BRAIN STIMULATION: Basic, Translational, and Clinical Research in Neuromodulation
Volume 2, Issue 2 , Pages 58-80 , April 2009

Consensus paper: Combining transcranial stimulation with neuroimaging

  • Hartwig R. Siebner, MD

      Affiliations

    • Danish Research Center for Magnetic Resonance, Copenhagen University Hospital-Hvidovre, Denmark
    • Department of Neurology, Christian-Albrechts-University, Kiel, Germany
    • Corresponding Author InformationCorrespondence: Dr. Hartwig R. Siebner, Danish Research Center for Magnetic Resonance, Copenhagen University Hospital-Hvidovre, Kettegaards Alle 30, 2650 Hvidovre, Denmark.
    • ,
  • Til O. Bergmann, MD

      Affiliations

    • Department of Neurology, Christian-Albrechts-University, Kiel, Germany
    • ,
  • Sven Bestmann, MD

      Affiliations

    • Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square, London, UK
    • Wellcome Trust Center for Neuroimaging, Institute of Neurology, University College, London, UK
    • ,
  • Marcello Massimini, MD

      Affiliations

    • Department of Clinical Science, Faculty of Medicine, University of Milan, Italy
    • ,
  • Heidi Johansen-Berg, MD

      Affiliations

    • Centre for Functional Magnetic Resonance Imaging of the Brain, University of Oxford, Oxford, UK
    • Department of Clinical Neurology, University of Oxford, Oxford, UK
    • ,
  • Hitoshi Mochizuki, MD

      Affiliations

    • Department of Neurology, School of Medicine, Fukushima Medical University, Fukushima, Japan
    • ,
  • Daryl E. Bohning, MD

      Affiliations

    • Center for Advanced Imaging Research, Medical University of South Carolina, Charleston, South Carolina
    • Department of Radiology, Medical University of South Carolina, Charleston, South Carolina
    • ,
  • Erie D. Boorman, MD

      Affiliations

    • Centre for Functional Magnetic Resonance Imaging of the Brain, University of Oxford, Oxford, UK
    • ,
  • Sergiu Groppa, MD

      Affiliations

    • Department of Neurology, Christian-Albrechts-University, Kiel, Germany
    • ,
  • Carlo Miniussi, MD

      Affiliations

    • IRCCS S. Giovanni di Dio Fatebenefratelli, Brescia, Italy
    • Department of Biomedical Sciences and Biotechnology, National Institute of Neuroscience, University of Brescia, Brescia, Italy
    • ,
  • Alvaro Pascual-Leone, MD

      Affiliations

    • Department of Neurology, Berenson-Allen Center for Noninvasive Brain Stimulation, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts
    • ,
  • Reto Huber, MD

      Affiliations

    • University Children's Hospital, Zurich, Switzerland
    • ,
  • Paul C.J. Taylor, MD

      Affiliations

    • The Henry Wellcome Building, School of Psychology, Birkbeck College, Torrington Square, London, UK
    • ,
  • Risto J. Ilmoniemi, MD

      Affiliations

    • BioMag Laboratory, Helsinki University Central Hospital, Helsinki, Finland
    • Department of Biomedical Engineering and Computational Science, Helsinki University of Technology, Helsinki, Finland
    • ,
  • Luigi De Gennaro, MD

      Affiliations

    • IRCCS S. Giovanni di Dio Fatebenefratelli, Brescia, Italy
    • Department of Psychology, University of Rome ‘‘La Sapienza,’’ Rome, Italy
    • ,
  • Antonio P. Strafella, MD

      Affiliations

    • Movement Disorders Center, Toronto Western Hospital, Division of Neurology, University of Toronto, Ontario, Canada
    • ,
  • Seppo Kähkönen, MD

      Affiliations

    • BioMag Laboratory, Helsinki University Central Hospital, Helsinki, Finland
    • Pain Clinic, Helsinki University Central Hospital, Helsinki, Finland
    • ,
  • Stefan Klöppel, MD

      Affiliations

    • Department of Psychiatry and Psychotherapy, Freiburg Brain Imaging, University Clinic Freiburg, Freiburg, Germany
    • ,
  • Giovanni B. Frisoni, MD

      Affiliations

    • The National Centre for Alzheimer's and Mental Diseases, Brescia, Italy
    • ,
  • Mark S. George, MD

      Affiliations

    • Center for Advanced Imaging Research, Medical University of South Carolina, Charleston, South Carolina
    • Brain Stimulation Laboratory, Medical University of South Carolina, Charleston, South Carolina
    • ,
  • Mark Hallett, MD

      Affiliations

    • Human Motor Control Section, NINDS, NIH, Bethesda, Maryland
    • ,
  • Stephan A. Brandt, MD

      Affiliations

    • Department of Neurology, Berlin NeuroImaging Center, Charité, Berlin, Germany
    • ,
  • Matthew F. Rushworth, MD

      Affiliations

    • Department of Experimental Psychology, University of Oxford, Oxford, UK
    • ,
  • Ulf Ziemann, MD

      Affiliations

    • Department of Neurology, Goethe-University Frankfurt, Germany
    • ,
  • John C. Rothwell, MD

      Affiliations

    • Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square, London, UK
    • ,
  • Nick Ward, MD

      Affiliations

    • Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square, London, UK
    • Wellcome Trust Center for Neuroimaging, Institute of Neurology, University College, London, UK
    • ,
  • Leonardo G. Cohen, MD

      Affiliations

    • Human Cortical Physiology and Stroke Neurorehabilitation Section, National Institute of Health, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland
    • ,
  • Jürgen Baudewig, MD

      Affiliations

    • MR-Research in Neurology and Psychiatry, Medical Faculty, Georg-August University, Goettingen, Germany
    • ,
  • Tomáš Paus, MD

      Affiliations

    • Brain and Body Centre, University of Nottingham, Nottingham, UK
    • Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada
    • ,
  • Yoshikazu Ugawa, MD

      Affiliations

    • Department of Neurology, School of Medicine, Fukushima Medical University, Fukushima, Japan
    • ,
  • Paolo M. Rossini, MD

      Affiliations

    • Casa di Cura S. Raffaele Cassino and IRCCS S. Raffaele Pisana, Roma, Italy
    • AFaR, Department of Neuroscience, Hosp. Fatebenefratelli, Isola Tiberina, Rome, Italy
    • Neurology Clinic, University Campus Biomedico, Rome, Italy

Received 21 October 2008 ,Accepted 30 November 2008.

References 

  1. Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet. 1985;1(8437):1106–1107
  2. Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol. 2003;2(3):145–156
  3. Pascual-Leone A, Walsh V, Rothwell J. Transcranial magnetic stimulation in cognitive neuroscience–virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol. 2000;10(2):232–237
  4. Walsh V, Cowey A. Transcranial magnetic stimulation and cognitive neuroscience. Nature Rev. 2000;1(1):73–79
  5. Jahanshahi M, Dirnberger G. The left dorsolateral prefrontal cortex and random generation of responses: studies with transcranial magnetic stimulation. Neuropsychologia. 1999;37(2):181–190
  6. Grosbras MH, Paus T. Transcranial magnetic stimulation of the human frontal eye field facilitates visual awareness. Eur J Neurosci. 2003;18(11):3121–3126
  7. Walsh V, Ellison A, Battelli L, Cowey A. Task-specific impairments and enhancements induced by magnetic stimulation of human visual area V5. Proc Biol Sci. 1998;265(1395):537–543
  8. O'Shea J, Taylor PC, Rushworth MF. Imaging causal interactions during sensorimotor processing. Cortex. 2008;44(5):598–608
  9. Thickbroom GW. Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Exp Brain Res. 2007;180(4):583–593
  10. Ziemann U, Paulus W, Nitsche MA, et al. Consensus: motor cortex plasticity protocols. Brain Stimulation. 2008;1(3):164–182
  11. Siebner HR, Lang N, Rizzo V, et al. Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci. 2004;24(13):3379–3385
  12. Siebner HR, Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res. 2003;148(1):1–16
  13. Ridding MC, Rothwell JC. Is there a future for therapeutic use of transcranial magnetic stimulation?. Nature Rev. 2007;8(7):559–567
  14. Siebner HR, Hartwigsen G, Kassuba T, Rothwell JC. How does transcranial magnetic stimulation modify neuronal activity in the brain?—implications for studies of cognition. Cortex [in press].
  15. Siebner HR, Filipovic SR, Rowe JB, et al. Patients with focal arm dystonia have increased sensitivity to slow-frequency repetitive TMS of the dorsal premotor cortex. Brain. 2003;126(Pt 12):2710–2725
  16. Lee L, Siebner HR, Rowe JB, et al. Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J Neurosci. 2003;23(12):5308–5318
  17. O'Shea J, Johansen-Berg H, Trief D, Gobel S, Rushworth MF. Functionally specific reorganization in human premotor cortex. Neuron. 2007;54(3):479–490
  18. Brandt SA, Brocke J, Roricht S, Ploner CJ, Villringer A, Meyer BU. In vivo assessment of human visual system connectivity with transcranial electrical stimulation during functional magnetic resonance imaging. Neuroimage. 2001;14(2):366–375
  19. Brocke J, Schmidt S, Irlbacher K, Cichy RM, Brandt SA. Transcranial cortex stimulation and fMRI: electrophysiological correlates of dual-pulse BOLD signal modulation. Neuroimage. 2008;40(2):631–643
  20. Siebner HR, Peller M, Willoch F, et al. Imaging functional activation of the auditory cortex during focal repetitive transcranial magnetic stimulation of the primary motor cortex in normal subjects. Neurosci Lett. 1999;270(1):37–40
  21. Cohen LG, Celnik P, Pascual-Leone A, et al. Functional relevance of cross-modal plasticity in blind humans. Nature. 1997;389(6647):180–183
  22. Neggers SF, Huijbers W, Vrijlandt CM, Vlaskamp BN, Schutter DJ, Kenemans JL. TMS pulses on the frontal eye fields break coupling between visuospatial attention and eye movements. J Neurophysiol. 2007;98(5):2765–2778
  23. Ilmoniemi RJ, Virtanen J, Ruohonen J, et al. Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport. 1997;8(16):3537–3540
  24. Virtanen J, Ruohonen J, Naatanen R, Ilmoniemi RJ. Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Med Biol Eng Comput. 1999;37(3):322–326
  25. Thut G, Ives JR, Kampmann F, Pastor MA, Pascual-Leone A. A new device and protocol for combining TMS and online recordings of EEG and evoked potentials. J Neurosci Methods. 2005;141(2):207–217
  26. Bonato C, Miniussi C, Rossini PM. Transcranial magnetic stimulation and cortical evoked potentials: a TMS/EEG co-registration study. Clin Neurophysiol. 2006;117(8):1699–1707
  27. Taylor PC, Walsh V, Eimer M. Combining TMS and EEG to study cognitive function and cortico-cortico interactions. Behav Brain Res. 2008;191(2):141–147
  28. Roth BJ, Pascual-Leone A, Cohen LG, Hallett M. The heating of metal electrodes during rapid-rate magnetic stimulation: a possible safety hazard. Electroencephalogr Clin Neurophysiol. 1992;85(2):116–123
  29. Ives JR, Rotenberg A, Poma R, Thut G, Pascual-Leone A. Electroencephalographic recording during transcranial magnetic stimulation in humans and animals. Clin Neurophysiol. 2006;117(8):1870–1875
  30. Julkunen P, Paakkonen A, Hukkanen T, et al. Efficient reduction of stimulus artefact in TMS-EEG by epithelial short-circuiting by mini-punctures. Clin Neurophysiol. 2008;119(2):475–481
  31. Nikouline V, Ruohonen J, Ilmoniemi RJ. The role of the coil click in TMS assessed with simultaneous EEG. Clin Neurophysiol. 1999;110(8):1325–1328
  32. Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G. Breakdown of cortical effective connectivity during sleep. Science. 2005;309(5744):2228–2232
  33. Komssi S, Aronen HJ, Huttunen J, et al. Ipsi- and contralateral EEG reactions to transcranial magnetic stimulation. Clin Neurophysiol. 2002;113(2):175–184
  34. Lioumis P, Kicic D, Savolainen P, Makela JP, Kahkonen S. Reproducibility of TMS-Evoked EEG responses. Hum Brain Mapp. 2008 Jun 6;[Published online ahead of print]
  35. Ruohonen J, Ilmoniemi RJ. Modeling of the stimulating field generation in TMS. Electroencephalogr Clin Neurophysiol. 1999;51:30–40
  36. De Lucia M, Parker GJ, Embleton K, Newton JM, Walsh V. Diffusion tensor MRI-based estimation of the influence of brain tissue anisotropy on the effects of transcranial magnetic stimulation. NeuroImage. 2007;36(4):1159–1170
  37. Huber R, Esser SK, Ferrarelli F, Massimini M, Peterson MJ, Tononi G. TMS-induced cortical potentiation during wakefulness locally increases slow wave activity during sleep. PLoS ONE. 2007;2:e276
  38. Huber R, Maatta S, Esser SK, et al. Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep. J Neurosci. 2008;28(31):7911–7918
  39. Bergmann TO, Mölle M, Marshall L, Kaya-Yildiz L, Born J, Siebner HR. A local signature of LTP- and LTD-like plasticity in human NREM sleep. Eur J Neurosci. 2008;27(9):2241–2249
  40. De Gennaro L, Fratello F, Marzano C, et al. Cortical plasticity induced by transcranial magnetic stimulation during wakefulness affects electroencephalogram activity during sleep. PLoS ONE. 2008;3(6):e2483
  41. De Gennaro L, Marzano C, Veniero D, et al. Neurophysiological correlates of sleepiness: a combined TMS and EEG study. Neuroimage. 2007;36(4):1277–1287
  42. 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(9):2010–2018
  43. 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. 2001;86(4):1983–1990
  44. Brignani D, Manganotti P, Rossini PM, Miniussi C. Modulation of cortical oscillatory activity during transcranial magnetic stimulation. Hum Brain Mapp. 2008;29(5):603–612
  45. Fuggetta G, Pavone EF, 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):1–13
  46. Taylor PC, Nobre AC, Rushworth MF. FEF TMS affects visual cortical activity. Cereb Cortex. 2007;17(2):391–399
  47. Taylor PC, Nobre AC, Rushworth MF. 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. 2007;27(42):11343–11353
  48. Fuggetta G, Pavone EF, Walsh V, Kiss M, Eimer M. Cortico-cortical interactions in spatial attention: a combined ERP/TMS study. J Neurophysiol. 2006;95(5):3277–3280
  49. Komssi S, Kahkonen S. The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research. Brain Res Rev. 2006;52(1):183–192
  50. Lehmann D, Skrandies W. Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr Clin Neurophysiol. 1980;48(6):609–621
  51. 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. 2006;69(1):86–94
  52. Massimini M, Ferrarelli F, Esser SK, et al. Triggering sleep slow waves by transcranial magnetic stimulation. Proc Natl Acad Sci U S A. 2007;104(20):8496–8501
  53. Litvak V, Komssi S, Scherg 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):56–70
  54. Komssi S, Savolainen P, Heiskala J, Kahkonen S. Excitation threshold of the motor cortex estimated with transcranial magnetic stimulation electroencephalography. Neuroreport. 2007;18(1):13–16
  55. Fuggetta G, Fiaschi A, Manganotti P. Modulation of cortical oscillatory activities induced by varying single-pulse transcranial magnetic stimulation intensity over the left primary motor area: a combined EEG and TMS study. Neuroimage. 2005;27(4):896–908
  56. Kahkonen S, Kesaniemi M, Nikouline VV, et al. Ethanol modulates cortical activity: direct evidence with combined TMS and EEG. Neuroimage. 2001;14(2):322–328
  57. Kahkonen S, Wilenius J, Nikulin VV, Ollikainen M, Ilmoniemi RJ. Alcohol reduces prefrontal cortical excitability in humans: a combined TMS and EEG study. Neuropsychopharmacol. 2003;28(4):747–754
  58. Ferrarelli F, Massimini M, Peterson MJ, et al. Reduced evoked gamma oscillations in the frontal cortex in schizophrenia patients: a TMS/EEG study. Am J Psychiatry. 2008;165:996–1005
  59. Esser SK, Hill SL, Tononi G. Modeling the effects of transcranial magnetic stimulation on cortical circuits. J Neurophysiol. 2005;94(1):622–639
  60. Bohning DE, Shastri A, Nahas Z, et al. Echoplanar BOLD fMRI of brain activation induced by concurrent transcranial magnetic stimulation. Invest Radiol. 1998;33(6):336–340
  61. Ferrarelli F, Haraldsson HM, Barnhart TE, et al. A [17F]-fluoromethane PET/TMS study of effective connectivity. Brain Res Bull. 2004;64(2):103–113
  62. Logothetis NK. The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philos Trans R Soc Lond B Biol Sci. 2002;357(1424):1003–1037
  63. Formisano E, Goebel R. Tracking cognitive processes with functional MRI mental chronometry. Curr Opin Neurobio. 2003;13(2):174–181
  64. Josephs O, Henson RN. Event-related functional magnetic resonance imaging: modelling, inference and optimization. Philos Trans R Soc Lond B Biol Sci. 1999;354(1387):1215–1228
  65. Bohning DE, Shastri A, McConnell KA, et al. A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol Psychiatry. 1999;45(4):385–394
  66. Shastri A, George MS, Bohning DE. Performance of a system for interleaving transcranial magnetic stimulation with steady-state magnetic resonance imaging. Electroencephalogr Clin Neurophysiol Suppl. 1999;51:55–64
  67. Baudewig J, Paulus W, Frahm J. Artifacts caused by transcranial magnetic stimulation coils and EEG electrodes in T(2)∗-weighted echo-planar imaging. Magn Reson Imaging. 2000;18(4):479–484
  68. Bestmann S, Baudewig J, Frahm J. On the synchronization of transcranial magnetic stimulation and functional echo-planar imaging. J Magn Reson Imaging. 2003;17(3):309–316
  69. Denslow S, Bohning DE, Bohning PA, Lomarev MP, George MS. An increased precision comparison of TMS-induced motor cortex BOLD fMRI response for image-guided versus function-guided coil placement. Cogn Behav Neurol. 2005;18(2):119–126
  70. Bestmann S, Swayne O, Blankenburg F, et al. Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. Cereb Cortex. 2008;18(6):1281–1291
  71. Weiskopf N, Josephs O, Ruff CC. et al. Image artifacts in concurrent transcranial magnetic stimulation (TMS) and fMRI caused by leakage currents: Modeling and compensation. J Magn Reson Imaging [in press].
  72. Bestmann S, Ruff CC, Driver J, Blankenburg F. Concurrent TMS and functional magnetic resonance imaging: methods and current advances. In:  Wassermann EM,  Epstein CM,  Ziemann U,  Walsh V,  Paus T,  Lisanby S editor. The Oxford Handbook of Transcranial Stimulation. Oxford: Oxford University Press; 2008;p. 569–592
  73. Ruff CC, Bestmann S, Blankenburg F, et al. Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. Cereb Cortex. 2008;18(4):817–827
  74. Bestmann S, Ruff CC, Blankenburg F, Weiskopf W, Driver J, Rothwell JC. Mapping causal interregional influences with concurrent TMS-fMRI. Exp Brain Res. 2008;191:383–402
  75. Paus T. Inferring causality in brain images: a perturbation approach. Philos Trans R Soc Lond B Biol Sci. 2005;360(1457):1109–1114
  76. Bohning DE, Shastri A, Wassermann EM, et al. BOLD-f MRI response to single-pulse transcranial magnetic stimulation (TMS). J Magn Reson Imaging. 2000;11(6):569–574
  77. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J. BOLD MRI responses to repetitive TMS over human dorsal premotor cortex. Neuroimage. 2005;28(1):22–29
  78. Denslow S, Lomarev M, George MS, Bohning DE. Cortical and subcortical brain effects of transcranial magnetic stimulation (TMS)-induced movement: an interleaved TMS/functional magnetic resonance imaging study. Biol Psychiatry. 2005;57(7):752–760
  79. 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. 2003;20(3):1685–1696
  80. 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(7):1950–1962
  81. Ruff CC, Blankenburg F, Bjoertomt O, et al. Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Curr Biol. 2006;16(15):1479–1488
  82. Sack AT, Kohler A, Bestmann S, et al. Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous FMRI, TMS, and behavioral studies. Cereb Cortex. 2007;17(12):2841–2852
  83. Blankenburg F, Ruff CC, Bestmann S, et al. Interhemispheric effect of parietal TMS on somatosensory response confirmed directly with concurrent TMS-fMRI. J Neurosci. 2008;28(49):13202–13208
  84. Bestmann S, Oliviero A, Voss M, et al. Cortical correlates of TMS-induced phantom hand movements revealed with concurrent TMS-fMRI. Neuropsychologia. 2006;44(14):2959–2971
  85. Friston KJ, Price CJ. Degeneracy and redundancy in cognitive anatomy. Trends Cogn Sci. 2003;7(4):151–152
  86. Li X, Nahas Z, Kozel FA, Anderson B, Bohning DE, George MS. 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. 2004;55(9):882–890
  87. Li X, Teneback CC, Nahas Z, et al. Interleaved transcranial magnetic stimulation/functional MRI confirms that lamotrigine inhibits cortical excitability in healthy young men. Neuropsychopharmacol. 2004;29(7):1395–1407
  88. Tegenthoff M, Ragert P, Pleger B, et al. Improvement of tactile discrimination performance and enlargement of cortical somatosensory maps after 5 Hz rTMS. PLoS Biol. 2005;3(11):e362
  89. Pleger B, Blankenburg F, Bestmann S, et al. Repetitive transcranial magnetic stimulation-induced changes in sensorimotor coupling parallel improvements of somatosensation in humans. J Neurosci. 2006;26(7):1945–1952
  90. Rango M, Cogiamanian F, Marceglia S, et al. Myoinositol content in the human brain is modified by transcranial direct current stimulation in a matter of minutes: a 1H-MRS study. Magn Reson Med. 2008;60(4):782–789
  91. Stagg CJ, Best J, Stephenson M, et al. Imaging the functional and neurochemical effects of transcranial direct current stimulation: a rationale for rehabilitation (Abstract). Special issue: Proceedings from the Third International Conference on TMS and tDCS. October 1-4, Göttingen, Germany. Brain Stimulation. 2008;1(3):260–261
  92. Moisa M, Pohmann R, Uludag K, Thielscher A. Interleaved TMS/CASL: a motor cortex study (Abstract). Special Issue: Proceedings from the Third International Conference on TMS and tDCS. October 1-4, Göttingen, Germany. Brain Stimulation. 2008;1(3):290–291
  93. Bohning DE, Pecheny AP, Epstein CM, et al. Mapping transcranial magnetic stimulation (TMS) fields in vivo with MRI. Neuroreport. 1997;8(11):2535–2538
  94. Ashburner J, Friston KJ. Voxel-based morphometry–the methods. Neuroimage. 2000;11(6 Pt 1):805
  95. Ashburner J, Csernansky JG, Davatzikos C, Fox NC, Frisoni GB, Thompson PM. Computer-assisted imaging to assess brain structure in healthy and diseased brains. Lancet Neurol. 2003;2(2):79–88
  96. Boorman ED, O'Shea J, Sebastian C, Rushworth MF, Johansen-Berg H. Individual differences in white-matter microstructure reflect variation in functional connectivity during choice. Curr Biol. 2007;17(16):1426–1431
  97. Wahl M, Lauterbach-Soon B, Hattingen E, et al. Human motor corpus callosum: topography, somatotopy, and link between microstructure and function. J Neurosci. 2007;27(45):12132–12138
  98. Stinear CM, Barber PA, Smale PR, Coxon JP, Fleming MK, Byblow WD. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain. 2007;130(Pt 1):170–180
  99. Kloppel S, Baumer T, Kroeger J, et al. The cortical motor threshold reflects microstructural properties of cerebral white matter. Neuroimage. 2008;40(4):1782–1791
  100. Smith SM, Jenkinson M, Johansen-Berg H, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage. 2006;31(4):1487–1505
  101. Silbert LC, Nelson C, Holman S, et al. Cortical excitability and age-related volumetric MRI changes. Clin Neurophysiol. 2006;117(5):1029–1036
  102. Sach M, Winkler G, Glauche V, et al. Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. Brain. 2004;127(Pt 2):340–350
  103. Piccini P, Whone A. Functional brain imaging in the differential diagnosis of Parkinson's disease. Lancet Neuro. 2004;3(5):284–290
  104. Herholz K, Heiss WD. Positron emission tomography in clinical neurology. Mol Imaging Biol. 2004;6(4):239–269
  105. Cagnin A, Gerhard A, Banati RB. In vivo imaging of neuroinflammation. Eur Neuropsychopharmacol. 2002;12(6):581–586
  106. Hayashi T, Ohnishi T, Okabe S, et al. Long-term effect of motor cortical repetitive transcranial magnetic stimulation. [correction] Ann Neurol. 2004;56(1):77–85
  107. Thompson CJ, Paus T, Clancy R. Magnetic schielding requirements for PET detectors during transcranial magnetic stimulation. IEEE Trans Nuclear Sci. 1998;20:1923–1927
  108. Siebner HR, Peller M, Lee L. TMS and positron emission tomography: methods and current advances. In:  Wassermann EM,  Epstein CM,  Ziemann U,  Walsh V,  Paus T,  Lisanby S editor. The Oxford Handbook of Transcranial Stimulation. Oxford: Oxford University Press; 2008;p. 549–567
  109. 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(9):3178–3184
  110. Paus T, Wolforth M. Transcranial magnetic stimulation during PET: reaching and verifying the target site. Hum Brain Mapp. 1998;6(5-6):399–402
  111. Siebner H, Peller M, Bartenstein P, et al. Activation of frontal premotor areas during suprathreshold transcranial magnetic stimulation of the left primary sensorimotor cortex: a glucose metabolic PET study. Hum Brain Mapp. 2001;12(3):157–167
  112. Speer AM, Willis MW, Herscovitch P, et al. 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. 2003;54(8):826–832
  113. Speer AM, Willis MW, Herscovitch P, et al. Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H215O positron emission tomography: I, effects of primary motor cortex rTMS. Biol Psychiatry. 2003;54(8):818–825
  114. Siebner HR, Takano B, Peinemann A, Schwaiger M, Conrad B, Drzezga A. Continuous transcranial magnetic stimulation during positron emission tomography: a suitable tool for imaging regional excitability of the human cortex. Neuroimage. 2001;14(4):883–890
  115. Mottaghy FM, Krause BJ, Kemna LJ, et al. Modulation of the neuronal circuitry subserving working memory in healthy human subjects by repetitive transcranial magnetic stimulation. Neurosci Lett. 2000;280(3):167–170
  116. Mottaghy FM, Pascual-Leone A, Kemna LJ, et al. Modulation of a brain-behavior relationship in verbal working memory by rTMS. Brain Res Cogn Brain Res. 2003;15(3):241–249
  117. Siebner HR, Peller M, Lee L. Applications of combined TMS-PET studies in clinical and basic research. Suppl Clin Neurophysiol. 2003;56:63–72
  118. Chouinard PA, Van Der Werf YD, Leonard G, Paus T. Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. J Neurophysiol. 2003;90(2):1071–1083
  119. Takano B, Drzezga A, Peller M, et al. Short-term modulation of regional excitability and blood flow in human motor cortex following rapid-rate transcranial magnetic stimulation. Neuroimage. 2004;23(3):849–859
  120. Rounis E, Lee L, Siebner HR, et al. Frequency specific changes in regional cerebral blood flow and motor system connectivity following rTMS to the primary motor cortex. Neuroimage. 2005;26(1):164–176
  121. 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. 2001;14(8):1405–1411
  122. Catafau AM, Perez V, Gironell A, et al. SPECT mapping of cerebral activity changes induced by repetitive transcranial magnetic stimulation in depressed patients: a pilot study. Psychiatry Res. 2001;106(3):151–160
  123. Nadeau SE, McCoy KJ, Crucian GP, et al. Cerebral blood flow changes in depressed patients after treatment with repetitive transcranial magnetic stimulation: evidence of individual variability. Neuropsychiatry Neuropsychol Behav Neurol. 2002;15(3):159–175
  124. Shajahan PM, Glabus MF, Steele JD, et al. Left dorso-lateral repetitive transcranial magnetic stimulation affects cortical excitability and functional connectivity, but does not impair cognition in major depression. Prog Neuropsychopharmacol Biol Psychiatry. 2002;26(5):945–954
  125. Speer AM, Kimbrell TA, Wassermann EM, et al. Opposite effects of high and low frequency rTMS on regional brain activity in depressed patients. Biol Psychiatry. 2000;48(12):1133–1141
  126. George MS, Wassermann EM, Williams WA, et al. Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression. Neuroreport. 1995;6(14):1853–1856
  127. 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(15):RC157
  128. 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(Pt 12):2609–2615
  129. 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(11):2946–2952
  130. Pogarell O, Koch W, Popperl G, et al. Acute prefrontal rTMS increases striatal dopamine to a similar degree as D-amphetamine. Psychiatry Res. 2007;156(3):251–255
  131. Pogarell O, Koch W, Popperl G, et al. Striatal dopamine release after prefrontal repetitive transcranial magnetic stimulation in major depression: preliminary results of a dynamic [123I] IBZM SPECT study. J Psychiatr Res. 2006;40(4):307–314
  132. Keck ME, Welt T, Muller MB, et al. Repetitive transcranial magnetic stimulation increases the release of dopamine in the mesolimbic and mesostriatal system. Neuropharmacology. 2002;43(1):101–109
  133. Erhardt A, Sillaber I, Welt T, Muller MB, Singewald N, Keck ME. Repetitive transcranial magnetic stimulation increases the release of dopamine in the nucleus accumbens shell of morphine-sensitized rats during abstinence. Neuropsychopharmacology. 2004;29(11):2074–2080
  134. Kanno M, Matsumoto M, Togashi H, Yoshioka M, Mano Y. Effects of acute repetitive transcranial magnetic stimulation on dopamine release in the rat dorsolateral striatum. J Neurol Sci. 2004;217(1):73–81
  135. Ohnishi T, Hayashi T, Okabe S, et al. Endogenous dopamine release induced by repetitive transcranial magnetic stimulation over the primary motor cortex: an [11C]raclopride positron emission tomography study in anesthetized macaque monkeys. Biol Psychiatry. 2004;55(5):484–489
  136. de la Fuente-Fernandez R, Ruth TJ, Sossi V, Schulzer M, Calne DB, Stoessl AJ. Expectation and dopamine release: mechanism of the placebo effect in Parkinson's disease. Science. 2001;293(5532):1164–1166
  137. Strafella AP, Ko JH, Monchi O. Therapeutic application of transcranial magnetic stimulation in Parkinson's disease: the contribution of expectation. Neuroimage. 2006;31(4):1666–1672
  138. Villringer A, Chance B. Non-invasive optical spectroscopy and imaging of human brain function. Trends Neurosci. 1997;20(10):435–442
  139. Germon TJ, Evans PD, Barnett NJ, Wall P, Manara AR, Nelson RJ. Cerebral near infrared spectroscopy: emitter-detector separation must be increased. Br J Anaesth. 1999;82(6):831–837
  140. Oliviero A, Di Lazzaro V, Piazza O, et al. Cerebral blood flow and metabolic changes produced by repetitive magnetic brain stimulation. J Neurol. 1999;246(12):1164–1168
  141. Miyai I, Tanabe HC, Sase I, et al. Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage. 2001;14(5):1186–1192
  142. Wenzel R, Wobst P, Heekeren HH, et al. Saccadic suppression induces focal hypooxygenation in the occipital cortex. J Cereb Blood Flow Metab. 2000;20(7):1103–1110
  143. Nissilä I, Kotilahti K, Komssi S, et al. Optical measurement of hemodynamic changes in the contralateral motor cortex induced by transcranial magnetic stimulation. In:  Nowak H,  Haueisen J,  Gießler F,  Huonker R, edis  editor. Proceedings of the 13th International Conference on Biomagnetism (BIOMAG 2002). Berlin: VDE Verlag; 2002;p. 851–854
  144. 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(1):156–162
  145. Mochizuki H, Ugawa Y, Terao Y, Sakai KL. Cortical hemoglobin-oncentration changes under the coil induced by single-pulse TMS in humans: a simultaneous recording with near-infrared spectroscopy. Exp Brain Res 200;169(3):302–310.
  146. Mochizuki H, Furubayashi T, Hanajima R, et al. Hemoglobin concentration changes in the contralateral hemisphere during and after theta burst stimulation of the human sensorimotor cortices. Exp Brain Res. 2007;180(4):667–675
  147. Chiang TC, Vaithianathan T, Leung T, Lavidor M, Walsh V, Delpy DT. Elevated haemoglobin levels in the motor cortex following 1 Hz transcranial magnetic stimulation: a preliminary study. Exp Brain Res. 2007;181(4):555–560
  148. May A, Hajak G, Ganssbauer S, et al. Structural brain alterations following 5 days of intervention: dynamic aspects of neuroplasticity. Cereb Cortex. 2007;17(1):205–210
  149. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;45(2):201–206
  150. Rizzo V, Siebner HS, Morgante F, Mastroeni C, Girlanda P, Quartarone A. Paired associative stimulation of left and right human motor cortex shapes interhemispheric motor inhibition based on a Hebbian mechanism. Cereb Cortex. 2008 Sep 12;[Published online ahead of print.]
  151. Lang N, Siebner HR, Ward NS, et al. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain?. Eur J Neurosci. 2005;22(2):495–504

PII: S1935-861X(08)00361-6

doi: 10.1016/j.brs.2008.11.002

BRAIN STIMULATION: Basic, Translational, and Clinical Research in Neuromodulation
Volume 2, Issue 2 , Pages 58-80 , April 2009

Article Tools

* Image Usage & Resolution