Skip to main content

Advertisement

SpringerLink
Log in

Presurgical brain mapping in epilepsy using simultaneous EEG and functional MRI at ultra-high field: feasibility and first results

  • Research Article
  • Published:
Magnetic Resonance Materials in Physics, Biology and Medicine Aims and scope Submit manuscript

Abstract

Objectives

The aim of this study was to demonstrate that eloquent cortex and epileptic-related hemodynamic changes can be safely and reliably detected using simultaneous electroencephalography (EEG)–functional magnetic resonance imaging (fMRI) recordings at ultra-high field (UHF) for clinical evaluation of patients with epilepsy.

Materials and methods

Simultaneous EEG–fMRI was acquired at 7 T using an optimized setup in nine patients with lesional epilepsy. According to the localization of the lesion, mapping of eloquent cortex (language and motor) was also performed in two patients.

Results

Despite strong artifacts, efficient correction of intra-MRI EEG could be achieved with optimized artifact removal algorithms, allowing robust identification of interictal epileptiform discharges. Noise-sensitive topography-related analyses and electrical source localization were also performed successfully. Localization of epilepsy-related hemodynamic changes compatible with the lesion were detected in three patients and concordant with findings obtained at 3 T. Local loss of signal in specific regions, essentially due to B 1 inhomogeneities were found to depend on the geometric arrangement of EEG leads over the cap.

Conclusion

These results demonstrate that presurgical mapping of epileptic networks and eloquent cortex is both safe and feasible at UHF, with the benefits of greater spatial resolution and higher blood-oxygenation-level-dependent sensitivity compared with the more traditional field strength of 3 T.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, Ugurbil K (1992) Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 89(13):5951–5955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Turner R, Jezzard P, Wen H, Kwong KK, Le Bihan D, Zeffiro T, Balaban RS (1993) Functional mapping of the human visual cortex at 4 and 1.5 tesla using deoxygenation contrast EPI. Magn Reson Med 29(2):277–279

    Article  CAS  PubMed  Google Scholar 

  3. van der Zwaag W, Francis S, Head K, Peters A, Gowland P, Morris P, Bowtell R (2009) fMRI at 1.5, 3 and 7 T: characterising BOLD signal changes. Neuroimage 47(4):1425–1434

    Article  PubMed  Google Scholar 

  4. Duong TQ, Yacoub E, Adriany G, Hu X, Ugurbil K, Kim SG (2003) Microvascular BOLD contribution at 4 and 7 T in the human brain: gradient-echo and spin-echo fMRI with suppression of blood effects. Magn Reson Med 49(6):1019–1027

    Article  PubMed  Google Scholar 

  5. Bianciardi M, Fukunaga M, van Gelderen P, de Zwart JA, Duyn JH (2011) Negative BOLD-fMRI signals in large cerebral veins. J Cereb Blood Flow Metab 31(2):401–412

    Article  PubMed  PubMed Central  Google Scholar 

  6. Felblinger J, Slotboom J, Kreis R, Jung B, Boesch C (1999) Restoration of electrophysiological signals distorted by inductive effects of magnetic field gradients during MR sequences. Magn Reson Med 41(4):715–721

    Article  CAS  PubMed  Google Scholar 

  7. Allen PJ, Josephs O, Turner R (2000) A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 12(2):230–239

    Article  CAS  PubMed  Google Scholar 

  8. Grouiller F, Vercueil L, Krainik A, Segebarth C, Kahane P, David O (2007) A comparative study of different artefact removal algorithms for EEG signals acquired during functional MRI. Neuroimage 38(1):124–137

    Article  PubMed  Google Scholar 

  9. Jorge J, Grouiller F, Gruetter R, van der Zwaag W, Figueiredo P (2015) Towards high-quality simultaneous EEG–fMRI at 7T: detection and reduction of EEG artifacts due to head motion. Neuroimage 120:143–153

    Article  PubMed  Google Scholar 

  10. Mullinger KJ, Havenhand J, Bowtell R (2013) Identifying the sources of the pulse artefact in EEG recordings made inside an MR scanner. Neuroimage 71:75–83

    Article  PubMed  PubMed Central  Google Scholar 

  11. Yan WX, Mullinger KJ, Geirsdottir GB, Bowtell R (2010) Physical modeling of pulse artefact sources in simultaneous EEG/fMRI. Hum Brain Mapp 31(4):604–620

    PubMed  Google Scholar 

  12. Vanderperren K, De Vos M, Ramautar JR, Novitskiy N, Mennes M, Assecondi S, Vanrumste B, Stiers P, Van den Bergh BR, Wagemans J, Lagae L, Sunaert S, Van Huffel S (2010) Removal of BCG artifacts from EEG recordings inside the MR scanner: a comparison of methodological and validation-related aspects. Neuroimage 50(3):920–934

    Article  PubMed  Google Scholar 

  13. Arrubla J, Neuner I, Dammers J, Breuer L, Warbrick T, Hahn D, Poole MS, Boers F, Shah NJ (2014) Methods for pulse artefact reduction: experiences with EEG data recorded at 9.4 T static magnetic field. J Neurosci Methods 232:110–117

    Article  PubMed  Google Scholar 

  14. Debener S, Mullinger KJ, Niazy RK, Bowtell RW (2008) Properties of the ballistocardiogram artefact as revealed by EEG recordings at 1.5, 3 and 7 T static magnetic field strength. Int J Psychophysiol 67(3):189–199

    Article  PubMed  Google Scholar 

  15. Debener S, Strobel A, Sorger B, Peters J, Kranczioch C, Engel AK, Goebel R (2007) Improved quality of auditory event-related potentials recorded simultaneously with 3-T fMRI: removal of the ballistocardiogram artefact. Neuroimage 34(2):587–597

    Article  PubMed  Google Scholar 

  16. Niazy RK, Beckmann CF, Iannetti GD, Brady JM, Smith SM (2005) Removal of FMRI environment artifacts from EEG data using optimal basis sets. Neuroimage 28(3):720–737

    Article  CAS  PubMed  Google Scholar 

  17. Rothlubbers S, Relvas V, Leal A, Figueiredo P (2013) Reduction of EEG artefacts induced by vibration in the MR-environment. Conf Proc IEEE Eng Med Biol Soc 2013:2092–2095

    PubMed  Google Scholar 

  18. Nierhaus T, Gundlach C, Goltz D, Thiel SD, Pleger B, Villringer A (2013) Internal ventilation system of MR scanners induces specific EEG artifact during simultaneous EEG–fMRI. Neuroimage 74:70–76

    Article  PubMed  Google Scholar 

  19. Jorge J, Grouiller F, Ipek O, Stoermer R, Michel CM, Figueiredo P, van der Zwaag W, Gruetter R (2015) Simultaneous EEG–fMRI at ultra-high field: artifact prevention and safety assessment. Neuroimage 105:132–144

    Article  PubMed  Google Scholar 

  20. Moosmann M, Schonfelder VH, Specht K, Scheeringa R, Nordby H, Hugdahl K (2009) Realignment parameter-informed artefact correction for simultaneous EEG–fMRI recordings. Neuroimage 45(4):1144–1150

    Article  PubMed  Google Scholar 

  21. Bonmassar G, Purdon PL, Jaaskelainen IP, Chiappa K, Solo V, Brown EN, Belliveau JW (2002) Motion and ballistocardiogram artifact removal for interleaved recording of EEG and EPs during MRI. Neuroimage 16(4):1127–1141

    Article  PubMed  Google Scholar 

  22. Masterton RA, Abbott DF, Fleming SW, Jackson GD (2007) Measurement and reduction of motion and ballistocardiogram artefacts from simultaneous EEG and fMRI recordings. Neuroimage 37(1):202–211

    Article  PubMed  Google Scholar 

  23. Mullinger K, Debener S, Coxon R, Bowtell R (2008) Effects of simultaneous EEG recording on MRI data quality at 1.5, 3 and 7 tesla. Int J Psychophysiol 67(3):178–188

    Article  PubMed  Google Scholar 

  24. Luo Q, Glover GH (2012) Influence of dense-array EEG cap on fMRI signal. Magn Reson Med 68(3):807–815

    Article  PubMed  PubMed Central  Google Scholar 

  25. Angelone LM, Potthast A, Segonne F, Iwaki S, Belliveau JW, Bonmassar G (2004) Metallic electrodes and leads in simultaneous EEG–MRI: specific absorption rate (SAR) simulation studies. Bioelectromagnetics 25(4):285–295

    Article  PubMed  Google Scholar 

  26. Dempsey MF, Condon B, Hadley DM (2001) Investigation of the factors responsible for burns during MRI. J Magn Reson Imaging 13(4):627–631

    Article  CAS  PubMed  Google Scholar 

  27. Schick F (2005) Whole-body MRI at high field: technical limits and clinical potential. Eur Radiol 15(5):946–959

    Article  PubMed  Google Scholar 

  28. Lemieux L, Allen PJ, Franconi F, Symms MR, Fish DR (1997) Recording of EEG during fMRI experiments: patient safety. Magn Reson Med 38(6):943–952

    Article  CAS  PubMed  Google Scholar 

  29. Marques JP, Kober T, Krueger G, van der Zwaag W, Van de Moortele PF, Gruetter R (2010) MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field. Neuroimage 49(2):1271–1281

    Article  PubMed  Google Scholar 

  30. Genetti M, Grouiller F, Vulliemoz S, Spinelli L, Seeck M, Michel CM, Schaller K (2013) Noninvasive language mapping in patients with epilepsy or brain tumors. Neurosurgery 72(4):555–565

    Article  PubMed  Google Scholar 

  31. Allen PJ, Polizzi G, Krakow K, Fish DR, Lemieux L (1998) Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 8(3):229–239

    Article  CAS  PubMed  Google Scholar 

  32. Sijbers J, Van Audekerke J, Verhoye M, Van der Linden A, Van Dyck D (2000) Reduction of ECG and gradient related artifacts in simultaneously recorded human EEG/MRI data. Magn Reson Imaging 18(7):881–886

    Article  Google Scholar 

  33. Iannotti GR, Pittau F, Michel CM, Vulliemoz S, Grouiller F (2015) Pulse artifact detection in simultaneous EEG–fMRI recording based on EEG map topography. Brain Topogr 28(1):21–32

    Article  PubMed  Google Scholar 

  34. Buades A, Coll B, Morel JM (2005) A review of image denoising algorithms, with a new one. Multiscale Model Simul 4(2):490–530

    Article  Google Scholar 

  35. Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35(3):346–355

    Article  CAS  PubMed  Google Scholar 

  36. Grouiller F, Thornton RC, Groening K, Spinelli L, Duncan JS, Schaller K, Siniatchkin M, Lemieux L, Seeck M, Michel CM, Vulliemoz S (2011) With or without spikes: localization of focal epileptic activity by simultaneous electroencephalography and functional magnetic resonance imaging. Brain 134(Pt 10):2867–2886

    Article  PubMed  PubMed Central  Google Scholar 

  37. Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, Grave de Peralta R (2004) EEG source imaging. Clin Neurophysiol 115(10):2195–2222

    Article  PubMed  Google Scholar 

  38. Brunet D, Murray MM, Michel CM (2011) Spatiotemporal analysis of multichannel EEG: CARTOOL. Comput Intell Neurosci 2011:813870

    Article  PubMed  PubMed Central  Google Scholar 

  39. de Peralta Grave, Menendez R, Murray MM, Michel CM, Martuzzi R, Gonzalez Andino SL (2004) Electrical neuroimaging based on biophysical constraints. Neuroimage 21(2):527–539

    Article  Google Scholar 

  40. Lantz G, Spinelli L, Seeck M, de Peralta Menendez RG, Sottas CC, Michel CM (2003) Propagation of interictal epileptiform activity can lead to erroneous source localizations: a 128-channel EEG mapping study. J Clin Neurophysiol 20(5):311–319

    Article  PubMed  Google Scholar 

  41. Eggenschwiler F, Kober T, Magill AW, Gruetter R, Marques JP (2012) SA2RAGE: a new sequence for fast B1 +-mapping. Magn Reson Med 67(6):1609–1619

    Article  CAS  PubMed  Google Scholar 

  42. Theysohn JM, Maderwald S, Kraff O, Moenninghoff C, Ladd ME, Ladd SC (2008) Subjective acceptance of 7 Tesla MRI for human imaging. Magn Reson Mater Phy 21(1–2):63–72

    Article  Google Scholar 

  43. Groening K, Brodbeck V, Moeller F, Wolff S, van Baalen A, Michel CM, Jansen O, Boor R, Wiegand G, Stephani U, Siniatchkin M (2009) Combination of EEG–fMRI and EEG source analysis improves interpretation of spike-associated activation networks in paediatric pharmacoresistant focal epilepsies. Neuroimage 46(3):827–833

    Article  PubMed  Google Scholar 

  44. Vulliemoz S, Thornton R, Rodionov R, Carmichael DW, Guye M, Lhatoo S, McEvoy AW, Spinelli L, Michel CM, Duncan JS, Lemieux L (2009) The spatio-temporal mapping of epileptic networks: combination of EEG–fMRI and EEG source imaging. Neuroimage 46(3):834–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Geissler A, Matt E, Fischmeister F, Wurnig M, Dymerska B, Knosp E, Feucht M, Trattnig S, Auff E, Fitch WT, Robinson S, Beisteiner R (2014) Differential functional benefits of ultra highfield MR systems within the language network. Neuroimage 103:163–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Beisteiner R, Robinson S, Wurnig M, Hilbert M, Merksa K, Rath J, Hollinger I, Klinger N, Marosi C, Trattnig S, Geissler A (2011) Clinical fMRI: evidence for a 7T benefit over 3T. Neuroimage 57(3):1015–1021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Vasios CE, Angelone LM, Purdon PL, Ahveninen J, Belliveau JW, Bonmassar G (2006) EEG/(f)MRI measurements at 7 Tesla using a new EEG cap (“InkCap”). Neuroimage 33(4):1082–1092

    Article  PubMed  Google Scholar 

  48. Gholipour T, Moeller F, Pittau F, Dubeau F, Gotman J (2011) Reproducibility of interictal EEG–fMRI results in patients with epilepsy. Epilepsia 52(3):433–442

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the Swiss National Science Foundation for Scientific Research (Grants 326030-150816, 33CM30-140332, 320030-141165 and 146633), by the Department of Radiology of Geneva University Hospitals (startup Grant 2013-10), and by the Center for Biomedical Imaging (CIBM) of the Universities and Hospitals of Geneva and Lausanne, and the EPFL.

Author information

Authors and Affiliations

  1. Department of Radiology and Medical Informatics, University of Geneva, Rue Gabrielle-Perret-Gentil 4, 1211, Geneva 14, Switzerland

    Frédéric Grouiller & François Lazeyras

  2. Laboratory for Functional and Metabolic Imaging, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland

    João Jorge

  3. ISR-Lisboa/LARSyS and Department of Bioengineering, Instituto Superior Técnico, Universidade de Lisboa, Lisbon, Portugal

    João Jorge

  4. EEG and Epilepsy Unit, Department of Neurology, Geneva University Hospitals, Geneva, Switzerland

    Francesca Pittau & Serge Vulliémoz

  5. Biomedical Imaging Research Center, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland

    Wietske van der Zwaag

  6. Spinoza Centre for Neuroimaging, Amsterdam, The Netherlands

    Wietske van der Zwaag

  7. Functional Brain Mapping Laboratory, Department of Fundamental Neurosciences, University of Geneva, Geneva, Switzerland

    Giannina Rita Iannotti & Christoph Martin Michel

  8. Division of Neuroradiology, Geneva University Hospitals, Geneva, Switzerland

    Maria Isabel Vargas

Authors
  1. Frédéric Grouiller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. João Jorge
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francesca Pittau
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wietske van der Zwaag
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Giannina Rita Iannotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christoph Martin Michel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Serge Vulliémoz
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria Isabel Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. François Lazeyras
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frédéric Grouiller.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants

All procedures performed in this study were in accordance with the ethical standards of the institutional and research committee and with the 1964 Declaration of Helsinki and its later amendments.

Informed consent

Informed consent was obtained from all participants in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Grouiller, F., Jorge, J., Pittau, F. et al. Presurgical brain mapping in epilepsy using simultaneous EEG and functional MRI at ultra-high field: feasibility and first results. Magn Reson Mater Phy 29, 605–616 (2016). https://doi.org/10.1007/s10334-016-0536-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10334-016-0536-5

Keywords

Search

Navigation