Skip to main content

Non-invasive Brain Stimulation with Multimodal Acquisitions

  • Chapter
  • First Online:
EEG - fMRI

Abstract

Non-invasive brain stimulation (NIBS) techniques, including transcranial magnetic stimulation (TMS) and low-intensity transcranial electric current stimulation (tES), offer the unique possibility of directly interfering with local and remote neural network activity in conscious human participants, with a quantifiable impact on behaviour or cognition. This makes brain stimulation in many ways complementary to brain imaging and a combination of both techniques particularly desirable. Brain stimulation can be combined with brain imaging either in two separate experimental sessions or simultaneously by using TMS or tES inside the MR scanner. The simultaneous combination of NIBS with fMRI enables the modulation of brain circuits, while concurrently assessing direct and remote neural network effects across the entire brain and linking these (network) activity changes to the induced behavioural manipulation. This chapter introduces the fundamental workings of NIBS and its application in fundamental brain research, rehabilitation and psychiatry and describes the different possibilities of combining brain stimulation and brain imaging with a focus on the methodological and technical challenges. Concrete research studies are used to exemplify how valuable such combined brain stimulation and brain imaging studies can be for fundamental and clinical brain research.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.00
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Ahdab R, Ayache SS, Brugieres P et al (2010) Comparison of “standard” and “navigated” procedures of TMS coil positioning over motor, premotor and prefrontal targets in patients with chronic pain and depression. Neurophysiol Clin 40:27–36

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Andoh J, Artiges E, Pallier C et al (2006) Modulation of language areas with functional mr image-guided magnetic stimulation. NeuroImage 29:619–627

    Article  CAS  Google Scholar 

  • Aydin-Abidin S, Moliadze V, Eysel UT et al (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  CAS  Google Scholar 

  • Aydin-Abidin S, Trippe J, Funke K et al (2008) High- and low-frequency repetitive transcranial magnetic stimulation differentially activates c-fos and zif268 protein expression in the rat brain. Exp Brain Res 188:249–261

    Article  CAS  Google Scholar 

  • Baudewig J, Paulus W, Frahm J (2000) Artifacts caused by transcranial magnetic stimulation coils and eeg electrodes in t(2)*-weighted echo-planar imaging. Magn Reson Imaging 18:479–484

    Article  CAS  Google Scholar 

  • Baudewig J, Siebner HR, Bestmann S et al (2001) Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS). Neuroreport 12:3543–3548

    Article  CAS  Google Scholar 

  • Beckers G, Homberg V (1992) Cerebral visual motion blindness: Transitory akinetopsia induced by transcranial magnetic stimulation of human area v5. Proc Biol Sci 249:173–178

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Bestmann S, Baudewig J, Siebner HR et al (2003b) 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  Google Scholar 

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

    Article  Google Scholar 

  • Bestmann S, Baudewig J, Siebner HR et al (2005) Bold MRI responses to repetitive TMS over human dorsal premotor cortex. NeuroImage 28:22–29

    Article  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(2):134–139. https://doi.org/10.1016/j.cub.2006.11.063

    Article  CAS  Google Scholar 

  • Bestmann S, Swayne O, Blankenburg F et al (2008) Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. Cereb Cortex 18:1281–1291

    Article  Google Scholar 

  • Blankenburg F, Ruff CC, Bestmann S et al (2008) Interhemispheric effect of parietal TMS on somatosensory response confirmed directly with concurrent tms-fmri. J Neurosci 28:13202–13208

    Article  CAS  Google Scholar 

  • Bohning DE, Shastri A, McConnell KA et al (1999) A combined tms/fmri study of intensity-dependent TMS over motor cortex. Biol Psychiatry 45:385–394

    Article  CAS  Google Scholar 

  • Bohning DE, Shastri A, McGavin L et al (2000a) Motor cortex brain activity induced by 1-hz transcranial magnetic stimulation is similar in location and level to that for volitional movement. Investig Radiol 35:676–683

    Article  CAS  Google Scholar 

  • Bohning DE, Shastri A, Wassermann EM et al (2000b) Bold-f MRI response to single-pulse transcranial magnetic stimulation (TMS). J Magn Reson Imaging 11:569–574

    Article  CAS  Google Scholar 

  • Boorman ED, O'Shea J, Sebastian C et al (2007) Individual differences in white-matter microstructure reflect variation in functional connectivity during choice. Curr Biol 17:1426–1431

    Article  CAS  Google Scholar 

  • Brighina F, Bisiach E, Oliveri M et al (2003) 1 hz repetitive transcranial magnetic stimulation of the unaffected hemisphere ameliorates contralesional visuospatial neglect in humans. Neurosci Lett 336:131–133

    Article  CAS  Google Scholar 

  • Bungert A, Chambers CD, Long E, Evans CJ (2012a) On the importance of specialized radiofrequency filtering for concurrent TMS/MRI. J Neurosci Methods 210(2):202–205. https://doi.org/10.1016/j.jneumeth.2012.07.023

    Article  Google Scholar 

  • Bungert A, Chambers CD, Phillips M, Evans CJ (2012b) Reducing image artefacts in concurrent TMS/fMRI by passive shimming. NeuroImage 59(3):2167–2174. https://doi.org/10.1016/j.neuroimage.2011.10.013

    Article  Google Scholar 

  • Burt T, Lisanby SH, Sackeim HA (2002) Neuropsychiatric applications of transcranial magnetic stimulation: a meta analysis. Int J Neuropsychopharmacol 5:73–103

    Article  Google Scholar 

  • Camprodon JA, Martinez-Raga J, Alonso-Alonso M et al (2007) One session of high frequency repetitive transcranial magnetic stimulation (rTMS) to the right prefrontal cortex transiently reduces cocaine craving. Drug Alcohol Depend 86:91–94

    Article  Google Scholar 

  • Caparelli EC, Backus W, Telang F, Wang G-J, Maloney T, Goldstein RZ et al (2010) Simultaneous TMS-fMRI of the visual cortex reveals functional network, even in absence of phosphene sensation. Open Neuroimaging J 4(1):100–110. https://doi.org/10.2174/1874440001004010100

    Article  CAS  Google Scholar 

  • Cardenas-Morales L, Gron G, Kammer T (2011) Exploring the after-effects of theta burst magnetic stimulation on the human motor cortex: a functional imaging study. Hum Brain Mapp 32:1948–1960

    Article  Google Scholar 

  • Cazzoli D, Muri RM, Hess CW et al (2010) Treatment of hemispatial neglect by means of rTMS–a review. Restor Neurol Neurosci 28:499–510

    Google Scholar 

  • Chechlacz M, Humphreys GW, Sotiropoulos SN, Kennard C, Cazzoli D (2015) Structural organization of the corpus callosum predicts attentional shifts after continuous theta burst stimulation. J Neurosci 35(46):15353–15368

    Article  CAS  Google Scholar 

  • Chibbaro G, Daniele M, Alagona G et al (2005) Repetitive transcranial magnetic stimulation in schizophrenic patients reporting auditory hallucinations. Neurosci Lett 383:54–57

    Article  CAS  Google Scholar 

  • d'Alfonso AA, van Honk J, Schutter DJ et al (2002) Spatial and temporal characteristics of visual motion perception involving v5 visual cortex. Neurol Res 24:266–270

    Article  CAS  Google Scholar 

  • Dambeck N, Sparing R, Meister IG, Wienemann M (2006) Interhemispheric imbalance during visuospatial attention investigated by unilateral and bilateral TMS over human parietal cortices. Brain Res 1072(1):194–199

    Article  CAS  Google Scholar 

  • de Graaf TA, Jacobs C, Roebroeck A et al (2009) Fmri effective connectivity and TMS chronometry: complementary accounts of causality in the visuospatial judgment network. PLoS One 4:e8307

    Article  Google Scholar 

  • de Graaf TA, Koivisto M, Jacobs C, Sack AT (2014) The chronometry of visual perception: review of occipital TMS masking studies. Neurosci Biobehav Rev 45:295–304

    Article  Google Scholar 

  • de Labra C, Rivadulla C, Grieve K et al (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  Google Scholar 

  • De Ridder D, Vanneste S, Kovacs S et al (2011) Transcranial magnetic stimulation and extradural electrodes implanted on secondary auditory cortex for tinnitus suppression. J Neurosurg 114:903–911

    Article  Google Scholar 

  • Denslow S, Lomarev M, George MS et al (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  Google Scholar 

  • Di Lazzaro V (2008) The physiological basis of the effects of intermittent theta burst stimulation of the human motor cortex. J Physiol 586:3871–3871

    Article  Google Scholar 

  • Duecker F, Formisano E, Sack AT (2013) Hemispheric differences in the voluntary control of spatial attention: direct evidence for a right-hemispheric dominance within frontal cortex. J Cogn Neurosci 25(8):1332–1342. https://doi.org/10.1162/jocn_a_00402

    Article  Google Scholar 

  • Duecker F, Frost MA, Graaf TA, Graewe B, Jacobs C, Goebel R, Sack AT (2014) The cortex-based alignment approach to TMS coil positioning. J Cogn Neurosci 26(10):2321–2329. https://doi.org/10.1162/jocn_a_00635

    Article  Google Scholar 

  • Dugué L, Marque P, VanRullen R (2011) The phase of ongoing oscillations mediates the causal relation between brain excitation and visual perception. J Neurosci 31(33):11889–11893

    Article  Google Scholar 

  • Eichhammer P, Johann M, Kharraz A et al (2003) High-frequency repetitive transcranial magnetic stimulation decreases cigarette smoking. J Clin Psychiatry 64:951–953

    Article  Google Scholar 

  • Engelen T, Zhan M, Sack AT, de Gelder B (2018) Dynamic interactions between emotion perception and action preparation for reacting to social threat: a combined cTBS-fMRI study. eNeuro 5(3):17. https://doi.org/10.1523/ENEURO.0408-17.2018

    Article  Google Scholar 

  • Esser SK, Hill SL, Tononi G (2005) Modeling the effects of transcranial magnetic stimulation on cortical circuits. J Neurophysiol 94:622–639

    Article  CAS  Google Scholar 

  • Feredoes E, Tononi G, Postle BR (2007) The neural bases of the short-term storage of verbal information are anatomically variable across individuals. J Neurosci 27:11003–11008

    Article  CAS  Google Scholar 

  • Fitzgerald PB, Sritharan A, Daskalakis ZJ et al (2007) A functional magnetic resonance imaging study of the effects of low frequency right prefrontal transcranial magnetic stimulation in depression. J Clin Psychopharmacol 27:488–492

    Article  Google Scholar 

  • Funke K, Benali A (2010) Cortical cellular actions of transcranial magnetic stimulation. Restor Neurol Neurosci 28:399–417

    Google Scholar 

  • George MS, Wassermann EM, Williams WA et al (1995) Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression. Neuroreport 6:1853–1856

    Article  CAS  Google Scholar 

  • Goldsworthy M, Vallence A, Yang R, Pitcher J, Ridding M (2016) Combined transcranial alternating current stimulation and continuous theta burst stimulation: a novel approach for neuroplasticity induction. Eur J Neurosci 43(4):572 579

    Article  Google Scholar 

  • Graaf TA, Thomson A, Janssens S, Bree S, Oever S, Sack AT (2020) Does alpha phase modulate visual target detection? Three experiments with tACS phase-based stimulus presentation. Eur J Neurosci 2020:1–15

    Google Scholar 

  • Gross M, Nakamura L, Pascual-Leone A et al (2007) Has repetitive transcranial magnetic stimulation (rTMS) treatment for depression improved? A systematic review and meta-analysis comparing the recent vs. The earlier rTMS studies. Acta Psychiatr Scand 116:165–173

    Article  CAS  Google Scholar 

  • Hada Y, Abo M, Kaminaga T et al (2006) Detection of cerebral blood flow changes during repetitive transcranial magnetic stimulation by recording hemoglobin in the brain cortex, just beneath the stimulation coil, with near-infrared spectroscopy. NeuroImage 32:1226–1230

    Article  Google Scholar 

  • Hanakawa T, Mima T, Matsumoto R et al (2009) Stimulus-response profile during single-pulse transcranial magnetic stimulation to the primary motor cortex. Cereb Cortex 19:2605–2615

    Article  Google Scholar 

  • Haraldsson HM, Ferrarelli F, Kalin NH et al (2004) Transcranial magnetic stimulation in the investigation and treatment of schizophrenia: a review. Schizophr Res 71:1–16

    Article  Google Scholar 

  • Hawco C, Armony JL, Daskalakis ZJ, Berlim MT, Chakravarty MM, Pike GB, Lepage M (2017) Differing time of onset of concurrent TMS-fMRI during associative memory encoding: a measure of dynamic connectivity. Front Hum Neurosci 11:404. https://doi.org/10.3389/fnhum.2017.00404

    Article  Google Scholar 

  • Hayashi T, Ohnishi T, Okabe S et al (2004) Long-term effect of motor cortical repetitive transcranial magnetic stimulation. Ann Neurol 56:77–85

    Article  Google Scholar 

  • Heinen K, Ruff CC, Bjoertomt O, Schenkluhn B, Bestmann S, Blankenburg F et al (2011) Concurrent TMS-fMRI reveals dynamic interhemispheric influences of the right parietal cortex during exogenously cued visuospatial attention. Eur J Neurosci 33(5):991–1000. https://doi.org/10.1111/j.1460-9568.2010.07580.x

    Article  Google Scholar 

  • Herbsman T, Avery D, Ramsey D et al (2009) More lateral and anterior prefrontal coil location is associated with better repetitive transcranial magnetic stimulation antidepressant response. Biol Psychiatry 66:509–515

    Article  Google Scholar 

  • Herwig U, Fallgatter AJ, Hoppner J et al (2007) Antidepressant effects of augmentative transcranial magnetic stimulation: Randomised multicentre trial. Br J Psychiatry 191:441–448

    Article  CAS  Google Scholar 

  • Hilgetag CC, Théoret H, Pascual-Leone A (2001) Enhanced visual spatial attention ipsilateral to rTMS-induced “virtual lesions” of human parietal cortex. Nat Neurosci. https://doi.org/10.1038/nn0901-953

  • Hoffman RE (2003) Variations on the chemical shift of TMS. J Magn Reson 163:325–331

    Article  CAS  Google Scholar 

  • Hoffman RE, Becker ED (2005) Temperature dependence of the 1h chemical shift of tetramethylsilane in chloroform, methanol, and dimethylsulfoxide. J Magn Reson 176:87–98

    Article  CAS  Google Scholar 

  • Holtzheimer PE, Russo J, Avery DH (2001) A meta-analysis of repetitive transcranial magnetic stimulation in the treatment of depression. Psychopharmacol Bull 35:149–169

    Google Scholar 

  • Huang Y-Z, Edwards MJ, Rounis E et al (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201–206

    Article  CAS  Google Scholar 

  • Hubl D, Nyffeler T, Wurtz P et al (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  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  CAS  Google Scholar 

  • Khedr EM, Kotb H, Kamel NF et al (2005) Longlasting antalgic effects of daily sessions of repetitive transcranial magnetic stimulation in central and peripheral neuropathic pain. J Neurol Neurosurg Psychiatry 76:833–838

    Article  CAS  Google Scholar 

  • Kimbrell TA, Little JT, Dunn RT et al (1999) Frequency dependence of antidepressant response to left prefrontal repetitive transcranial magnetic stimulation (rTMS) as a function of baseline cerebral glucose metabolism. Biol Psychiatry 46:1603–1613

    Article  CAS  Google Scholar 

  • Kimbrell TA, Ketter TA, George MS et al (2002) Regional cerebral glucose utilization in patients with a range of severities of unipolar depression. Biol Psychiatry 51:237–252

    Article  CAS  Google Scholar 

  • Kloppel S, Baumer T, Kroeger J et al (2008) The cortical motor threshold reflects microstructural properties of cerebral white matter. NeuroImage 40:1782–1791

    Article  Google Scholar 

  • Koch G, Oliveri M, Cheeran B et al (2008) Hyperexcitability of parietal-motor functional connections in the intact left-hemisphere of patients with neglect. Brain 131:3147–3155

    Article  Google Scholar 

  • Kozel FA, George MS (2002) Meta-analysis of left prefrontal repetitive transcranial magnetic stimulation (rTMS) to treat depression. J Psychiatr Pract 8:270–275

    Article  Google Scholar 

  • Kozel FA, Tian F, Dhamne S et al (2009) Using simultaneous repetitive transcranial magnetic stimulation/functional near infrared spectroscopy (rTMS/fNIRS) to measure brain activation and connectivity. NeuroImage 47:1177–1184

    Article  Google Scholar 

  • Lee SH, Kim W, Chung YC et al (2005) A double blind study showing that two weeks of daily repetitive TMS over the left or right temporoparietal cortex reduces symptoms in patients with schizophrenia who are having treatment-refractory auditory hallucinations. Neurosci Lett 376:177–181

    Article  CAS  Google Scholar 

  • Lefaucheur JP, Drouot X, Nguyen JP (2001) Interventional neurophysiology for pain control: Duration of pain relief following repetitive transcranial magnetic stimulation of the motor cortex. Neurophysiol Clin 31:247–252

    Article  CAS  Google Scholar 

  • Lefaucheur J-P, André-Obadia N, Antal A, Ayache SS, Baeken C, Benninger DH et al (2014) Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol 125(11):2150–2206. https://doi.org/10.1016/j.clinph.2014.05.021

    Article  Google Scholar 

  • Leitão J, Thielscher A, Tünnerhoff J, Noppeney U (2015) Concurrent TMS-fMRI reveals interactions between dorsal and ventral attentional systems. J Neurosci 35(32):11445–11457. https://doi.org/10.1523/JNEUROSCI.0939-15.2015

    Article  CAS  Google Scholar 

  • Leitão J, Thielscher A, Lee H, Tuennerhoff J, Noppeney U (2017) Transcranial magnetic stimulation of right inferior parietal cortex causally influences prefrontal activation for visual detection. Eur J Neurosci 17:309. https://doi.org/10.1111/ejn.13743

    Article  Google Scholar 

  • Logothetis NK (2008) What we can do and what we cannot do with fMRI. Nature 453:869–878

    Article  CAS  Google Scholar 

  • Logothetis NK, Augath M, Murayama Y et al (2010) The effects of electrical microstimulation on cortical signal propagation. Nat Neurosci 13:1283–1291

    Article  CAS  Google Scholar 

  • Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 133(4):425–430

    Article  CAS  Google Scholar 

  • Martin JL, Barbanoj MJ, Perez V et al (2003) Transcranial magnetic stimulation for the treatment of obsessive-compulsive disorder. Cochrane Database Syst Rev 3:CD003387

    Google Scholar 

  • McNamara B, Ray JL, Arthurs OJ et al (2001) Transcranial magnetic stimulation for depression and other psychiatric disorders. Psychol Med 31:1141–1146

    Article  CAS  Google Scholar 

  • Mochizuki H, Ugawa Y, Terao Y et al (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  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Moliadze V, Giannikopoulos D, Eysel UT et al (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  CAS  Google Scholar 

  • Navarro de Lara LI, Tik M, Woletz M, Frass-Kriegl R, Moser E, Laistler E, Windischberger C (2017) High-sensitivity TMS/fMRI of the human motor cortex using a dedicated multichannel MR coil. NeuroImage 150:262–269. https://doi.org/10.1016/j.neuroimage.2017.02.062

    Article  Google Scholar 

  • Nyffeler T, Cazzoli D, Hess CW et al (2009) One session of repeated parietal theta burst stimulation trains induces long-lasting improvement of visual neglect. Stroke 40:2791–2796

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ohnishi T, Hayashi T, Okabe S et al (2004) 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 55:484–489

    Article  CAS  Google Scholar 

  • Oliveri M, Rossini PM, Traversa R et al (1999) Left frontal transcranial magnetic stimulation reduces contralesional extinction in patients with unilateral right brain damage. Brain 122(Pt 9):1731–1739

    Article  Google Scholar 

  • Oliveri M, Caltagirone C, Filippi MM et al (2000a) Paired transcranial magnetic stimulation protocols reveal a pattern of inhibition and facilitation in the human parietal cortex. J Physiol 529(Pt 2):461–468

    Article  CAS  Google Scholar 

  • Oliveri M, Rossini PM, Filippi MM et al (2000b) Time-dependent activation of parieto-frontal networks for directing attention to tactile space. A study with paired transcranial magnetic stimulation pulses in right-brain-damaged patients with extinction. Brain 123(Pt 9):1939–1947

    Article  Google Scholar 

  • Oliveri M, Bisiach E, Brighina F et al (2001) rTMS of the unaffected hemisphere transiently reduces contralesional visuospatial hemineglect. Neurology 57:1338–1340

    Article  CAS  Google Scholar 

  • Pascual-Leone A, Rubio B, Pallardo F et al (1996) Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. Lancet 348:233–237

    Article  CAS  Google Scholar 

  • Pasley BN, Allen EA, Freeman RD (2009) State-dependent variability of neuronal responses to transcranial magnetic stimulation of the visual cortex. Neuron 62:291–303

    Article  CAS  Google Scholar 

  • Paus T, Barrett J (2004) Transcranial magnetic stimulation (TMS) of the human frontal cortex: implications for repetitive TMS treatment of depression. J Psychiatry Neurosci 29:268–279

    Google Scholar 

  • Peters JC, Reithler J, Schuhmann T, de Graaf TA, Uludag K, Goebel R, Sack AT (2013) On the feasibility of concurrent human TMS-EEG-fMRI measurements. J Neurophysiol 109(4):1214–1227

    Article  Google Scholar 

  • Peters JC, Reithler J, de Graaf TA, Schuhmann T, Goebel R, Sack AT (2020) Concurrent human TMS-EEG-fMRI enables monitoring of oscillatory brain state-dependent gating of cortico-subcortical network activity. Nat Commun Biol 3(1):40

    Article  Google Scholar 

  • Pogarell O, Koch W, Popperl G et al (2006) Striatal dopamine release after prefrontal repetitive transcranial magnetic stimulation in major depression: preliminary results of a dynamic [123i] ibzm spect study. J Psychiatr Res 40:307–314

    Article  Google Scholar 

  • Pogarell O, Koch W, Popperl G et al (2007) Acute prefrontal rTMS increases striatal dopamine to a similar degree as d-amphetamine. Psychiatry Res 156:251–255

    Article  CAS  Google Scholar 

  • Reithler J, Peters JC, Sack AT (2011) Multimodal transcranial magnetic stimulation: using concurrent neuroimaging to reveal the neural network dynamics of noninvasive brain stimulation. Prog Neurobiol 94:149–165

    Article  CAS  Google Scholar 

  • Ricci R, Salatino A, Li X, Funk AP, Logan SL, Mu Q et al (2012) Imaging the neural mechanisms of TMS neglect-like bias in healthy volunteers with the interleaved TMS/fMRI technique: preliminary evidence. Front Hum Neurosci 6:326. https://doi.org/10.3389/fnhum.2012.00326

    Article  Google Scholar 

  • Ridding MC, Rothwell JC (2007) Is there a future for therapeutic use of transcranial magnetic stimulation? Nat Rev Neurosci 8:559–567

    Article  CAS  Google Scholar 

  • Romei V, Brodbeck V, Michel C, Amedi A, Pascual-Leone A, Thut G (2008a) Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas. Cereb Cortex 18(9):2010–2018

    Article  Google Scholar 

  • Romei V, Rihs T, Brodbeck V, Thut G (2008b) Resting electroencephalogram alpha-power over posterior sites indexes baseline visual cortex excitability. Neuroreport 19(2):203–208

    Article  Google Scholar 

  • Rossi S, Hallett M, Rossini PM et al (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039

    Article  Google Scholar 

  • Ruff CC, Blankenburg F, Bjoertomt O et al (2006) Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Curr Biol 16:1479–1488

    Article  CAS  Google Scholar 

  • Ruff CC, Bestmann S, Blankenburg F et al (2008) Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent tms-fmri. Cereb Cortex 18:817–827

    Article  Google Scholar 

  • Ruff CC, Driver J, Bestmann S (2009) Combining TMS and fMRI: from ‘virtual lesions’ to functional-network accounts of cognition. Cortex 45:1043–1049

    Article  Google Scholar 

  • Rushworth MF, Hadland KA, Paus T et al (2002) Role of the human medial frontal cortex in task switching: a combined FMRI and TMS study. J Neurophysiol 87:2577–2592

    Article  CAS  Google Scholar 

  • Sachdev PS, McBride R, Loo CK et al (2001) Right versus left prefrontal transcranial magnetic stimulation for obsessive-compulsive disorder: a preliminary investigation. J Clin Psychiatry 62:981–984

    Article  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  CAS  Google Scholar 

  • Sack AT (2010) Does TMS need functional imaging? Cortex 46:131–133

    Article  Google Scholar 

  • Sack AT, Kohler A, Linden DE et al (2006) The temporal characteristics of motion processing in hmt/v5+: combining FMRI and neuronavigated TMS. NeuroImage 29:1326–1335

    Article  Google Scholar 

  • Sack AT, Kohler A, Bestmann S et al (2007) Imaging the brain activity changes underlying impaired visuospatial judgments: Simultaneous FMRI, TMS, and behavioral studies. Cereb Cortex 17:2841–2852

    Article  Google Scholar 

  • Sack AT, Cohen Kadosh R, Schuhmann T et al (2009) Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. J Cogn Neurosci 21:207–221

    Article  Google Scholar 

  • Schilberg L, Engelen T, Oever S, Schuhmann T, de Gelder B, de Graaf TA, Sack AT (2018) Phase of beta-frequency tACS over primary motor cortex modulates corticospinal excitability. Cortex 103:142–152

    Article  Google Scholar 

  • Schonfeldt-Lecuona C, Cardenas-Morales L, Freudenmann RW et al (2010) Transcranial magnetic stimulation in depression–lessons from the multicentre trials. Restor Neurol Neurosci 28:569–576

    CAS  Google Scholar 

  • Schuhmann T, Schiller NO, Goebel R, Sack AT (2009) The temporal characteristics of functional activation in Broca’s area during overt picture naming. Cortex 45(9):1111–1116

    Article  Google Scholar 

  • Schuhmann T, Schiller NO, Goebel R, Sack AT (2012) Speaking of which: dissecting the neurocognitive network of language production in picture naming. Cereb Cortex 22(3):701–709

    Article  Google Scholar 

  • Shastri A, George MS, Bohning DE (1999) Performance of a system for interleaving transcranial magnetic stimulation with steady-state magnetic resonance imaging. Electroencephalogr Clin Neurophysiol Suppl 51:55–64

    CAS  Google Scholar 

  • Shindo K, Sugiyama K, Huabao L et al (2006) Long-term effect of low-frequency repetitive transcranial magnetic stimulation over the unaffected posterior parietal cortex in patients with unilateral spatial neglect. J Rehabil Med 38:65–67

    Article  Google Scholar 

  • Song W, Du B, Xu Q et al (2009) Low-frequency transcranial magnetic stimulation for visual spatial neglect: a pilot study. J Rehabil Med 41:162–165

    Article  Google Scholar 

  • Sparing R, Buelte D, Meister IG et al (2008) Transcranial magnetic stimulation and the challenge of coil placement: a comparison of conventional and stereotaxic neuronavigational strategies. Hum Brain Mapp 29:82–96

    Article  Google Scholar 

  • Speer AM, Kimbrell TA, Wassermann EM et al (2000) Opposite effects of high and low frequency rTMS on regional brain activity in depressed patients. Biol Psychiatry 48:1133–1141

    Article  CAS  Google Scholar 

  • Speer AM, Benson BE, Kimbrell TK et al (2009) Opposite effects of high and low frequency RTMS on mood in depressed patients: relationship to baseline cerebral activity on pet. J Affect Disord 115:386–394

    Article  CAS  Google Scholar 

  • Stagg CJ, Wylezinska M, Matthews PM et al (2009) Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. J Neurophysiol 101:2872–2877

    Article  CAS  Google Scholar 

  • Teneback CC, Nahas Z, Speer AM et al (1999) Changes in prefrontal cortex and paralimbic activity in depression following two weeks of daily left prefrontal TMS. J Neuropsychiatry Clin Neurosci 11:426–435

    CAS  Google Scholar 

  • Thiel A, Haupt WF, Habedank B et al (2005) Neuroimaging-guided rTMS of the left inferior frontal gyrus interferes with repetition priming. NeuroImage 25:815–823

    Article  Google Scholar 

  • Trippe J, Mix A, Aydin-Abidin S et al (2009) Theta burst and conventional low-frequency RTMS differentially affect GABAergic neurotransmission in the rat cortex. Exp Brain Res 199:411–421

    Article  CAS  Google Scholar 

  • Valero-Cabre A, Payne BR, Rushmore J et al (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  Google Scholar 

  • Valero-Cabre A, Payne BR, Pascual-Leone A (2007) Opposite impact on 14c-2-deoxyglucose brain metabolism following patterns of high and low frequency repetitive transcranial magnetic stimulation in the posterior parietal cortex. Exp Brain Res 176:603–615

    Article  CAS  Google Scholar 

  • Walsh V, Pascual-Leone A (2003) Transcranial magnetic stimulation: a neurochronometrics of mind. MIT Press, Cambridge

    Google Scholar 

  • Weiskopf N, Josephs O, Ruff CC et al (2009) Image artifacts in concurrent transcranial magnetic stimulation (TMS) and fmri caused by leakage currents: modeling and compensation. J Magn Reson Imaging 29:1211–1217

    Article  Google Scholar 

  • Zrenner C, Belardinelli P, Müller-Dahlhaus F, Ziemann U (2016) Closed-Loop Neuroscience and Non-Invasive Brain Stimulation: A Tale of Two Loops. Front Cell Neurosci 7;10:92. https://doi.org/10.3389/fncel.2016.00092. PMID: 27092055; PMCID: PMC4823269

  • Zrenner C, Desideri D, Belardinelli P, Ziemann U (2018) Real-time EEG-defined excitability states determine efficacy of TMS-induced plasticity in human motor cortex. Brain Stimul 11(2):374–389. https://doi.org/10.1016/j.brs.2017.11.016. Epub 2017 Nov 24. PMID: 29191438.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexander T. Sack .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2022 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sack, A.T., Schuhmann, T., de Graaf, T.A. (2022). Non-invasive Brain Stimulation with Multimodal Acquisitions. In: Mulert, C., Lemieux, L. (eds) EEG - fMRI. Springer, Cham. https://doi.org/10.1007/978-3-031-07121-8_14

Download citation

  • DOI: https://doi.org/10.1007/978-3-031-07121-8_14

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-031-07120-1

  • Online ISBN: 978-3-031-07121-8

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics