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Simultaneous EEG-fMRI

Chapter

Abstract

Simultaneous EEG-fMRI combines the advantages of high temporal resolution of EEG with high spatial resolution of fMRI. In addition, it is a noninvasive technique for the study of human brain function. However, it remains many challenges such as the low signal-to-noise ratio, poor individual comfort, and difficulty in data analysis. In this chapter, we first introduce the hardware of simultaneous EEG-fMRI system. Then a review about the advance of this technique is given, including the EEG artifacts correction, the EEG-fMRI data fusion method, and the application of EEG-fMRI. Specifically, we provide a systematic classification for the fMRI-constrained EEG and the EEG-informed fMRI from simple to complex level. Then we provide program practice for the EEG artifacts correction, which may contribute to the widespread application of this new technique. Finally, we discuss the prospects of simultaneous EEG-fMRI for future research.

Keywords

EEG-fMRI Fusion EEG artifacts correction fMRI-constrained EEG EEG-informed fMRI 

References

  1. Abreu R, Leal A, Figueiredo P. EEG-informed fMRI: a review of data analysis methods. Front Hum Neurosci. 2018;12:29.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Acharjee PP, Phlypo R, Wu L, Calhoun VD, Adali T. Independent vector analysis for gradient artifact removal in concurrent EEG-fMRI data. IEEE Trans Biomed Eng. 2015;62:1750–8.PubMedCrossRefPubMedCentralGoogle Scholar
  3. Allen PJ, Polizzi G, Krakow K, Fish DR, Lemieux L. Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage. 1998;8:229–39.PubMedCrossRefPubMedCentralGoogle Scholar
  4. Allen PJ, Josephs O, Turner R. A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage. 2000;12:230–9.PubMedCrossRefPubMedCentralGoogle Scholar
  5. Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD. Tracking whole-brain connectivity dynamics in the resting state. Cerebral Cortex. 2014;24:663–76.PubMedCrossRefGoogle Scholar
  6. Auranen T, Nummenmaa A, Vanni S, Vehtari A, Hamalainen MS, Lampinen J, Jaaskelainen IP. Automatic fMRI-guided MEG multidipole localization for visual responses. Hum Brain Mapp. 2009;30:1087–99.PubMedCrossRefPubMedCentralGoogle Scholar
  7. Becker R, Ritter P, Moosmann M, Villringer A. Visual evoked potentials recovered from fMRI scan periods. Hum Brain Mapp. 2005;26:221–30.PubMedCrossRefGoogle Scholar
  8. Bénar C, Aghakhani Y, Wang Y, Izenberg A, Al-Asmi A, Dubeau F, Gotman J. Quality of EEG in simultaneous EEG-fMRI for epilepsy. Clin Neurophysiol. 2003;114:569–80.PubMedCrossRefGoogle Scholar
  9. Bénar CG, Schon D, Grimault S, Nazarian B, Burle B, Roth M, Badier JM, Marquis P, Liegeois-Chauvel C, Anton JL. Single-trial analysis of oddball event-related potentials in simultaneous EEG-fMRI. Hum Brain Mapp. 2007;28:602–13.PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bharath RD, Panda R, Reddam VR, Bhaskar MV, Gohel S, Bhardwaj S, Prajapati A, Pal PK. A single session of rTMS enhances small-worldness in writer’s cramp: evidence from simultaneous EEG-fMRI multi-modal brain graph. Front Hum Neurosci. 2017;11:443.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bonmassar G, Purdon PL, Jaaskelainen IP, Chiappa K, Solo V, Brown EN, Belliveau JW. Motion and ballistocardiogram artifact removal for interleaved recording of EEG and EPs during MRI. Neuroimage. 2002;16:1127–41.PubMedCrossRefGoogle Scholar
  12. Calhoun VD, Adali T, Pearlson GD, Pekar JJ. A method for making group inferences from functional MRI data using independent component analysis. Hum Brain Mapp. 2001;14:140–51.PubMedCrossRefGoogle Scholar
  13. Chen AC, Feng W, Zhao H, Yin Y, Wang P. EEG default mode network in the human brain: spectral regional field powers. Neuroimage. 2008;41:561–74.PubMedCrossRefGoogle Scholar
  14. Chowdhury ME, Mullinger KJ, Glover P, Bowtell R. Reference layer artefact subtraction (RLAS): a novel method of minimizing EEG artefacts during simultaneous fMRI. Neuroimage. 2014;84:307–19.PubMedCrossRefGoogle Scholar
  15. de Munck JC, Goncalves SI, Mammoliti R, Heethaar RM, Lopes da Silva FH. Interactions between different EEG frequency bands and their effect on alpha-fMRI correlations. Neuroimage. 2009;47:69–76.PubMedCrossRefGoogle Scholar
  16. Debener S, Ullsperger M, Siegel M, Fiehler K, von Cramon DY, Engel AK. Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J Neurosci. 2005;25:11730–7.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Debener S, Ullsperger M, Siegel M, Engel AK. Single-trial EEG-fMRI reveals the dynamics of cognitive function. Trends Cognit Sci. 2006;10:558–63.CrossRefGoogle Scholar
  18. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 2004;134:9–21.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dong L, Luo C, Xiaobo L, Sisi J, Fali L, Hongshuo F, Jianfu L, Diankun G, Dezhong Y. Neuroscience information toolbox: an open source toolbox for EEG–fMRI multimodal fusion analysis. Front Neuroinf. 2018;12:56.CrossRefGoogle Scholar
  20. Eichele T, Specht K, Moosmann M, Jongsma ML, Quiroga RQ, Nordby H, Hugdahl K. Assessing the spatiotemporal evolution of neuronal activation with single-trial event-related potentials and functional MRI. Proc Natl Acad Sci U S A. 2005;102:17798–803.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Freyer F, Becker R, Anami K, Curio G, Villringer A, Ritter P. Ultrahigh-frequency EEG during fMRI: pushing the limits of imaging-artifact correction. Neuroimage. 2009;48:94–108.PubMedCrossRefGoogle Scholar
  22. Friston KJ, Price CJ. Dynamic representations and generative models of brain function. Brain Res Bull. 2001;54:275–285.PubMedCrossRefGoogle Scholar
  23. Friston KJ. Modalities, modes, and models in functional neuroimaging. Science. 2009;326:399–403.PubMedCrossRefGoogle Scholar
  24. Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp. 1994;2:189–210.CrossRefGoogle Scholar
  25. Goense JB, Logothetis NK. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr Biol. 2008;18:631–40.PubMedCrossRefGoogle Scholar
  26. Goldman RI, Stern JM, Engel J Jr, Cohen MS. Simultaneous EEG and fMRI of the alpha rhythm. Neuroreport. 2002;13:2487–92.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Goldman RI, Wei CY, Philiastides MG, Gerson AD, Friedman D, Brown TR, Sajda P. Single-trial discrimination for integrating simultaneous EEG and fMRI: identifying cortical areas contributing to trial-to-trial variability in the auditory oddball task. Neuroimage. 2009;47:136–47.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Gotman J, Bénar CG, Dubeau F. Combining EEG and FMRI in epilepsy: methodological challenges and clinical results. J Clin Neurophysiol. 2004;21:229–40.PubMedCrossRefPubMedCentralGoogle Scholar
  29. Green JJ, Boehler CN, Roberts KC, Chen L-C, Krebs RM, Song AW, Woldorff MG. Cortical and subcortical coordination of visual spatial attention revealed by simultaneous EEG-fMRI recording. J Neurosci Off J Soc Neurosci. 2017;37:7803–10.CrossRefGoogle Scholar
  30. Grouiller F, Vercueil L, Krainik A, Segebarth C, Kahane P, David O. A comparative study of different artefact removal algorithms for EEG signals acquired during functional MRI. Neuroimage. 2007;38:124–37.PubMedCrossRefPubMedCentralGoogle Scholar
  31. Hamandi K, Laufs H, Noth U, Carmichael DW, Duncan JS, Lemieux L. BOLD and perfusion changes during epileptic generalised spike wave activity. Neuroimage. 2008;39:608–18.PubMedCrossRefPubMedCentralGoogle Scholar
  32. He BJ. Spontaneous and task-evoked brain activity negatively interact. J Neurosci. 2013;33:4672–82.PubMedPubMedCentralCrossRefGoogle Scholar
  33. Horovitz SG, Braun AR, Carr WS, Picchioni D, Balkin TJ, Fukunaga M, Duyn JH. Decoupling of the brain’s default mode network during deep sleep. Proc Natl Acad Sci U S A. 2009;106:11376–81.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Ives JR, Warach S, Schmitt F, Edelman RR, Schomer DL. Monitoring the patient’s EEG during echo planar MRI. Electroencephalogr Clin Neurophysiol. 1993;87:417–20.PubMedCrossRefPubMedCentralGoogle Scholar
  35. Jahnke K, von Wegner F, Morzelewski A, Borisov S, Maischein M, Steinmetz H, Laufs H. To wake or not to wake? the two-sided nature of the human K-complex. Neuroimage. 2012;59:1631–8.PubMedCrossRefPubMedCentralGoogle Scholar
  36. Jann K, Dierks T, Boesch C, Kottlow M, Strik W, Koenig T. BOLD correlates of EEG alpha phase-locking and the fMRI default mode network. Neuroimage. 2009;45:903–16.PubMedCrossRefPubMedCentralGoogle Scholar
  37. Jorge J, Bouloc C, Bréchet L, Michel CM, Gruetter R. Investigating the variability of cardiac pulse artifacts across heartbeats in simultaneous EEG-fMRI recordings: a 7T study. Neuroimage. 2019;191:21–35.PubMedCrossRefPubMedCentralGoogle Scholar
  38. Kaufmann C, Wehrle R, Wetter TC, Holsboer F, Auer DP, Pollmächer T, Czisch M. Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: an EEG/fMRI study. Brain. 2006;129:655–67.PubMedCrossRefGoogle Scholar
  39. Krishnaswamy P, Bonmassar G, Poulsen C, Pierce ET, Purdon PL, Brown EN. Reference-free removal of EEG-fMRI ballistocardiogram artifacts with harmonic regression. Neuroimage. 2016;128:398–412.PubMedCrossRefGoogle Scholar
  40. Ladenbauer J, Ladenbauer J, Kulzow N, de Boor R, Avramova E, Grittner U, Floel A. Promoting sleep oscillations and their functional coupling by transcranial stimulation enhances memory consolidation in mild cognitive impairment. J Neurosci. 2017;37:7111–24.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Lange N, Zeger SL. Non-linear Fourier time series analysis for human brain mapping by functional magnetic resonance imaging. J R Stat Soc Ser C (Appl Stat). 1997;46:1–29.CrossRefGoogle Scholar
  42. Laufs H, Krakow K, Sterzer P, Eger E, Beyerle A, Salek-Haddadi A, Kleinschmidt A. Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest. Proc Natl Acad Sci U S A. 2003;100:11053–8.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Laufs H, Daunizeau J, Carmichael DW, Kleinschmidt A. Recent advances in recording electrophysiological data simultaneously with magnetic resonance imaging. Neuroimage. 2008;40:515–28.PubMedCrossRefGoogle Scholar
  44. Lei X, Yang P, Yao D. An empirical Bayesian framework for brain-computer interfaces. IEEE Trans Neural Syst Rehabil Eng. 2009;17:521–9.PubMedCrossRefPubMedCentralGoogle Scholar
  45. Lei X, Qiu C, Xu P, Yao D. A parallel framework for simultaneous EEG/fMRI analysis: methodology and simulation. Neuroimage. 2010;52:1123–34.PubMedCrossRefGoogle Scholar
  46. Lei X, Ostwald D, Hu J, Qiu C, Porcaro C, Bagshaw AP, Yao D. Multimodal functional network connectivity: an EEG-fMRI fusion in network space. Plos One. 2011a;6:e24642.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Lei X, Xu P, Luo C, Zhao J, Zhou D, Yao D. fMRI functional networks for EEG source imaging. Hum Brain Mapp. 2011b;32:1141–60.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Lei X, Hu J, Yao D. Incorporating fMRI functional networks in EEG source imaging: a Bayesian model comparison approach. Brain Topogr. 2012;25:27–38.CrossRefGoogle Scholar
  49. Lei X, Wang Y, Yuan H, Mantini D. Neuronal oscillations and functional interactions between resting state networks: effects of alcohol intoxication. Hum Brain Mapp. 2014;35:3517–28.PubMedCrossRefGoogle Scholar
  50. Lei X, Wang Y, Yuan H, Chen A. Brain scale-free properties in awake rest and NREM sleep: a simultaneous EEG/fMRI study. Brain Topogr. 2015;28:292–304.PubMedCrossRefGoogle Scholar
  51. Leopold DA, Maier A. Ongoing physiological processes in the cerebral cortex. Neuroimage. 2012;62:2190–200.PubMedCrossRefGoogle Scholar
  52. Liu AK, Belliveau JW, Dale AM. Spatiotemporal imaging of human brain activity using functional MRI constrained magnetoencephalography data: Monte Carlo simulations. Proc Natl Acad Sci U S A. 1998;95:8945–50.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;412:150–7.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Makeig S, Westerfield M, Jung TP, Enghoff S, Townsend J, Courchesne E, Sejnowski TJ. Dynamic brain sources of visual evoked responses. Science. 2002;295:690–4.CrossRefGoogle Scholar
  55. Mantini D, Perrucci MG, Del Gratta C, Romani GL, Corbetta M. Electrophysiological signatures of resting state networks in the human brain. Proc Natl Acad Sci U S A. 2007;104:13170–5.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Masterton RA, Abbott DF, Fleming SW, Jackson GD. Measurement and reduction of motion and ballistocardiogram artefacts from simultaneous EEG and fMRI recordings. Neuroimage. 2007;37:202–11.PubMedCrossRefGoogle Scholar
  57. Moosmann M, Ritter P, Krastel I, Brink A, Thees S, Blankenburg F, Taskin B, Obrig H, Villringer A. Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy. Neuroimage. 2003;20:145–58.PubMedCrossRefGoogle Scholar
  58. Mullinger KJ, Yan WX, Bowtell R. Reducing the gradient artefact in simultaneous EEG-fMRI by adjusting the subject’s axial position. Neuroimage. 2011;54:1942–50.PubMedCrossRefGoogle Scholar
  59. Murta T, Leite M, Carmichael DW, Figueiredo P, Lemieux L. Electrophysiological correlates of the BOLD signal for EEG-informed fMRI. Hum Brain Mapp. 2015;36:391–414.PubMedCrossRefGoogle Scholar
  60. Nguyen VT, Breakspear M, Cunnington R. Fusing concurrent EEG-fMRI with dynamic causal modeling: application to effective connectivity during face perception. Neuroimage. 2014;  https://doi.org/10.1016/j.neuroimage.2013.06.083.PubMedCrossRefGoogle Scholar
  61. Niazy RK, Beckmann CF, Iannetti GD, Brady JM, Smith SM. Removal of FMRI environment artifacts from EEG data using optimal basis sets. Neuroimage. 2005;28:720–37.PubMedCrossRefGoogle Scholar
  62. Nunez P. Neocortical dynamics and human EEG rhythms. Oxford: Oxford University Press; 1995.Google Scholar
  63. Phillips C, Rugg MD, Fristont KJ. Systematic regularization of linear inverse solutions of the EEG source localization problem. Neuroimage. 2002;17:287–301.PubMedCrossRefGoogle Scholar
  64. Raichle ME, Mintun MA. Brain work and brain imaging. Annu Rev Neurosci. 2006;29:449–76.PubMedCrossRefGoogle Scholar
  65. Ritter P, Freyer F, Curio G, Villringer A. High-frequency (600 Hz) population spikes in human EEG delineate thalamic and cortical fMRI activation sites. Neuroimage. 2008;42:483–90.PubMedCrossRefPubMedCentralGoogle Scholar
  66. Rosa MJ, Kilner J, Blankenburg F, Josephs O, Penny W. Estimating the transfer function from neuronal activity to BOLD using simultaneous EEG-fMRI. Neuroimage. 2010;49:1496–509.PubMedPubMedCentralCrossRefGoogle Scholar
  67. Schabus M, Dang-Vu TT, Albouy G, Balteau E, Boly M, Carrier J, Darsaud A, Degueldre C, Desseilles M, Gais S, Phillips C, Rauchs G, Schnakers C, Sterpenich V, Vandewalle G, Luxen A, Maquet P. Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc Natl Acad Sci. 2007;104:13164–9.PubMedCrossRefPubMedCentralGoogle Scholar
  68. Scholvinck ML, Leopold DA, Brookes MJ, Khader PH. The contribution of electrophysiology to functional connectivity mapping. Neuroimage. 2013;80:297–306.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Schubert R, Ritter P, Wustenberg T, Preuschhof C, Curio G, Sommer W, Villringer A. Spatial attention related SEP amplitude modulations covary with BOLD signal in S1--a simultaneous EEG--fMRI study. Cerebral Cortex. 2008;18:2686–700.PubMedCrossRefPubMedCentralGoogle Scholar
  70. Shirer WR, Ryali S, Rykhlevskaia E, Menon V, Greicius MD. Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cerebral Cortex. 2012;22:158–65.PubMedCrossRefPubMedCentralGoogle Scholar
  71. Stancak A, Polacek H, Vrana J, Rachmanova R, Hoechstetter K, Tintra J, Scherg M. EEG source analysis and fMRI reveal two electrical sources in the fronto-parietal operculum during subepidermal finger stimulation. Neuroimage. 2005;25:8–20.PubMedCrossRefPubMedCentralGoogle Scholar
  72. Steyrl D, Krausz G, Koschutnig K, Edlinger G, Müller-Putz GR. Online reduction of artifacts in EEG of simultaneous EEG-fMRI using reference layer adaptive filtering (RLAF). Brain Topogr. 2017;31(1):129–49.PubMedPubMedCentralCrossRefGoogle Scholar
  73. Tamminen J, Payne JD, Stickgold R, Wamsley EJ, Gaskell MG. Sleep spindle activity is associated with the integration of new memories and existing knowledge. J Neurosci. 2010;30:14356–60.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Trujillo-Barreto N, Martinez-Montes E, Melie-Garcia L, Valdes-Sosa P. A symmetrical Bayesian model for fMRI and EEG/MEG neuroimage fusion. Int J Bioelectromag. 2001;3:1.Google Scholar
  75. Uehara T, Yamasaki T, Okamoto T, Koike T, Kan S, Miyauchi S, Kira J-I, Tobimatsu S. Efficiency of a “Small-World” brain network depends on consciousness level: a resting-state fMRI study. Cerebral Cortex. 2014;24:1529–39.PubMedCrossRefGoogle Scholar
  76. Valdes-Sosa PA, Sanchez-Bornot JM, Sotero RC, Iturria-Medina Y, Aleman-Gomez Y, Bosch-Bayard J, Carbonell F, Ozaki T. Model driven EEG/fMRI fusion of brain oscillations. Hum Brain Mapp. 2009;30:2701–21.CrossRefGoogle Scholar
  77. van der Meer JN, Pampel A, Van Someren EJW, Ramautar JR, van der Werf YD, Gomez-Herrero G, Lepsien J, Hellrung L, Hinrichs H, Moller HE, Walter M. Carbon-wire loop based artifact correction outperforms post-processing EEG/fMRI corrections--a validation of a real-time simultaneous EEG/fMRI correction method. Neuroimage. 2016;125:880–94.PubMedCrossRefGoogle Scholar
  78. Vincent JL, Larson-Prior LJ, Zempel JM, Snyder AZ. Moving GLM ballistocardiogram artifact reduction for EEG acquired simultaneously with fMRI. Clin Neurophysiol. 2007;118:981–98.PubMedCrossRefGoogle Scholar
  79. Vulliemoz S, Rodionov R, Carmichael DW, Thornton R, Guye M, Lhatoo SD, Michel CM, Duncan JS, Lemieux L. Continuous EEG source imaging enhances analysis of EEG-fMRI in focal epilepsy. Neuroimage. 2010;49:3219–29.PubMedCrossRefGoogle Scholar
  80. Wan X, Riera J, Iwata K, Takahashi M, Wakabayashi T, Kawashima R. The neural basis of the hemodynamic response nonlinearity in human primary visual cortex: Implications for neurovascular coupling mechanism. Neuroimage. 2006;32:616–25.PubMedCrossRefGoogle Scholar
  81. Wang K, Li W, Dong L, Zou L, Wang C. Clustering-constrained ICA for ballistocardiogram artifacts removal in simultaneous EEG-fMRI. Front Neurosci. 2018;12:59.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Xia H, Ruan D, Cohen MS. Removing ballistocardiogram (BCG) artifact from full-scalp EEG acquired inside the MR scanner with Orthogonal Matching Pursuit (OMP). Front Neurosci. 2014;8:218.PubMedPubMedCentralGoogle Scholar
  83. Yu Q, Erhardt EB, Sui J, Du Y, He H, Hjelm D, Cetin MS, Rachakonda S, Miller RL, Pearlson G, Calhoun VD. Assessing dynamic brain graphs of time-varying connectivity in fMRI data: application to healthy controls and patients with schizophrenia. Neuroimage. 2015;107:345–55.PubMedCrossRefGoogle Scholar
  84. Yu Q, Wu L, Bridwell DA, Erhardt EB, Du Y, He H, Chen J, Liu P, Sui J, Pearlson G, Calhoun VD. Building an EEG-fMRI multi-modal brain graph: a concurrent EEG-fMRI study. Front Hum Neurosci. 2016;10:476.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Zich C, Debener S, Kranczioch C, Bleichner MG, Gutberlet I, De Vos M. Real-time EEG feedback during simultaneous EEG-fMRI identifies the cortical signature of motor imagery. Neuroimage. 2015;114:438–47.PubMedCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Sleep and Neuroimaging Centre, Faculty of PsychologySouthwest UniversityChongqingChina

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