor and visuo-proprioceptive synchrony. Neuroimage 31:308–312

    Article  PubMed  Google Scholar 

  • Baudewig J, Nitsche MA, Paulus W, Frahm J (2001a) Regional modulation of BOLD MRI responses to human sensorimotor activation by transcranial direct current stimulation. Magn Reson Med 45:196–201

    Article  PubMed  CAS  Google Scholar 

  • Baudewig J, Siebner HR, Bestmann S, Tergau F, Tings T, Paulus W, Frahm J (2001b) Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS). Neuroreport 12:3543–3548

    Article  PubMed  CAS  Google Scholar 

  • Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J (2003) Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS. Neuroimage 20:1685–1696

    Article  PubMed  Google Scholar 

  • Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J (2004) Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits. Eur J Neurosci 19:1950–1962

    Article  PubMed  Google Scholar 

  • Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J (2005) BOLD MRI responses to repetitive TMS over human dorsal premotor cortex. Neuroimage 28:22–29

    Article  PubMed  Google Scholar 

  • Bestmann S, Oliviero A, Voss M, Dechent P, Lopez-Dolado E, Driver J, Baudewig J (2006) Cortical correlates of TMS-induced phantom hand movements revealed with concurrent TMS–fMRI. Neuropsychologia 44:2959–2971

    Article  PubMed  CAS  Google Scholar 

  • Bestmann S, Ruff CC, Blakemore C, Driver J, Thilo KV (2007) Spatial attention changes excitability of human visual cortex to direct stimulation. Curr Biol 17:134–139

    Article  PubMed  CAS  Google Scholar 

  • Bestmann S, Ruff CC, Driver J, Blankenburg F (2008a) Concurrent TMS and functional magnetic resonance imaging: methods and current advances. In: Wasserman EA, Epstein CM, Ziemann U, Walsh V, Paus T, Lisanby SH (eds) Oxford handbook of transcranial stimulation. Oxford University Press, Oxford

    Google Scholar 

  • Bestmann S, Swayne O, Blankenburg F, Ruff CC, Haggard P, Weiskopf N, Josephs O, Driver J, Rothwell JC, Ward NS (2008b) Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. Cereb Cortex 18:1281–1291

    Article  PubMed  Google Scholar 

  • Blankenburg F, Ruff CC, Bestmann S, Bjoertomt O, Eshel N, Josephs O, Weiskopf N, Driver J (2008) Interhemispheric effect of parietal tms on somatosensory response confirmed directly with concurrent TMS–fMRI. J Neurosci (in press)

  • Bohning DE, Shastri A, Nahas Z, Lorberbaum JP, Andersen SW, Dannels WR, Haxthausen EU, Vincent DJ, George MS (1998) Echoplanar BOLD fMRI of brain activation induced by concurrent transcranial magnetic stimulation. Invest Radiol 33:336–340

    Article  PubMed  CAS  Google Scholar 

  • Bohning DE, Shastri A, McConnell KA, Nahas Z, Lorberbaum JP, Roberts DR, Teneback C, Vincent DJ, George MS (1999) A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol Psychiatry 45:385–394

    Article  PubMed  CAS  Google Scholar 

  • Bohning DE, Shastri A, McGavin L, McConnell KA, Nahas Z, Lorberbaum JP, Roberts DR, George MS (2000a) Motor cortex brain activity induced by 1-Hz transcranial magnetic stimulation is similar in location and level to that for volitional movement. Invest Radiol 35:676–683

    Article  PubMed  CAS  Google Scholar 

  • Bohning DE, Shastri A, Wassermann EM, Ziemann U, Lorberbaum JP, Nahas Z, Lomarev MP, George MS (2000b) BOLD-f MRI response to single-pulse transcranial magnetic stimulation (TMS). J Magn Reson Imaging 11:569–574

    Article  PubMed  CAS  Google Scholar 

  • Bohning DE, Shastri A, Lomarev MP, Lorberbaum JP, Nahas Z, George MS (2003) BOLD-fMRI response vs. transcranial magnetic stimulation (TMS) pulse-train length: testing for linearity. J Magn Reson Imaging 17:279–290

    Article  PubMed  Google Scholar 

  • Brandt SA, Brocke J, Roricht S, Ploner CJ, Villringer A, Meyer BU (2001) In vivo assessment of human visual system connectivity with transcranial electrical stimulation during functional magnetic resonance imaging. Neuroimage 14:366–375

    Article  PubMed  CAS  Google Scholar 

  • Brocke J, Schmidt S, Irlbacher K, Cichy RM, Brandt SA (2007) Transcranial cortex stimulation and fMRI: Electrophysiological correlates of dual-pulse BOLD signal modulation. Neuroimage 40:631–643

    Article  PubMed  Google Scholar 

  • Chambers CD, Mattingley JB (2005) Neurodisruption of selective attention: insights and implications. Trends Cogn Sci 9:542–550

    Article  PubMed  Google Scholar 

  • Chen R (2004) Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res 154:1–10

    Article  PubMed  Google Scholar 

  • Chouinard PA, Van Der Werf YD, Leonard G, Paus T (2003) Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. J Neurophysiol 90:1071–1083

    Article  PubMed  Google Scholar 

  • Civardi C, Cantello R, Asselman P, Rothwell JC (2001) Transcranial magnetic stimulation can be used to test connections to primary motor areas from frontal and medial cortex in humans. Neuroimage 14:1444–1453

    Article  PubMed  CAS  Google Scholar 

  • Classen J, Stefan K (2008) Changes in TMS measures induced by repetitive TMS. The Oxford handbook of transcranial magnetic stimulation. Oxford University Press, Oxford, pp 185-200

  • Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215

    Article  PubMed  CAS  Google Scholar 

  • Curra A, Modugno N, Inghilleri M, Manfredi M, Hallett M, Berardelli A (2002) Transcranial magnetic stimulation techniques in clinical investigation. Neurology 59:1851–1859

    PubMed  CAS  Google Scholar 

  • Daskalakis ZJ, Christensen BK, Fitzgerald PB, Chen R (2008) Dysfunctional neural plasticity in patients with schizophrenia. Arch Gen Psychiatry 65:378–385

    Article  PubMed  Google Scholar 

  • Davare M, Andres M, Cosnard G, Thonnard JL, Olivier E (2006) Dissociating the role of ventral and dorsal premotor cortex in precision grasping. J Neurosci 26:2260–2268

    Article  PubMed  Google Scholar 

  • de Labra C, Rivadulla C, Grieve K, Marino J, Espinosa N, Cudeiro J (2007) Changes in visual responses in the feline dLGN: selective thalamic suppression induced by transcranial magnetic stimulation of V1. Cereb Cortex 17:1376–1385

    Article  PubMed  Google Scholar 

  • Denslow S, Lomarev M, George MS, Bohning DE (2005) Cortical and subcortical brain effects of transcranial magnetic stimulation (TMS)-induced movement: an interleaved TMS/functional magnetic resonance imaging study. Biol Psychiatry 57:752–760

    Article  PubMed  Google Scholar 

  • Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193–222

    Article  PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Restuccia D, Oliviero A, Profice P, Ferrara L, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Magnetic transcranial stimulation at intensities below active motor threshold activates intracortical inhibitory circuits. Exp Brain Res 119:265–268

    Article  PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Mazzone P, Insola A, Tonali PA, Rothwell JC (2004) The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115:255–266

    Article  PubMed  CAS  Google Scholar 

  • Driver J (2001) A selective review of selective attention research from the past century. Br J Psychol 92:53–78

    Article  CAS  Google Scholar 

  • Ekstrom LB, Roelfsema PR, Arsenault JT, Bonmassar G, Vanduffel W (2008) Bottom–up dependent gating of frontal signals in early visual cortex. Science 321:414–417

    Article  PubMed  CAS  Google Scholar 

  • Epstein CM (2008) TMS stimulation coils. In: Wasserman EA, Epstein CM, Ziemann U, Walsh V, Paus T, Lisanby SH (eds) Oxford handbook of transcranial stimulation. Oxford University Press, Oxford

    Google Scholar 

  • Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD (1992) Interhemispheric inhibition of the human motor cortex. J Physiol 453:525–546

    PubMed  CAS  Google Scholar 

  • Formisano E, Goebel R (2003) Tracking cognitive processes with functional MRI mental chronometry. Curr Opin Neurobiol 13:174–181

    Article  PubMed  CAS  Google Scholar 

  • Fox P, Ingham R, George MS, Mayberg H, Ingham J, Roby J, Martin C, Jerabek P (1997) Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport 8:2787–2791

    Article  PubMed  CAS  Google Scholar 

  • Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuroimage 19:1273–1302

    Article  PubMed  CAS  Google Scholar 

  • Friston KJ, Price CJ (2003) Degeneracy and redundancy in cognitive anatomy. Trends Cogn Sci 7:151–152

    Article  PubMed  Google Scholar 

  • Fujiwara T, Rothwell JC (2004) The after effects of motor cortex rTMS depend on the state of contraction when rTMS is applied. Clin Neurophysiol 115:1514–1518

    Article  PubMed  Google Scholar 

  • George MS, Nahas Z, Kozol FA, Li X, Yamanaka K, Mishory A, Bohning DE (2003) Mechanisms and the current state of transcranial magnetic stimulation. CNS Spectr 8:496–514

    PubMed  Google Scholar 

  • Hallett M (2007) Transcranial magnetic stimulation: a primer. Neuron 55:187–199

    Article  PubMed  CAS  Google Scholar 

  • Hanaoka N, Aoyama Y, Kameyama M, Fukuda M, Mikuni M (2007) Deactivation and activation of left frontal lobe during and after low-frequency repetitive transcranial magnetic stimulation over right prefrontal cortex: a near-infrared spectroscopy study. Neurosci Lett 414:99–104

    Article  PubMed  CAS  Google Scholar 

  • Huang YZ, Rothwell JC, Edwards MJ, Chen RS (2008) Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb Cortex 18:563–570

    Article  PubMed  Google Scholar 

  • Hubl D, Nyffeler T, Wurtz P, Chaves S, Pflugshaupt T, Luthi M, von Wartburg R, Wiest R, Dierks T, Strik WK, Hess CW, Muri RM (2008) Time course of blood oxygenation level-dependent signal response after theta burst transcranial magnetic stimulation of the frontal eye field. Neuroscience 151:921–928

    Article  PubMed  CAS  Google Scholar 

  • Ilmoniemi R, Karhu J (2008) TMS and electroencephalography: methods and current advances. In: Wasserman EM, Epstein CM, Ziemann U, Walsh V, Paus T, Lisanby SH (eds) The Oxford handbook of transcranial magnetic stimulation. Oxford University Press, Oxford, pp 593–608

    Google Scholar 

  • Ilmoniemi RJ, Ruohonen J, Virtanen J, Aronen HJ, Karhu J (1999) EEG responses evoked by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol Suppl 51:22–29

    PubMed  CAS  Google Scholar 

  • Josephs O, Henson RN (1999) Event-related functional magnetic resonance imaging: modelling, inference and optimization. Philos Trans R Soc Lond B Biol Sci 354:1215–1228

    Article  PubMed  CAS  Google Scholar 

  • Kahkonen S, Komssi S, Wilenius J, Ilmoniemi RJ (2005) Prefrontal transcranial magnetic stimulation produces intensity-dependent EEG responses in humans. Neuroimage 24:955–960

    Article  PubMed  CAS  Google Scholar 

  • Kemna LJ, Gembris D (2003) Repetitive transcranial magnetic stimulation induces different responses in different cortical areas: a functional magnetic resonance study in humans. Neurosci Lett 336:85–88

    Article  PubMed  CAS  Google Scholar 

  • Kimbrell TA, Dunn RT, George MS, Danielson AL, Willis MW, Repella JD, Benson BE, Herscovitch P, Post RM, Wassermann EM (2002) Left prefrontal-repetitive transcranial magnetic stimulation (rTMS) and regional cerebral glucose metabolism in normal volunteers. Psychiatry Res 115:101–113

    Article  PubMed  CAS  Google Scholar 

  • Koch G, Franca M, Del Olmo MF, Cheeran B, Milton R, Alvarez SM, Rothwell JC (2006) Time course of functional connectivity between dorsal premotor and contralateral motor cortex during movement selection. J Neurosci 26:7452–7459

    Article  PubMed  CAS  Google Scholar 

  • Koch G, Franca M, Mochizuki H, Marconi B, Caltagirone C, Rothwell JC (2007) Interactions between pairs of transcranial magnetic stimuli over the human left dorsal premotor cortex differ from those seen in primary motor cortex. J Physiol 578:551–562

    Article  PubMed  CAS  Google Scholar 

  • Komssi S, Aronen HJ, Huttunen J, Kesaniemi M, Soinne L, Nikouline VV, Ollikainen M, Roine RO, Karhu J, Savolainen S, Ilmoniemi RJ (2002) Ipsi- and contralateral EEG reactions to transcranial magnetic stimulation. Clin Neurophysiol 113:175–184

    Article  PubMed  Google Scholar 

  • Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519

    PubMed  CAS  Google Scholar 

  • Lee L, Siebner H, Bestmann S (2006) Rapid modulation of distributed brain activity by transcranial magnetic stimulation of human motor cortex. Behav Neurol 17:135–148

    PubMed  Google Scholar 

  • Lee L, Siebner HR, Rowe JB, Rizzo V, Rothwell JC, Frackowiak RS, Friston KJ (2003) Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J Neurosci 23:5308–5318

    PubMed  CAS  Google Scholar 

  • Li X, Nahas Z, Kozel FA, Anderson B, Bohning DE, George MS (2004a) Acute left prefrontal transcranial magnetic stimulation in depressed patients is associated with immediately increased activity in prefrontal cortical as well as subcortical regions. Biol Psychiatry 55:882–890

    Article  PubMed  Google Scholar 

  • Li X, Teneback CC, Nahas Z, Kozel FA, Large C, Cohn J, Bohning DE, George MS (2004b) Interleaved transcranial magnetic stimulation/functional MRI confirms that lamotrigine inhibits cortical excitability in healthy young men. Neuropsychopharmacology 29:1395–1407

    Article  PubMed  CAS  Google Scholar 

  • Logothetis NK, Pfeuffer J (2004) On the nature of the BOLD fMRI contrast mechanism. Magn Reson Imaging 22:1517–1531

    Article  PubMed  Google Scholar 

  • Logothetis NK, Wandell BA (2004) Interpreting the BOLD signal. Annu Rev Physiol 66:735–769

    Article  PubMed  CAS  Google Scholar 

  • Lotze M, Montoya P, Erb M, Hulsmann E, Flor H, Klose U, Birbaumer N, Grodd W (1999) Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. J Cogn Neurosci 11:491–501

    Article  PubMed  CAS  Google Scholar 

  • Martinez A, Anllo-Vento L, Sereno MI, Frank LR, Buxton RB, Dubowitz DJ, Wong EC, Hinrichs H, Heinze HJ, Hillyard SA (1999) Involvement of striate and extrastriate visual cortical areas in spatial attention. Nat Neurosci 2:364–369

    Article  PubMed  CAS  Google Scholar 

  • Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G (2005) Breakdown of cortical effective connectivity during sleep. Science 309:2228–2232

    Article  PubMed  CAS  Google Scholar 

  • Matthews PM, Jezzard P (2004) Functional magnetic resonance imaging. J Neurol Neurosurg Psychiatry 75:6–12

    PubMed  CAS  Google Scholar 

  • Mazzocchio R, Rothwell JC, Day BL, Thompson PD (1994) Effect of tonic voluntary activity on the excitability of human motor cortex. J Physiol 474:261–267

    PubMed  CAS  Google Scholar 

  • Mercier C, Reilly KT, Vargas CD, Aballea A, Sirigu A (2006) Mapping phantom movement representations in the motor cortex of amputees. Brain 129:2202–2210

    Article  PubMed  Google Scholar 

  • Mochizuki H, Ugawa Y, Terao Y, Sakai KL (2006) Cortical hemoglobin-concentration changes under the coil induced by single-pulse TMS in humans: a simultaneous recording with near-infrared spectroscopy. Exp Brain Res 169:302–310

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki H, Furubayashi T, Hanajima R, Terao Y, Mizuno Y, Okabe S, Ugawa Y (2007) Hemoglobin concentration changes in the contralateral hemisphere during and after theta burst stimulation of the human sensorimotor cortices. Exp Brain Res 180:667–675

    Article  PubMed  CAS  Google Scholar 

  • Moeller S, Freiwald WA, Tsao DY (2008) Patches with links: a unified system for processing faces in the macaque temporal lobe. Science 320:1355–1359

    Article  PubMed  CAS  Google Scholar 

  • Moliadze V, Zhao Y, Eysel U, Funke K (2003) Effect of transcranial magnetic stimulation on single-unit activity in the cat primary visual cortex. J Physiol 553:665–679

    Article  PubMed  CAS  Google Scholar 

  • Moliadze V, Giannikopoulos D, Eysel UT, Funke K (2005) Paired-pulse transcranial magnetic stimulation protocol applied to visual cortex of anaesthetized cat: effects on visually evoked single-unit activity. J Physiol 566:955–965

    Article  PubMed  CAS  Google Scholar 

  • Moore T, Armstrong KM (2003) Selective gating of visual signals by microstimulation of frontal cortex. Nature 421:370–373

    Article  PubMed  CAS  Google Scholar 

  • Munchau A, Bloem BR, Irlbacher K, Trimble MR, Rothwell JC (2002) Functional connectivity of human premotor and motor cortex explored with repetitive transcranial magnetic stimulation. J Neurosci 22:554–561

    PubMed  CAS  Google Scholar 

  • Nahas Z, Lomarev M, Roberts DR, Shastri A, Lorberbaum JP, Teneback C, McConnell K, Vincent DJ, Li X, George MS, Bohning DE (2001) Unilateral left prefrontal transcranial magnetic stimulation (TMS) produces intensity-dependent bilateral effects as measured by interleaved BOLD fMRI. Biol Psychiatry 50:712–720

    Article  PubMed  CAS  Google Scholar 

  • Naito E, Ehrsson HH, Geyer S, Zilles K, Roland PE (1999) Illusory arm movements activate cortical motor areas: a positron emission tomography study. J Neurosci 19:6134–6144

    PubMed  CAS  Google Scholar 

  • Naito E, Roland PE, Ehrsson HH (2002) I feel my hand moving: a new role of the primary motor cortex in somatic perception of limb movement. Neuron 36:979–988

    Article  PubMed  CAS  Google Scholar 

  • Nikouline V, Ruohonen J, Ilmoniemi RJ (1999) The role of the coil click in TMS assessed with simultaneous EEG. Clin Neurophysiol 110:1325–1328

    Article  PubMed  CAS  Google Scholar 

  • Nikulin VV, Kicic D, Kahkonen S, Ilmoniemi RJ (2003) Modulation of electroencephalographic responses to transcranial magnetic stimulation: evidence for changes in cortical excitability related to movement. Eur J Neurosci 18:1206–1212

    Article  PubMed  Google Scholar 

  • Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527:633–639

    Article  PubMed  CAS  Google Scholar 

  • Nitsche MA, Liebetanz D, Antal A, Lang N, Tergau F, Paulus W (2003) Modulation of cortical excitability by weak direct current stimulation–technical, safety and functional aspects. Suppl Clin Neurophysiol 56:255–276

    PubMed  Google Scholar 

  • O’Shea J, Johansen-Berg H, Trief D, Gobel S, Rushworth MF (2007a) Functionally specific reorganization in human premotor cortex. Neuron 54:479–490

    Article  PubMed  CAS  Google Scholar 

  • O’Shea J, Sebastian C, Boorman ED, Johansen-Berg H, Rushworth MF (2007b) Functional specificity of human premotor-motor cortical interactions during action selection. Eur J Neurosci 26:2085–2095

    Article  PubMed  Google Scholar 

  • Oliviero A, Di Lazzaro V, Piazza O, Profice P, Pennisi MA, Della CF, Tonali P (1999) Cerebral blood flow and metabolic changes produced by repetitive magnetic brain stimulation. J Neurol 246:1164–1168

    Article  PubMed  CAS  Google Scholar 

  • Ortu E, Deriu F, Suppa A, Tolu E, Rothwell JC (2008) Effects of volitional contraction on intracortical inhibition and facilitation in the human motor cortex. J Physiol (in press). doi:10.1113/jphysiol.2008.158956

  • Pascual-Leone A, Bartres-Faz D, Keenan JP (1999) Transcranial magnetic stimulation: studying the brain-behaviour relationship by induction of ‘virtual lesions’. Philos Trans R Soc Lond B Biol Sci 354:1229–1238

    Article  PubMed  CAS  Google Scholar 

  • Pascual-Leone A, Walsh V, Rothwell J (2000) Transcranial magnetic stimulation in cognitive neuroscience–virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol 10:232–237

    Article  PubMed  CAS  Google Scholar 

  • Pascual-Leone A, Walsh V (2001) Fast backprojections from the motion to the primary visual area necessary for visual awareness. Science 292:510–512

    Article  PubMed  CAS  Google Scholar 

  • Patel RS, Bowman FD, Rilling JK (2006) A Bayesian approach to determining connectivity of the human brain. Hum Brain Mapp 27:267–276

    Article  PubMed  Google Scholar 

  • Paus T (1999) Imaging the brain before, during, and after transcranial magnetic stimulation. Neuropsychologia 37:219–224

    Article  PubMed  CAS  Google Scholar 

  • Paus T (2005) Inferring causality in brain images: a perturbation approach. Philos Trans R Soc Lond B Biol Sci 360:1109–1114

    Article  PubMed  Google Scholar 

  • Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans AC (1997) Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J Neurosci 17:3178–3184

    PubMed  CAS  Google Scholar 

  • Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans AC (1998) Dose-dependent reduction of cerebral blood flow during rapid-rate transcranial magnetic stimulation of the human sensorimotor cortex. J Neurophysiol 79:1102–1107

    PubMed  CAS  Google Scholar 

  • Paus T, Castro-Alamancos MA, Petrides M (2001a) Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation. Eur J Neurosci 14:1405–1411

    Article  PubMed  CAS  Google Scholar 

  • Paus T, Sipila PK, Strafella AP (2001b) Synchronization of neuronal activity in the human primary motor cortex by transcranial magnetic stimulation: an EEG study. J Neurophysiol 86:1983–1990

    PubMed  CAS  Google Scholar 

  • Penny WD, Stephan KE, Mechelli A, Friston KJ (2004a) Modelling functional integration: a comparison of structural equation and dynamic causal models. Neuroimage 23(suppl 1):S264–S274

    Google Scholar 

  • Penny WD, Stephan KE, Mechelli A, Friston KJ (2004b) Comparing dynamic causal models. Neuroimage 22:1157–1172

    Article  PubMed  CAS  Google Scholar 

  • Pleger B, Blankenburg F, Bestmann S, Ruff CC, Wiech K, Stephan KE, Friston KJ, Dolan RJ (2006a) Repetitive transcranial magnetic stimulation-induced changes in sensorimotor coupling parallel improvements of somatosensation in humans. J Neurosci 26:1945–1952

    Article  PubMed  CAS  Google Scholar 

  • Pleger B, Ruff CC, Blankenburg F, Bestmann S, Wiech K, Stephan KE, Capilla A, Friston KJ, Dolan RJ (2006b) Neural coding of tactile decisions in the human prefrontal cortex. J Neurosci 26:12596–12601

    Article  PubMed  CAS  Google Scholar 

  • Radovanovic S, Korotkov A, Ljubisavljevic M, Lyskov E, Thunberg J, Kataeva G, Danko S, Roudas M, Pakhomov S, Medvedev S, Johansson H (2002) Comparison of brain activity during different types of proprioceptive inputs: a positron emission tomography study. Exp Brain Res 143:276–285

    Article  PubMed  Google Scholar 

  • Reddy H, Floyer A, Donaghy M, Matthews PM (2001) Altered cortical activation with finger movement after peripheral denervation: comparison of active and passive tasks. Exp Brain Res 138:484–491

    Article  PubMed  CAS  Google Scholar 

  • Reis J, Swayne OB, Vandermeeren Y, Camus M, Dimyan MA, Harris-Love M, Perez MA, Ragert P, Rothwell JC, Cohen LG (2008) Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control. J Physiol 586:325–351

    Article  PubMed  CAS  Google Scholar 

  • Ridding MC, Rothwell JC (2007) Therapeutic use of rTMS. Nat Rev Neurosci 8:559–567

    Article  PubMed  CAS  Google Scholar 

  • Ridding MC, Taylor JL, Rothwell JC (1995) The effect of voluntary contraction on cortico-cortical inhibition in human motor cortex. J Physiol 487:541–548

    PubMed  CAS  Google Scholar 

  • Roberts DR, Vincent DJ, Speer AM, Bohning DE, Cure J, Young J, George MS (1997) Multi-modality mapping of motor cortex: comparing echoplanar BOLD fMRI and transcranial magnetic stimulation. Short communication. J Neural Transm 104:833–843

    Article  PubMed  CAS  Google Scholar 

  • Roebroeck A, Formisano E, Goebel R (2005) Mapping directed influence over the brain using Granger causality and fMRI. Neuroimage 25:230–242

    Article  PubMed  Google Scholar 

  • Romaiguere P, Anton JL, Roth M, Casini L, Roll JP (2003) Motor and parietal cortical areas both underlie kinaesthesia. Brain Res Cogn Brain Res 16:74–82

    Article  PubMed  Google Scholar 

  • Romei V, Murray MM, Merabet LB, Thut G (2007) Occipital transcranial magnetic stimulation has opposing effects on visual and auditory stimulus detection: implications for multisensory interactions. J Neurosci 27:11465–11472

    Article  PubMed  CAS  Google Scholar 

  • Romei V, Rihs T, Brodbeck V, Thut G (2008) Resting electroencephalogram alpha-power over posterior sites indexes baseline visual cortex excitability. Neuroreport 19:203–208

    Article  PubMed  Google Scholar 

  • Rosen G, Hugdahl K, Ersland L, Lundervold A, Smievoll AI, Barndon R, Sundberg H, Thomsen T, Roscher BE, Tjolsen A, Engelsen B (2001) Different brain areas activated during imagery of painful and non-painful ‘finger movements’ in a subject with an amputated arm. Neurocase 7:255–260

    Article  PubMed  CAS  Google Scholar 

  • Roth BJ, Cohen LG, Hallett M (1991a) The electric field induced during magnetic stimulation. Electroencephalogr Clin Neurophysiol Suppl 43:268–278

    PubMed  CAS  Google Scholar 

  • Roth BJ, Saypol JM, Hallett M, Cohen LG (1991b) A theoretical calculation of the electric field induced in the cortex during magnetic stimulation. Electroencephalogr Clin Neurophysiol 81:47–56

    Article  PubMed  CAS  Google Scholar 

  • Rothwell JC (1997) Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods 74:113–122

    Article  PubMed  CAS  Google Scholar 

  • Rothwell JC (1999) Paired-pulse investigations of short-latency intracortical facilitation using TMS in humans. Electroencephalogr Clin Neurophysiol Suppl 51:113–119

    PubMed  CAS  Google Scholar 

  • Rounis E, Stephan KE, Lee L, Siebner HR, Pesenti A, Friston KJ, Rothwell JC, Frackowiak RS (2006) Acute changes in frontoparietal activity after repetitive transcranial magnetic stimulation over the dorsolateral prefrontal cortex in a cued reaction time task. J Neurosci 26:9629–9638

    Article  PubMed  CAS  Google Scholar 

  • Ruff CC, Blankenburg F, Bjoertomt O, Bestmann S, Freeman E, Haynes JD, Rees G, Josephs O, Deichmann R, Driver J (2006) Concurrent TMS–fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Curr Biol 16:1479–1488

    Article  PubMed  CAS  Google Scholar 

  • Ruff CC, Bestmann S, Blankenburg F, Bjoertomt O, Josephs O, Weiskopf N, Deichmann R, Driver J (2008a) Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS fMRI. Cereb Cortex 18:817–827

    Article  PubMed  Google Scholar 

  • Ruff CC, Blankenburg F, Bjoertomt O, Bestmann S, Weiskopf N, Driver J (2008b) Hemispheric Differences in Frontal and Parietal Influences on the Human Occipital Cortex: Direct Confirmation with Concurrent TMS–fMRI. J Cogn Neurosci (in press)

  • Rushworth MF, Johansen-Berg H, Gobel SM, Devlin JT (2003) The left parietal and premotor cortices: motor attention and selection. Neuroimage 20(suppl 1):S89–S100

    Google Scholar 

  • Sack AT, Camprodon JA, Pascual-Leone A, Goebel R (2005) The dynamics of interhemispheric compensatory processes in mental imagery. Science 308:702–704

    Article  PubMed  CAS  Google Scholar 

  • Sack AT (2006) Transcranial magnetic stimulation, causal structure-function mapping and networks of functional relevance. Curr Opin Neurobiol 16:593–599

    Article  PubMed  CAS  Google Scholar 

  • Sack AT, Kohler A, Bestmann S, Linden DE, Dechent P, Goebel R, Baudewig J (2007) Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous FMRI, TMS, and behavioral studies. Cereb Cortex 17:2841–2852

    Article  PubMed  Google Scholar 

  • Sack AT, Sperling JM, Prvulovic D, Formisano E, Goebel R, Di Salle F, Dierks T, Linden DE (2002) Tracking the mind’s image in the brain II: transcranial magnetic stimulation reveals parietal asymmetry in visuospatial imagery. Neuron 35:195–204

    Article  PubMed  CAS  Google Scholar 

  • Schafer RJ, Moore T (2007) Attention governs action in the primate frontal eye field. Neuron 56:541–551

    Article  PubMed  CAS  Google Scholar 

  • Schluppeck D, Curtis CE, Glimcher PW, Heeger DJ (2006) Sustained activity in topographic areas of human posterior parietal cortex during memory-guided saccades. J Neurosci 26:5098–5108

    Article  PubMed  CAS  Google Scholar 

  • Schluter ND, Krams M, Rushworth MF, Passingham RE (2001) Cerebral dominance for action in the human brain: the selection of actions. Neuropsychologia 39:105–113

    Article  PubMed  CAS  Google Scholar 

  • Seyal M, Ro T, Rafal R (1995) Increased sensitivity to ipsilateral cutaneous stimuli following transcranial magnetic stimulation of the parietal lobe. Ann Neurol 38:264–267

    Article  PubMed  CAS  Google Scholar 

  • Shmuel A, Augath M, Oeltermann A, Logothetis NK (2006) Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 9:569–577

    Article  PubMed  CAS  Google Scholar 

  • Siebner HR, Peller M, Willoch F, Auer C, Bartenstein P, Drzezga A, Schwaiger M, Conrad B (1999) Imaging functional activation of the auditory cortex during focal repetitive transcranial magnetic stimulation of the primary motor cortex in normal subjects. Neurosci Lett 270:37–40

    Article  PubMed  CAS  Google Scholar 

  • Siebner HR, Peller M, Willoch F, Minoshima S, Boecker H, Auer C, Drzezga A, Conrad B, Bartenstein P (2000) Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology 54:956–963

    PubMed  CAS  Google Scholar 

  • Siebner HR, Rothwell J (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148:1–16

    Article  PubMed  Google Scholar 

  • Siebner HR, Filipovic SR, Rowe JB, Cordivari C, Gerschlager W, Rothwell JC, Frackowiak RS, Bhatia KP (2003a) Patients with focal arm dystonia have increased sensitivity to slow-frequency repetitive TMS of the dorsal premotor cortex. Brain 126:2710–2725

    Article  PubMed  Google Scholar 

  • Siebner HR, Peller M, Lee L (2003b) Applications of combined TMS-PET studies in clinical and basic research. Suppl Clin Neurophysiol 56:63–72

    PubMed  Google Scholar 

  • Siebner HR, Peller M, Lee L (2008) TMS and positron emission tomography: methods and current advances. In: Wasserman EM, Epstein CM, Ziemann U, Walsh V, Paus T, Lisanby SH (eds) The Oxford handbook of transcranial magnetic stimulation. Oxford University Press, Oxford, pp 549–567

    Google Scholar 

  • Siebner HR, Takano B, Peinemann A, Schwaiger M, Conrad B, Drzezga A (2001) Continuous transcranial magnetic stimulation during positron emission tomography: a suitable tool for imaging regional excitability of the human cortex. Neuroimage 14:883–890

    Article  PubMed  CAS  Google Scholar 

  • Siebner HR, Willoch F, Peller M, Auer C, Boecker H, Conrad B, Bartenstein P (1998) Imaging brain activation induced by long trains of repetitive transcranial magnetic stimulation. Neuroreport 9:943–948

    Article  PubMed  CAS  Google Scholar 

  • Silvanto J, Muggleton NG, Cowey A, Walsh V (2007) Neural activation state determines behavioral susceptibility to modified theta burst transcranial magnetic stimulation. Eur J Neurosci 26:523–528

    Article  PubMed  Google Scholar 

  • Speer AM, Willis MW, Herscovitch P, Daube-Witherspoon M, Shelton JR, Benson BE, Post RM, Wassermann EM (2003) Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H215O positron emission tomography: II. Effects of prefrontal cortex rTMS. Biol Psychiatry 54:826–832

    Article  PubMed  Google Scholar 

  • Stefanovic B, Warnking JM, Pike GB (2004) Hemodynamic and metabolic responses to neuronal inhibition. Neuroimage 22:771–778

    Article  PubMed  Google Scholar 

  • Stephan KE, Penny WD, Marshall JC, Fink GR, Friston KJ (2005) Investigating the functional role of callosal connections with dynamic causal models. Ann NY Acad Sci 1064:16–36

    Article  PubMed  Google Scholar 

  • Stephan KE, Kasper L, Harrison LM, Daunizeau J, den Ouden HE, Breakspear M, Friston KJ (2008) Nonlinear dynamic causal models for fMRI. Neuroimage 42:649–662

    Article  PubMed  Google Scholar 

  • Strafella AP, Paus T, Barrett J, Dagher A (2001) Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci 21:RC157

    Google Scholar 

  • Strafella AP, Paus T, Fraraccio M, Dagher A (2003) Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain 126:2609–2615

    Article  PubMed  Google Scholar 

  • Strens LH, Oliviero A, Bloem BR, Gerschlager W, Rothwell JC, Brown P (2002) The effects of subthreshold 1 Hz repetitive TMS on cortico-cortical and interhemispheric coherence. Clin Neurophysiol 113:1279–1285

    Article  PubMed  Google Scholar 

  • Swayne O, Bestmann S, Blankenburg F, Ruff CC, Teo JT, Weiskopf N, Driver J, Frackowiak R, Rothwell JC, Ward NS. (2006) The role of contralesional premotor cortex after stroke. 559.8. 2006. Society for Neuroscience

  • Taylor PC, Nobre AC, Rushworth MF (2007a) FEF TMS affects visual cortical activity. Cereb Cortex 17:391–399

    Article  PubMed  Google Scholar 

  • Taylor PC, Nobre AC, Rushworth MF (2007b) Subsecond changes in top down control exerted by human medial frontal cortex during conflict and action selection: a combined transcranial magnetic stimulation electroencephalography study. J Neurosci 27:11343–11353

    Article  PubMed  CAS  Google Scholar 

  • Tegenthoff M, Ragert P, Pleger B, Schwenkreis P, Forster AF, Nicolas V, Dinse HR (2005) Improvement of tactile discrimination performance and enlargement of cortical somatosensory maps after 5 Hz rTMS. PLoS Biol 3:e362

    Article  PubMed  CAS  Google Scholar 

  • Tehovnik EJ, Tolias AS, Sultan F, Slocum WM, Logothetis NK (2006) Direct and indirect activation of cortical neurons by electrical microstimulation. J Neurophysiol 96:512–521

    Article  PubMed  CAS  Google Scholar 

  • Tolias AS, Sultan F, Augath M, Oeltermann A, Tehovnik EJ, Schiller PH, Logothetis NK (2005) Mapping cortical activity elicited with electrical microstimulation using FMRI in the macaque. Neuron 48:901–911

    Article  PubMed  CAS  Google Scholar 

  • Tootell RB, Hadjikhani NK, Vanduffel W, Liu AK, Mendola JD, Sereno MI, Dale AM (1998) Functional analysis of primary visual cortex (V1) in humans. Proc Natl Acad Sci USA 95:811–817

    Article  PubMed  CAS  Google Scholar 

  • Touge T, Gerschlager W, Brown P, Rothwell JC (2001) Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clin Neurophysiol 112:2138–2145

    Article  PubMed  CAS  Google Scholar 

  • Valero-Cabre A, Payne BR, Rushmore J, Lomber SG, Pascual-Leone A (2005) Impact of repetitive transcranial magnetic stimulation of the parietal cortex on metabolic brain activity: a 14C–2DG tracing study in the cat. Exp Brain Res 163:1–12

    Article  PubMed  Google Scholar 

  • Virtanen J, Ruohonen J, Naatanen R, Ilmoniemi RJ (1999) Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Med Biol Eng Comput 37:322–326

    Article  PubMed  CAS  Google Scholar 

  • Wagner T, Valero-Cabre A, Pascual-Leone A (2007) Noninvasive human brain stimulation. Annu Rev Biomed Eng 9:527–565

    Article  PubMed  CAS  Google Scholar 

  • Walsh V, Cowey A (2000) Transcranial magnetic stimulation and cognitive neuroscience. Nat Rev Neurosci 1:73–79

    Article  PubMed  CAS  Google Scholar 

  • Worsley KJ, Cao J, Paus T, Petrides M, Evans AC (1998) Applications of random field theory to functional connectivity. Hum Brain Mapp 6:364–367

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U, Rothwell JC (2000) I-waves in motor cortex. J Clin Neurophysiol 17:397–405

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U (2004a) TMS and drugs. Clin Neurophysiol 115:1717–1729

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U (2004b) TMS induced plasticity in human cortex. Rev Neurosci 15:253–266

    PubMed  Google Scholar 

  • Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996) Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:367–378

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U, Tergau F, Wischer S, Hildebrandt J, Paulus W (1998) Pharmacological control of facilitatory I-wave interaction in the human motor cortex. A paired transcranial magnetic stimulation study. Electroencephalogr Clin Neurophysiol 109:321–330

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U, Meintzschel F, Korchounov A, Ilic TV (2006) Pharmacological modulation of plasticity in the human motor cortex. Neurorehabil Neural Repair 20:243–251

    Article  PubMed  Google Scholar 

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Acknowledgments

The support of the Wellcome Trust and Medical Research Council (MRC) is acknowledged. JD holds a Royal Society Leverhulme Senior Research Fellowship.

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Bestmann, S., Ruff, C.C., Blankenburg, F. et al. Mapping causal interregional influences with concurrent TMS–fMRI. Exp Brain Res 191, 383–402 (2008). https://doi.org/10.1007/s00221-008-1601-8

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