Combining EEG and fMRI

  • Karen Mullinger
  • Richard Bowtell
Part of the Methods in Molecular Biology book series (MIMB, volume 711)


The combination of electroencephalography (EEG) with functional magnetic resonance imaging (fMRI) forms a powerful tool for the investigation of brain function, but concurrent implementation of EEG and fMRI poses many technical challenges. Here, the motivation for combining EEG and fMRI is explored and methods underlying the combination are described. After a brief introduction to the two different techniques, the advantages and disadvantages of different methods of data recording are detailed, followed by a description of the artefacts encountered when performing EEG and fMRI measurements simultaneously, and the methods which have been developed to eliminate these artefacts. Important safety considerations and potential pitfalls associated with simultaneous recording are also described. The ways in which EEG and fMRI data analysis can be integrated are then described along with examples of key work which illustrate the power of combined EEG/fMRI measurements. The chapter concludes with a brief discussion of future directions for combined EEG/fMRI research.

Key words

Simultaneous EEG–fMRI gradient artefact correction pulse artefact correction B0 inhomogeneity B1 inhomogeneity EEG–fMRI safety EEG–fMRI data fusion 


  1. 1.
    Berger, H. Uber das elektrenkephalogramm des menschen. Arch Psychiatr Nervenkr 1929;87:527–570.CrossRefGoogle Scholar
  2. 2.
    Berger, H. On the electroencephalogram of man. Electroencephalogr Clin Neurophysiol 1969;Supplement 28:37–73.Google Scholar
  3. 3.
    Phillips, C. Source Estimation in EEG. Combining Anatomical and Functional Constraints [PhD]. Belgium: University de Liege; 2000.Google Scholar
  4. 4.
    Michel, C. M., Thut, G., Morand, S. et al. Review: Electric source imaging of human brain functions. Brain Res Rev 2001;36:108–118.PubMedCrossRefGoogle Scholar
  5. 5.
    Kwong, K., Belliveau, J., Chesler, D. A. et al. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci USA 1992;23:3963–3971.Google Scholar
  6. 6.
    Ogawa, S., Menon, R. S., Tank, D. W., Kim, S. -G., Merkle, H., Ellermann, J. M., Ugurbil, K. Functional brain mapping by blood oxygenation level dependent contrast magnetic resonance imaging. Biophys J 1993;64:803–812.PubMedCrossRefGoogle Scholar
  7. 7.
    Ogawa, S., Lee, T. M., Kay, A. R., Tank, D. W. Brain magnetic-resonance-imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A 1990;87:9868–9872.PubMedCrossRefGoogle Scholar
  8. 8.
    Detre, J. A., Leigh, J. S., Williams, D. S., Koretsky, A. P. Perfusion imaging. Magn Reson Med Sci 1992;23:37–45.CrossRefGoogle Scholar
  9. 9.
    Kim, S. G. Quantification of relative cerebral blood-flow changed by flow-sensitive alternating inversion -recovery (FAIR) technique-application to functional mapping. Magn Reson Med Sci 1995;34:293–301.CrossRefGoogle Scholar
  10. 10.
    Blockley, N. P., Francis, S. T., Gowland, P. A. Perturbation of the BOLD response by contrast agent and interpretation through a modified balloon model. Neuroimage 2009;48:84–93.PubMedGoogle Scholar
  11. 11.
    Frahm, J., Baudewig, J., Kallenberg, K., Kastrup, A., Merboldt, K. D., Dechent, P. The post-stimulation understoot in BOLD fMRI of human brain is not caused by elevated cerebral blood volume. Neuroimage 2008;40:473–481.PubMedCrossRefGoogle Scholar
  12. 12.
    Buxton, R. B. Introduction to Functional Magnetic Resonance Imaging: Principles and Techniques. New York, NY: Cambridge University Press; 2002.Google Scholar
  13. 13.
    Bonmassar, G., Schwartz, D. P., Liu, A. K., Kwong, K., Dale, A. M., Belliveau, J. Spatiotemporal brain imaging of visual-evoked activity using interleaved EEG and fMRI recordings. Neuroimage 2001;13:1035–1043.PubMedCrossRefGoogle Scholar
  14. 14.
    Krakow, K., Woermann, F. G., Symms, M. R. et al. EEG-triggered functional MRI of interictal epileptiform activity in patients with partial seizures. Brain 1999;122:1679–1688.PubMedCrossRefGoogle Scholar
  15. 15.
    Haacke, E. M., Brown, R. W., Thompson, M. R., Venkatesan, R. Magnetic Resonance Imaging: Physical Principles and Sequence Design. New York, NY: Wiley; 1999.Google Scholar
  16. 16.
    Debener, S., Ullsperger, M., Siegel, M., Engel, A. K. Single-trial EEG-fMRI reveals the dynamics of cognitive function. Trends Cogn Sci 2006;10:558–563.PubMedCrossRefGoogle Scholar
  17. 17.
    Laufs, H. Endogenous brain oscialltions and related networks detected by surface EEG-combined fMRI. Hum Brain Mapp 2008;29:762–769.PubMedCrossRefGoogle Scholar
  18. 18.
    Laufs, H., Krakow, K., Sterzer, P. et al. Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest. Proc Natl Acad Sci USA 2003;100:11053–11058.PubMedCrossRefGoogle Scholar
  19. 19.
    Ritter, P., Villringer, A. Review: Simultaneous EEG-fMRI. Neurosci Behav Rev 2006;30:823–838.CrossRefGoogle Scholar
  20. 20.
    Vulliemoz, S., Thornton, R., Rodionov, R. et al. The spatio-temporal mapping of epileptic networks: Combination of EEG-fMRI and EEG source imaging. Neuroimage 2009;46:834–843.PubMedCrossRefGoogle Scholar
  21. 21.
    Parkes, L. M., Bastiaansen, M. C. M., Norris, D. G. Combining EEG adn fMRI to investigate the post-movement beta rebound. Neuroimage 2006;29:685–696.PubMedCrossRefGoogle Scholar
  22. 22.
    Keller, F. J., Gettys, W. E., Skove, M. J. Physics: Classical and Modern, 2nd ed. New York, NY: McGraw-Hill; 1993.Google Scholar
  23. 23.
    Tenforde, T. S., Gaffey, C. T., Moyer, B. R., Budinger, T. F. Cardiovascular alterations in macaca monkeys exposed to stationary magnetic fields: Experimental observations and theoretical analysis. Bioelectromagnetics 1983;4:1–9.PubMedCrossRefGoogle Scholar
  24. 24.
    Allen, P. J., Poizzi, G., Krakow, K., Fish, D. R., Lemieux, L. Identification of EEG events in the MR scanner: The problem of pulse artifact and a method for its subtraction. Neuroimage 1998;8:229–239.PubMedCrossRefGoogle Scholar
  25. 25.
    Allen, P. J., Josephs, O., Turner, R. A. Method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 2000;12:230–239.PubMedCrossRefGoogle Scholar
  26. 26.
    Ives, J. R., Warach, S., Schmitt, F., Edelman, R. R., Schomer, D. L. Monitoring a patient’s EEG during echo planar MRI. Electroencephalogr Clin Neurophysiol 1993;87:417–420.PubMedCrossRefGoogle Scholar
  27. 27.
    Debener, S., Mullinger, K. J., Niazy, R. K., Bowtell, R. W. Properties of the ballistocardiogram artefact as revealed by EEG recordings at 1.5, 3 and 7 tesla static magnetic field strength. Int J Psychophysiol 2008;67:189–199.PubMedCrossRefGoogle Scholar
  28. 28.
    Yan, W. X., Mullinger, K. J., Geirsdottir, G. B., Bowtell, R. W. Physical modelling of pulse artefact sources in simultaneous EEG/fMRI. Hum Brain Mapp 2009;31:604–620.Google Scholar
  29. 29.
    Anami, K., Mori, T., Tanaka, F. et al. Stepping stone sampling for retrieving artifact-free electoencephalogram during functional magnetic resonance imaging. Neuroimage 2003;19:281–295 (Part 1).PubMedCrossRefGoogle Scholar
  30. 30.
    Freyer, F., Becker, R., Anami, K., Curio, G., Villringer, A., Ritter, P. Ultra high-frequency EEG during fMRI: Pushing the limits of imaging-artifact correction. Neuroimage 2009;48:94–108.PubMedCrossRefGoogle Scholar
  31. 31.
    Mandelkow, H., Brandeis, D., Boesiger, P. Good practices in EEG-fMRI: The utility of retrospective synchronisation and PCA for the removal of MRI gradient artefacts. Neuroimage 2009;49:2287–2303.PubMedCrossRefGoogle Scholar
  32. 32.
    Gutberlet, I. BP_Press_Release_Issue_N3. Brain Products 2001;10.Google Scholar
  33. 33.
    Moosmann, M., Schonfelder, V. H., Specht, K., Scheeringa, R., Nordby, H., Hugdahl, K. Realignment parameter-informed artefact correction for simultaneous EEG-fMRI recordings. Neuroimage 2009;45:1144–1150.PubMedCrossRefGoogle Scholar
  34. 34.
    Naizy, R. K., Bechmann, C. F., Iannetti, G. D., Brady, J. M., Smith, S. M. Removal of fMRI environment artifacts from EEG data using optimal basis sets. Neuroimage 2005;28:720–737.CrossRefGoogle Scholar
  35. 35.
    Debener, S., Strobel, A., Sorger, B. et al. Improved quality of auditory event-related potentials recorded simultaneously with 3-T fMRI: Removal of the ballistocardiogram artefact. Neuroimage 2007;34:587–597.PubMedCrossRefGoogle Scholar
  36. 36.
    Iriarte, J., Urrestarazu, E., Valencia, M. et al. Independent component analysis as a tool to eliminate artifacts in EEG: A quantitative study. J Clin Neurophysiol 2003;20:249–257.PubMedCrossRefGoogle Scholar
  37. 37.
    Jung, T. P., Makeig, S., Humphries, C. et al. Removing electroencephalographic artifacts by blind source separation. Psychophysiology 2000;37:163–178.PubMedCrossRefGoogle Scholar
  38. 38.
    Makeig, S., Westernfield, M., Jung, T. P. et al. Functionally independent components of the late positive event-related potential during visual spatial attention. J Neurosci 1999;19:2665–2680.PubMedGoogle Scholar
  39. 39.
    Srivastava, G., Crottaz-Herbette, S., Lau, K. M., Glover, G. H., Menon, V. ICA-based procedures for removing ballistocariogram artifacts from EEG data acquired in MRI scanner. Neuroimage 2005;24:50–60.PubMedCrossRefGoogle Scholar
  40. 40.
    Mantini, D., Perrucci, M. G., Cugini, S., Ferretti, A., Romani, G. L., Del Gratta, C. Complete artifact removal for EEG recorded during continuous fMRI using independent component analysis. Neuroimage 2007;34:598–607.PubMedCrossRefGoogle Scholar
  41. 41.
    Assecondi, S., Hallez, H., Staelens, S., Bianchi, A. M., Huiskamp, G. M., Lemahieu, I. Removal of the ballistocardiographic artifact from EEG-fMRI data: A canonical correlation approach. Phys Med Biol 2009;54:1673–1689.PubMedCrossRefGoogle Scholar
  42. 42.
    Sun, L., Rieger, J., Hinrichs, H. Maximum noise fraction (MNF) transforms to remove ballistocariographic artifacts in EEG signals recorded during fMRI scanning. Neuroimage 2009;46:144–153.PubMedCrossRefGoogle Scholar
  43. 43.
    Van Veen, B. D., van Drongelen, W., Yuchtman, M., Suzuki, A. Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE Trans Biomed Eng 1997;44:867–880.PubMedCrossRefGoogle Scholar
  44. 44.
    Brookes, M. J., Mullinger, K. J., Stevenson, C. M., Morris, P. G., Bowtell, R. W. Simultaneous EEG source localisation and artifact rejection during concurrent fMRI by means of spatial filtering. Neuroimage 2008;40:1090–1104.PubMedCrossRefGoogle Scholar
  45. 45.
    Brookes, M. J., Vrba, J., Mullinger, K. J. et al. Source localisation in concurrent EEG/fMRI: Applications at 7t. Neuroimage 2009;45:440–452.PubMedCrossRefGoogle Scholar
  46. 46.
    Dunseath, W. J. R. Interference reduction apparatus for electroencephalography (EEG) measurement, has one or more of reference electrodes arranged to be in close physical proximity but not in direct electrical contact with subject.Google Scholar
  47. 47.
    Mullinger, K. J., Debener, S., Coxon, R., Bowtell, R. W. Effects of simultaneous EEG recording on MRI data quality at 1.5, 3 and 7 tesla. Int J Psychophysiol 2008;67:178–188.PubMedCrossRefGoogle Scholar
  48. 48.
    Scarff, C. J., Reynolds, A., Goodyear, B. G., Ponton, C. W., Dort, J. C., Eggermont, J. J. Simultaneous 3-T fMRI and high-density recording of human auditory evoked potentials. Neuroimage 2004;23:1129–1142.PubMedCrossRefGoogle Scholar
  49. 49.
    Yarnykh, V. L. Actual flip angle imaging in the pulsed steady state: A method for rapid three-dimensional mapping of the transmitted radio frequency field. Magn Reson Med Sci 2007;51:192–200.Google Scholar
  50. 50.
    Krakow, K., Allen, P. J., Symms, M. R., Lemieux, L., Josephs, O., Fish, D. R. EEG recording during fMRI experiments: Image quality. Hum Brain Mapp 2000;10:10–15.PubMedCrossRefGoogle Scholar
  51. 51.
    Stevens, T. K., Ives, J. R., Bartha, R. Energy Coupling between Electric Fields and Conductive Wires: Image Artifacts and Heating. In Joint Annual meeting ISMRM-ESMRMB; 2007 19–25 May; Berlin; 2007.Google Scholar
  52. 52.
    Stevens, T. K., Ives, J. R., Klassen, L. M., Bartha, R. MR compatibility of EEG scalp electrodes at 4 tesla. J Magn Reson Imaging 2007;25:872–877.PubMedCrossRefGoogle Scholar
  53. 53.
    Vasios, C. E., Angelone, L. M., Purdon, P. L., Ahveninen, J., Belliveau, J., Bonmassar, G. EEG/(f)MRI measurements at 7 tesla using a new EEG cap (“InkCAP”). Neuroimage 2006;33:1082–1092.PubMedCrossRefGoogle Scholar
  54. 54.
    Adriany, G., Van de Moortele, P. F., Wiesinger, F. et al. Transmit and receive transmission line arrays for 7 tesla parallel imaging. Magn Reson Med Sci 2005;53:434–445.CrossRefGoogle Scholar
  55. 55.
    Katscher, U., Bornert, P. Parallel RF transmission in MRI. NMR Biomed 2006;19:393–400.PubMedCrossRefGoogle Scholar
  56. 56.
    Lemieux, L., Allen, P. J., Franconi, F., Symms, M. R., Fish, D. R. Recording of EEG during fMRI experiments: Patient safety. Magn Reson Med Sci 1997;38:943–952.CrossRefGoogle Scholar
  57. 57.
    Lazeyras, F., Zimine, I., Blanke, O., Perrig, S. H., Seeck, M. Functional MRI with simultaneous EEG recording: Feasibility and application to motor and visual activation. J Magn Reson Imaging 2001;13:943–948.PubMedCrossRefGoogle Scholar
  58. 58.
    Angelone, L. M., Potthast, A., Segonne, F., Iwaki, S., Belliveau, J. W., Bonmassar, G. Metallic electrodes and leads in simultaneous EEG-MRI: Specific absorption rate (SAR) simulation studies. Bioelectromagnetics 2004;25:285–295.PubMedCrossRefGoogle Scholar
  59. 59.
    Mullinger, K. J., Brookes, M. J., Stevenson, C. M., Morgan, P. S., Bowtell, R. W. Exploring the feasibility of simultaneous EEG/fMRI at 7 T. Magn Reson Imag 2008;26:607–616.CrossRefGoogle Scholar
  60. 60.
    Agency, H. P. Protection of Patients and Volunteers Undergoing MRI Procedures. In: Radiation CaEH, ed. Health Protection Agency; 2008;90.Google Scholar
  61. 61.
    ICNIRP Guidelines for limiting exposure to time-varying electric, magnetic and electromagnetic fields (up to 300 GHz). Health Phys 1998;74:494–522.Google Scholar
  62. 62.
    ICNIRP Medical magnetic resoance (MR) procedures: Protection of patients. Health Phys 2004;87:197–216.CrossRefGoogle Scholar
  63. 63.
    Mandelkow, H., Halder, P., Boesiger, P., Brandeis, D. Synchronisation facilitates removal of MRI artefacts from concurrent EEG recordings and increases usable bandwidth. Neuroimage 2006;32:1120–1126.PubMedCrossRefGoogle Scholar
  64. 64.
    Mullinger, K. J., Morgan, P. S., Bowtell, R. W. Improved artefact correction for combined electroencephalography/functional MRI by means of synchronization and use of VCG recordings. J Magn Reson Imaging 2008;27:607–616.PubMedCrossRefGoogle Scholar
  65. 65.
    Kilner, J. M., Mattout, J., Henson, R., Friston, K. J. Hemodynamic correlates of EEG: A heuristic. Neuroimage 2005;28:280–286.PubMedCrossRefGoogle Scholar
  66. 66.
    Goldman, R. I., Stern, J. M., Engel, J., Cohen, M. S. Simultaneous EEG and fMRI of the alpha rhythm. NeuroReport 2002;13:2487–2492.PubMedCrossRefGoogle Scholar
  67. 67.
    Moosmann, M., Ritter, P., Krastel, I. et al. Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy. Neuroimage 2003;20:145–158.PubMedCrossRefGoogle Scholar
  68. 68.
    Koch, S. P., Steinbrink, J., Villringer, A., Obrig, H. Synchronisation between background activity adn visually evoked potential is not mirrored by focal hyperoxygenation: Implications for the interpretation of vascular brain imaging. J Neurosci 2006;26:4940–4948.PubMedCrossRefGoogle Scholar
  69. 69.
    Scheeringa, R., Petersson, K. M., Oostenveld, R., Norris, D. G., Hagoort, P., Bastiaansen, M. C. M. Trial-by-trial coupling between EEG and BOLD identifies networks related to alpha and theta EEG power increases during working memory maintance. Neuroimage 2009;44:1224–1238.PubMedCrossRefGoogle Scholar
  70. 70.
    Eichele, T., Specht, K., Moosmann, M. et al. Assessing the spatiotemporal evolution of neuronal activation with single-trial event-related potential and functional MRI. Proc Natl Acad Sci USA 2005;102:17789–17803.CrossRefGoogle Scholar
  71. 71.
    Mulert, C., Jager, L., Schmitt, R. et al. Integration of fMRI and simultaneous EEG: Towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage 2004;22:83–94.PubMedCrossRefGoogle Scholar
  72. 72.
    Phillips, C., Rugg, M. D., Friston, K. J. Anatomically informed basis functions for EEG source localization: Combining functional and anatomical constraints. Neuroimage 2002;16:678–695.PubMedCrossRefGoogle Scholar
  73. 73.
    Wan, X., Sekiguchi, A., Yokoyama, S. R., Riera, J., Kawashima, R. Electromagnetic source imaging: Backus-Gilbert resolution spread function-constrained and funtional MRI-guided spatial filtering. Hum Brain Mapp 2008;29:627–643.PubMedCrossRefGoogle Scholar
  74. 74.
    Ostwald, D., Porcaro, C., Bagshaw, A. P. An information theoretic approach to EEG-fMRI integration of visually evoked responses. Neuroimage 2010;49:498–516.PubMedCrossRefGoogle Scholar
  75. 75.
    Sotero, R. C., Trujillo-Barreto, N. J. Biophysical model for integrating neuronal activity, EEG, fMRI and metabolism. Neuroimage 2008;39:290–309.PubMedCrossRefGoogle Scholar
  76. 76.
    Salek-Haddadi, A., Friston, K. J., Lemieux, L., Fish, D. R. Review: Studying spontaneous EEG activity with fMRI. Brain Res Rev 2003;43:110–133.PubMedCrossRefGoogle Scholar
  77. 77.
    Bates, A. T., Keiehl, K. A., Laurens, K. R., Liddle, P. F. Low-frequency EEG oscillations associated with information processing in schizophrenia. Schizophr Res 2009;115:220–230.CrossRefGoogle Scholar
  78. 78.
    Czisch, M., Wetter, T. C., Kaufmann, C., Pollmacher, T., Holsboer, F., Auer, D. P. Altered processing of acoustic stimuli during sleep: Reduced auditory activation and visual deactivation detected by a combined fMRI/EEG study. Neuroimage 2002;16:251–258.PubMedCrossRefGoogle Scholar
  79. 79.
    Wacker, J., Dillon, D. G., Pissagalli, D. A. The role of the nucleus accumbens and rostal anterior cingulate cortex in anhedonia: Integration of resting EEG, FMRI and volumetric techniques. Neuroimage 2009;46:327–337.PubMedCrossRefGoogle Scholar
  80. 80.
    Logothetis, N. K. The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philos Trans R Soc Lond B Biol Sci 2002;357:1003–1037.PubMedCrossRefGoogle Scholar
  81. 81.
    Nir, Y., Fisch, L., Mukamel, R. et al. Coupling between neuronal firing rate, gamma LFP, and BOLD MRI is related to interneuronal correlations. Curr Biol 2007;17:1275–1285.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.School of Physics and Astronomy, Sir Peter Mansfield Magnetic Resonance CentreUniversity of NottinghamNottinghamUK

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