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Combination of Transcranial Magnetic Stimulation (TMS) with Functional Magnetic Resonance Imaging

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Transcranial Magnetic Stimulation

Part of the book series: Neuromethods ((NM,volume 89))

Abstract

Transcranial magnetic stimulation (TMS) is a noninvasive brain stimulation and neuromodulation technique widely used in systems neurophysiology, cognitive neuroscience, and neuropsychiatry. Unlike other neuroimaging modalities, it is interventional and therefore able to establish causal relationships between brain activity and behavior. Despite the many advantages of independent TMS studies to demonstrate causal influence of brain areas on cognitive tasks, these studies assume TMS modulation of cortex underneath the coil but do not obtain any neurobiological measures. Multimodal approaches that combine TMS with neuroimaging, though technically challenging, are able to circumvent this problem. In this chapter, we will discuss the challenges, solutions, and applications of the combination of TMS with functional magnetic resonance imaging.

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References

  1. Sack AT (2006) Transcranial magnetic stimulation, causal structure-function mapping and networks of functional relevance. Curr Opin Neurobiol 16(5):593–599

    Article  CAS  PubMed  Google Scholar 

  2. Gugino LD, Romero JR, Aglio L, Titone D, Ramirez M, Pascual-Leone A et al (2001) Transcranial magnetic stimulation coregistered with MRI: a comparison of a guided versus blind stimulation technique and its effect on evoked compound muscle action potentials. Clin Neurophysiol 112(10):1781–1792

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Paus T (1996) Location and function of the human frontal eye-field: a selective review. Neuropsychologia 34(6):475–483

    Article  CAS  PubMed  Google Scholar 

  4. 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(9):3178–3184

    CAS  PubMed  Google Scholar 

  5. Sack AT, Cohen Kadosh R, Schuhmann T, Moerel M, Walsh V, Goebel R (2009) Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. J Cogn Neurosci 21(2):207–221

    Article  PubMed  Google Scholar 

  6. Bystritsky A, Kaplan JT, Feusner JD, Kerwin LE, Wadekar M, Burock M, Wu AD, Iacoboni M (2008) A preliminary study of fMRI-guided rTMS in the treatment of generalized anxiety disorder. J Clin Psychiatry 69(7):1092–1098

    Article  PubMed  Google Scholar 

  7. Fitzgerald PB, Hoy K, McQueen S, Maller JJ, Herring S, Segrave R, Bailey M, Been G, Kulkarni J, Daskalakis ZJ (2009) A randomized trial of rTMS targeted with MRI based neuro-navigation in treatment-resistant depression. Neuropsychopharmacology 34(5):1255–1262

    Article  PubMed  Google Scholar 

  8. George MS, Lisanby SH, Avery D, McDonald WM, Durkalski V, Pavlicova M et al (2010) Daily left prefrontal transcranial magnetic stimulation therapy for major depressive disorder: a sham-controlled randomized trial. Arch Gen Psychiatry 67(5):507–516

    Article  PubMed  Google Scholar 

  9. O’Reardon JP, Solvason HB, Janicak PG, Sampson S, Isenberg KE, Nahas Z et al (2007) Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multisite randomized controlled trial. Biol Psychiatry 62(11):1208–1216

    Article  PubMed  Google Scholar 

  10. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19(1):72–78

    Article  PubMed Central  PubMed  Google Scholar 

  11. Fox P, Ingham R, George MS, Mayberg H, Ingham J, Roby J et al (1997) Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport 8(12):2787–2791

    Article  CAS  PubMed  Google Scholar 

  12. O’Shea J, Sebastian C, Boorman ED, Johansen-Berg H, Rushworth MF (2007) Functional specificity of human premotor-motor cortical interactions during action selection. Eur J Neurosci 26(7):2085–2095

    Article  PubMed  Google Scholar 

  13. 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(12):5308–5318

    CAS  PubMed  Google Scholar 

  14. Pleger B, Blankenburg F, Bestmann S, Ruff CC, Wiech K, Stephan KE, Friston KJ, Dolan RJ (2006) Repetitive transcranial magnetic stimulation-induced changes in sensorimotor coupling parallel improvements of somatosensation in humans. J Neurosci 26(7):1945–1952

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Grefkes C, Nowak DA, Wang LE, Dafotakis M, Eickhoff SB, Fink GR (2010) Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. Neuroimage 50(1):233–242

    Article  PubMed  Google Scholar 

  16. 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(15):RC157

    CAS  PubMed  Google Scholar 

  17. Cho SS, Strafella AP (2009) rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS One 4(8):e6725

    Article  PubMed Central  PubMed  Google Scholar 

  18. Drevets WC, Savitz J, Trimble M (2008) The subgenual anterior cingulate cortex in mood disorders. CNS Spectr 13(8):663–681

    PubMed Central  PubMed  Google Scholar 

  19. Andoh J, Paus T (2011) Combining functional neuroimaging with off-line brain stimulation: modulation of task-related activity in language areas. J Cogn Neurosci 23(2):349–361

    Article  PubMed  Google Scholar 

  20. Mevorach C, Hodsoll J, Allen H, Shalev L, Humphreys G (2010) Ignoring the elephant in the room: a neural circuit to downregulate salience. J Neurosci 30(17):6072–6079

    Article  CAS  PubMed  Google Scholar 

  21. Nahas Z, Lomarev M, Roberts DR, Shastri A, Lorberbaum JP, Teneback C et al (2001) Unilateral left prefrontal transcranial magnetic stimulation (TMS) produces intensity-dependent bilateral effects as measured by interleaved BOLD fMRI. Biol Psychiatry 50(9):712–720

    Article  CAS  PubMed  Google Scholar 

  22. May A, Hajak G, Ganssbauer S, Steffens T, Langguth B, Kleinjung T, Eichhammer P (2007) Structural brain alterations following 5 days of intervention: dynamic aspects of neuroplasticity. Cereb Cortex 17(1):205–210

    Article  CAS  PubMed  Google Scholar 

  23. Ilmoniemi R, Aronen H (2000) Cortical excitability and connectivity reflected in fMRI, MEG, EEG and TMS. In: Moneen C, Bandettini P (eds) Functional MRI. Springer, New York, pp 453–463

    Chapter  Google Scholar 

  24. Ilmoniemi RJ, Virtanen J, Ruohonen J, Karhu J, Aronen HJ, Naatanen R et al (1997) Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 8(16):3537–3540

    Article  CAS  PubMed  Google Scholar 

  25. Izumi S, Takase M, Arita M, Masakado Y, Kimura A, Chino N (1997) Transcranial magnetic stimulation-induced changes in EEG and responses recorded from the scalp of healthy humans. Electroencephalogr Clin Neurophysiol 103(2):319–322

    Article  CAS  PubMed  Google Scholar 

  26. Paus T, Sipila PK, Strafella AP (2001) Synchronization of neuronal activity in the human primary motor cortex by transcranial magnetic stimulation: an EEG study. J Neurophysiol 86(4):1983–1990

    CAS  PubMed  Google Scholar 

  27. Thut G, Northoff G, Ives JR, Kamitani Y, Pfennig A, Kampmann F et al (2003) Effects of single-pulse transcranial magnetic stimulation (TMS) on functional brain activity: a combined event-related TMS and evoked potential study. Clin Neurophysiol 114(11):2071–2080

    Article  CAS  PubMed  Google Scholar 

  28. Thut G, Pascual-Leone A (2010) Integrating TMS with EEG: how and what for? Brain Topogr 22(4):215–218

    Article  PubMed  Google Scholar 

  29. Thut G, Theoret H, Pfennig A, Ives J, Kampmann F, Northoff G et al (2003) Differential effects of low-frequency rTMS at the occipital pole on visual-induced alpha desynchronization and visual-evoked potentials. Neuroimage 18(2):334–347

    Article  CAS  PubMed  Google Scholar 

  30. 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(3):322–326

    Article  CAS  PubMed  Google Scholar 

  31. Catafau AM, Perez V, Gironell A, Martin JC, Kulisevsky J, Estorch M et al (2001) SPECT mapping of cerebral activity changes induced by repetitive transcranial magnetic stimulation in depressed patients. A pilot study. Psychiatry Res 106(3):151–160

    Article  CAS  PubMed  Google Scholar 

  32. Mottaghy FM, Pascual-Leone A, Kemna LJ, Topper R, Herzog H, Muller-Gartner HW et al (2003) Modulation of a brain-behavior relationship in verbal working memory by rTMS. Brain Res Cogn Brain Res 15(3):241–249

    Article  PubMed  Google Scholar 

  33. 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(2):1102–1107

    CAS  PubMed  Google Scholar 

  34. Siebner HR, Peller M, Willoch F, Minoshima S, Boecker H, Auer C et al (2000) Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology 54(4):956–963

    Article  CAS  PubMed  Google Scholar 

  35. 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(4):883–890

    Article  CAS  PubMed  Google Scholar 

  36. Siebner HR, Willoch F, Peller M, Auer C, Boecker H, Conrad B et al (1998) Imaging brain activation induced by long trains of repetitive transcranial magnetic stimulation. Neuroreport 9(5):943–948

    Article  CAS  PubMed  Google Scholar 

  37. Speer AM, Willis MW, Herscovitch P, Daube-Witherspoon M, Shelton JR, Benson BE et al (2003) 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 54(8):818–825

    Article  PubMed  Google Scholar 

  38. Speer AM, Willis MW, Herscovitch P, Daube-Witherspoon M, Shelton JR, Benson BE et al (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(8):826–832

    Article  PubMed  Google Scholar 

  39. Bestmann S, Baudewig J, Frahm J (2003) On the synchronization of transcranial magnetic stimulation and functional echo-planar imaging. J Magn Reson Imaging 17(3):309–316

    Article  PubMed  Google Scholar 

  40. Friston K (1994) Functional and effective connectivity in neuroimaging: a synthesis. Hum Brain Mapp 2(1–2):56–78

    Article  Google Scholar 

  41. McIntosh AR, Nyberg L, Bookstein FL, Tulving E (1997) Differential functional connectivity of prefrontal and medial temporal cortices during episodic memory retrieval. Hum Brain Mapp 5(4):323–327

    Article  CAS  PubMed  Google Scholar 

  42. Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuroimage 19(4):1273–1302

    Article  CAS  PubMed  Google Scholar 

  43. Roebroeck A, Formisano E, Goebel R (2005) Mapping directed influence over the brain using Granger causality and fMRI. Neuroimage 25(1):230–242

    Article  PubMed  Google Scholar 

  44. Baudewig J, Siebner HR, Bestmann S, Tergau F, Tings T, Paulus W et al (2001) Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS). Neuroreport 12(16):3543–3548

    Article  CAS  PubMed  Google Scholar 

  45. 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(3):1685–1696

    Article  PubMed  Google Scholar 

  46. 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(7):1950–1962

    Article  PubMed  Google Scholar 

  47. Bohning DE, Shastri A, McConnell KA, Nahas Z, Lorberbaum JP, Roberts DR et al (1999) A combined TMS/fMRI study of intensity-dependent TMS over motor cortex. Biol Psychiatry 45(4):385–394

    Article  CAS  PubMed  Google Scholar 

  48. Bohning DE, Shastri A, Nahas Z, Lorberbaum JP, Andersen SW, Dannels WR et al (1998) Echoplanar BOLD fMRI of brain activation induced by concurrent transcranial magnetic stimulation. Invest Radiol 33(6):336–340

    Article  CAS  PubMed  Google Scholar 

  49. Bohning DE, Shastri A, McGavin L, McConnell KA, Nahas Z, Lorberbaum JP et al (2000) 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(11):676–683

    Article  CAS  PubMed  Google Scholar 

  50. Bohning DE, Shastri A, Wassermann EM, Ziemann U, Lorberbaum JP, Nahas Z et al (2000) BOLD-f MRI response to single-pulse transcranial magnetic stimulation (TMS). J Magn Reson Imaging 11(6):569–574

    Article  CAS  PubMed  Google Scholar 

  51. 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(7):752–760

    Article  PubMed  Google Scholar 

  52. Li X, Nahas Z, Kozel FA, Anderson B, Bohning DE, George MS (2004) 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(9):882–890

    Article  PubMed  Google Scholar 

  53. Nahas Z, DeBrux C, Chandler V, Lorberbaum JP, Speer AM, Molloy MA, Liberatos C, Risch SC, George MS (2000) Lack of significant changes on magnetic resonance scans before and after 2 weeks of daily left prefrontal repetitive transcranial magnetic stimulation for depression. J ECT 16(4):380–390

    Article  CAS  PubMed  Google Scholar 

  54. Ruff CC, Blankenburg F, Bjoertomt O, Bestmann S, Freeman E, Haynes JD et al (2006) Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Curr Biol 16(15):1479–1488

    Article  CAS  PubMed  Google Scholar 

  55. Camprodon JA, Sack AT, Pascual-Leone A (2010) Developing strategies for therapeutic neuromodulation: simultaneous Transcranial Magnetic Stimulation and functional Magnetic Resonance Imaging to study the mechanisms of Hemispatial Neglect recovery. In: 49th Annual Meeting of the American College of Neuro-psychopharmacology (ACNP), Miami, FL

    Google Scholar 

  56. Ruff CC, Bestmann S, Blankenburg F, Bjoertomt O, Josephs O, Weiskopf N et al (2008) Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. Cereb Cortex 18(4):817–827

    Article  PubMed Central  PubMed  Google Scholar 

  57. Ruff CC, Blankenburg F, Bjoertomt O, Bestmann S, Weiskopf N, Driver J (2009) Hemispheric differences in frontal and parietal influences on human occipital cortex: direct confirmation with concurrent TMS-fMRI. J Cogn Neurosci 21(6):1146–1161

    Article  PubMed Central  PubMed  Google Scholar 

  58. Sack AT, Kohler A, Bestmann S, Linden DE, Dechent P, Goebel R et al (2007) Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous FMRI, TMS, and behavioral studies. Cereb Cortex 17(12):2841–2852

    Article  PubMed  Google Scholar 

  59. Bestmann S, Ruff CC, Blankenburg F, Weiskopf N, Driver J, Rothwell JC (2008) Mapping causal interregional influences with concurrent TMS-fMRI. Exp Brain Res 191(4):383–402

    Article  PubMed  Google Scholar 

  60. Blankenburg F, Ruff CC, Bestmann S, Bjoertomt O, Josephs O, Deichmann R et al (2010) Studying the role of human parietal cortex in visuospatial attention with concurrent TMS-fMRI. Cereb Cortex 20(11):2702–2711

    Article  PubMed Central  PubMed  Google Scholar 

  61. Bestmann S, Swayne O, Blankenburg F, Ruff CC, Teo J, Weiskopf N et al (2010) The role of contralesional dorsal premotor cortex after stroke as studied with concurrent TMS-fMRI. J Neurosci 30(36):11926–11937

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103(37):13848–13853

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 102(27):9673–9678

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci U S A 100(1):253–258

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  65. Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120(12):2008–2039

    Article  PubMed Central  PubMed  Google Scholar 

  66. Halko MA, Eldaief MC, Horvath JC, Pascual-Leone A (2010) Combining transcranial magnetic stimulation and FMRI to examine the default mode network. J Vis Exp 46:2271

    PubMed  Google Scholar 

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Author information

Authors and Affiliations

  1. Massachusetts General Hospital, 6th Floor, 1 Bowdoin Square, Boston, MA, 02214, USA

    Joan A. Camprodon

  2. Berenson-Allen Center for Noninvasive Brain Stimulation, Beth Israel Deaconess Medical Center, Boston, MA, USA

    Mark A. Halko

Authors
  1. Joan A. Camprodon
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  2. Mark A. Halko
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Corresponding author

Correspondence to Joan A. Camprodon .

Editor information

Editors and Affiliations

  1. Neuromodulation Program, Department of Neurology, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts, USA

    Alexander Rotenberg

  2. Psychological Sciences, University of Melbourne, Melbourne, Victoria, Australia

    Jared Cooney Horvath

  3. Berenson Allen Center for Noninvasive, Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, USA

    Alvaro Pascual-Leone

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Camprodon, J.A., Halko, M.A. (2014). Combination of Transcranial Magnetic Stimulation (TMS) with Functional Magnetic Resonance Imaging. In: Rotenberg, A., Horvath, J., Pascual-Leone, A. (eds) Transcranial Magnetic Stimulation. Neuromethods, vol 89. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-0879-0_10

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  • DOI: https://doi.org/10.1007/978-1-4939-0879-0_10

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  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-0878-3

  • Online ISBN: 978-1-4939-0879-0

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