Abstract
Background
Electroencephalography (EEG) and magnetoencephalography (MEG) are neurophysiological methods used to investigate noninvasively the spatial, temporal, and spectral dynamics of human brain functions.
Objectives
This article reviews data on the use of EEG and MEG for presurgical functional brain mapping in patients with refractory focal epilepsy. The focus is on the localization of the primary sensorimotor (SM1) cortex as well as the verbal language and episodic memory functions.
Material and methods
The English literature was reviewed based on a PubMed search. Relevant references in the selected papers were also included.
Results
Presurgical MEG functional localization of the SM1 cortex generally overlaps with intracranial mapping. MEG allows for determination of hemispheric verbal (receptive and expressive) language dominance in neurosurgical patients with a high degree of concordance with the intracarotid amobarbital test. MEG represents an interesting technique for assessing postoperative memory outcome in patients with mesial temporal lobe epilepsy. Very few studies have evaluated the yield of EEG in these three clinical indications. High-density EEG might be a promising technique that needs further validation.
Conclusion
MEG is a validated and robust technique for noninvasive functional mapping of the SM1 cortex and verbal language hemispheric dominance in patients with refractory focal epilepsy. Current data also suggest that MEG is a promising technique for assessing the hemispheric dominance of memory function. Further studies are needed to assess the clinical added value of high-density EEG in these clinical indications.
Zusammenfassung
Hintergrund
Elektroenzephalographie (EEG) und Magnetenzephalographie (MEG) sind neurophysiologische Methoden, die für die nichtinvasive Untersuchung der räumlichen, zeitlichen und spektralen Dynamik der menschlichen Hirnfunktion eingesetzt werden.
Zielsetzung
Der vorgestellte Artikel bietet einen Überblick über die Anwendung von EEG und MEG für das prächirurgische funktionelle Mapping bei Patienten mit refraktärer fokaler Epilepsie. Der Fokus liegt auf der Lokalisation des primären sensomotorischen Kortex (SM1) sowie der verbalen Sprach- und episodischen Gedächtnisfunktion.
Material und Methoden
Auf einer PubMed-Suche basierend wurden entsprechende Artikel in englischer Sprache ausgewertet. Darüber hinaus wurden relevante Zitate in den ausgewählten Artikeln in die Auswertung einbezogen.
Ergebnisse
Die prächirurgische funktionelle Lokalisation des SM1-Kortex mittels MEG überlappt i. Allg. mit den Ergebnissen des intrakraniellen Mappings. Die MEG ermöglicht die Bestimmung der hemisphärischen (rezeptiven und expressiven) Sprachdominanz neurochirurgischer Patienten mit einem hohen Grad an Konkordanz mit dem Intrakarotis-Amobarbital-Test (Wada-Test). MEG-Untersuchungen sind auch für die Evaluation der postoperativen Gedächtnisfunktion bei Patienten mit mesialer Temporallappenepilepsie interessant. In sehr wenigen Studien wurde bisher der Nutzen des EEG im Rahmen dieser 3 Indikationen untersucht. Die High-Density-EEG stellt eine vielversprechende Technik dar, die jedoch weitere Validierung benötigt.
Schlussfolgerungen
Die MEG ist eine validierte und robuste Technik für die nichtinvasive funktionelle Lokalisation des SM1-Kortex sowie der verbalen hemisphärischen Sprachdominanz bei Patienten mit refraktären fokalen Epilepsien. Die Studienlage weist zudem darauf hin, dass die MEG eine vielversprechende Technik zur Bestimmung der hemisphärischen Gedächtnisdominanz darstellen könnte. Weitere Untersuchungen zum zusätzlichen Nutzen der High-Density-EEG im Rahmen dieser Indikationen sind erforderlich.
Similar content being viewed by others
References
Alessio A, Pereira FR, Sercheli MS et al (2013) Brain plasticity for verbal and visual memories in patients with mesial temporal lobe epilepsy and hippocampal sclerosis: an fMRI study. Hum Brain Mapp 34:186–199
Bagic AI (2011) Disparities in clinical magnetoencephalography practice in the United States: a survey-based appraisal. J Clin Neurophysiol 28:341–347
Bagic AI, Bowyer SM, Kirsch HE et al (2017) American Clinical MEG Society (ACMEGS) Position Statement #2: The Value of Magnetoencephalography (MEG)/Magnetic Source Imaging (MSI) in Noninvasive Presurgical Mapping of Eloquent Cortices of Patients Preparing for Surgical Interventions. J Clin Neurophysiol. https://doi.org/10.1097/WNP.0000000000000366
Bartsch AJ, Homola G, Biller A et al (2006) Diagnostic functional MRI: illustrated clinical applications and decision-making. J Magn Reson Imaging 23:921–932
Bast T, Wright T, Boor R et al (2007) Combined EEG and MEG analysis of early somatosensory evoked activity in children and adolescents with focal epilepsies. Clin Neurophysiol 118:1721–1735
Baxendale S, Thompson PJ, Duncan JS (2008) The role of the Wada test in the surgical treatment of temporal lobe epilepsy: an international survey. Epilepsia 49:715–720 (discussion 720–715)
Beisteiner R, Erdler M, Teichtmeister C et al (1997) Magnetoencephalography may help to improve functional MRI brain mapping. Eur J Neurosci 9:1072–1077
Beisteiner R, Gomiscek G, Erdler M et al (1995) Comparing localization of conventional functional magnetic resonance imaging and magnetoencephalography. Eur J Neurosci 7:1121–1124
Bonelli SB, Powell RH, Yogarajah M et al (2010) Imaging memory in temporal lobe epilepsy: predicting the effects of temporal lobe resection. Brain 133:1186–1199
Boto E, Meyer SS, Shah V et al (2017) A new generation of magnetoencephalography: room temperature measurements using optically-pumped magnetometers. Neuroimage 149:404–414
Bourguignon M, De Tiège X, Op de Beeck M et al (2011) Functional motor-cortex mapping using corticokinematic coherence. Neuroimage 55:1475–1479
Bourguignon M, Jousmäki V, Marty B et al (2013) Comprehensive functional mapping scheme for non-invasive primary sensorimotor cortex mapping. Brain Topogr 26:511–523
Bowyer SM, Moran JE, Weiland BJ et al (2005) Language laterality determined by MEG mapping with MR-FOCUSS. Epilepsy Behav 6:235–241
Breier JI, Simos PG, Wheless JW et al (2001) Language dominance in children as determined by magnetic source imaging and the intracarotid amobarbital procedure: a comparison. J Child Neurol 16:124–130
Breier JI, Simos PG, Zouridakis G et al (1999) Language dominance determined by magnetic source imaging: a comparison with the Wada procedure. Neurology 53:938–945
Burgess RC, Funke ME, Bowyer SM et al (2011) American Clinical Magnetoencephalography Society Clinical Practice Guideline 2: presurgical functional brain mapping using magnetic evoked fields. J Clin Neurophysiol 28:355–361
Cheyne D, Bostan AC, Gaetz W et al (2007) Event-related beamforming: a robust method for presurgical functional mapping using MEG. Clin Neurophysiol 118:1691–1704
Chou N, Serafini S, Muh CR (2018) Cortical language areas and plasticity in pediatric patients with epilepsy: a review. Pediatr Neurol 78:3–12
Collinge S, Prendergast G, Mayers ST et al (2017) Pre-surgical mapping of eloquent cortex for paediatric epilepsy surgery candidates: evidence from a review of advanced functional neuroimaging. Seizure 52:136–146
D’esposito M, Deouell LY, Gazzaley A (2003) Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat Rev Neurosci 4:863–872
De Ribaupierre S, Wang A, Hayman-Abello S (2012) Language mapping in temporal lobe epilepsy in children: special considerations. Epilepsy Res Treat 2012:837036
De Tiège X, Connelly A, Liegeois F et al (2009) Influence of motor functional magnetic resonance imaging on the surgical management of children and adolescents with symptomatic focal epilepsy. Neurosurgery 64:856–864 (discussion 864)
De Tiège X, Lundqvist D, Beniczky S et al (2017) Current clinical magnetoencephalography practice across europe: are we closer to use MEG as an established clinical tool? Seizure 50:53–59
Doss RC, Zhang W, Risse GL et al (2009) Lateralizing language with magnetic source imaging: validation based on the Wada test. Epilepsia 50:2242–2248
Duncan JS, Winston GP, Koepp MJ et al (2016) Brain imaging in the assessment for epilepsy surgery. Lancet Neurol 15:420–433
Findlay AM, Ambrose JB, Cahn-Weiner DA et al (2012) Dynamics of hemispheric dominance for language assessed by magnetoencephalographic imaging. Ann Neurol 71:668–686
Fisher AE, Furlong PL, Seri S et al (2008) Interhemispheric differences of spectral power in expressive language: a MEG study with clinical applications. Int J Psychophysiol 68:111–122
Forster MT, Hattingen E, Senft C et al (2011) Navigated transcranial magnetic stimulation and functional magnetic resonance imaging: advanced adjuncts in preoperative planning for central region tumors. Neurosurgery 68:1317–1324 (discussion 1324–1315)
Gaetz W, Cheyne D, Rutka JT et al (2009) Presurgical localization of primary motor cortex in pediatric patients with brain lesions by the use of spatially filtered magnetoencephalography. Neurosurgery 64:177–185 (discussion ons186)
Gleissner U, Helmstaedter C, Schramm J et al (2004) Memory outcome after selective amygdalohippocampectomy in patients with temporal lobe epilepsy: one-year follow-up. Epilepsia 45:960–962
Gleissner U, Helmstaedter C, Schramm J et al (2002) Memory outcome after selective amygdalohippocampectomy: a study in 140 patients with temporal lobe epilepsy. Epilepsia 43:87–95
Goldenholz DM, Ahlfors SP, Hamalainen MS et al (2009) Mapping the signal-to-noise-ratios of cortical sources in magnetoencephalography and electroencephalography. Hum Brain Mapp 30:1077–1086
Hämäläinen M, Hari R, Ilmoniemi RJ et al (1993) Magnetoencephalography: theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev Mod Phys 65:413–497
Hamberger MJ, Cole J (2011) Language organization and reorganization in epilepsy. Neuropsychol Rev 21:240–251
Helmstaedter C, Kurthen M, Lux S et al (2003) Chronic epilepsy and cognition: a longitudinal study in temporal lobe epilepsy. Ann Neurol 54:425–432
Hirata M, Kato A, Taniguchi M et al (2004) Determination of language dominance with synthetic aperture magnetometry: comparison with the Wada test. Neuroimage 23:46–53
Inoue T, Shimizu H, Nakasato N et al (1999) Accuracy and limitation of functional magnetic resonance imaging for identification of the central sulcus: comparison with magnetoencephalography in patients with brain tumors. Neuroimage 10:738–748
Kamada K, Houkin K, Takeuchi F et al (2003) Visualization of the eloquent motor system by integration of MEG, functional, and anisotropic diffusion-weighted MRI in functional neuronavigation. Surg Neurol 59:352–361 (discussion 361–352)
Kamada K, Sawamura Y, Takeuchi F et al (2007) Expressive and receptive language areas determined by a non-invasive reliable method using functional magnetic resonance imaging and magnetoencephalography. Neurosurgery 60:296–305 (discussion 305–296)
Klamer S, Elshahabi A, Lerche H et al (2015) Differences between MEG and high-density EEG source localizations using a distributed source model in comparison to fMRI. Brain Topogr 28:87–94
Kober H, Moller M, Nimsky C et al (2001) New approach to localize speech relevant brain areas and hemispheric dominance using spatially filtered magnetoencephalography. Hum Brain Mapp 14:236–250
Kober H, Nimsky C, Moller M et al (2001) Correlation of sensorimotor activation with functional magnetic resonance imaging and magnetoencephalography in presurgical functional imaging: a spatial analysis. Neuroimage 14:1214–1228
Korvenoja A, Kirveskari E, Aronen HJ et al (2006) Sensorimotor cortex localization: comparison of magnetoencephalography, functional MR imaging, and intraoperative cortical mapping. Radiology 241:213–222
Krieg SM, Shiban E, Droese D et al (2012) Predictive value and safety of intraoperative neurophysiological monitoring with motor evoked potentials in glioma surgery. Neurosurgery 70:1060–1070 (discussion 1070–1061)
Lascano AM, Grouiller F, Genetti M et al (2014) Surgically relevant localization of the central sulcus with high-density somatosensory-evoked potentials compared with functional magnetic resonance imaging. Neurosurgery 74:517–526
Liegeois F, Cross JH, Gadian DG et al (2006) Role of fMRI in the decision-making process: epilepsy surgery for children. J Magn Reson Imaging 23:933–940
Lin PT, Berger MS, Nagarajan SS (2006) Motor field sensitivity for preoperative localization of motor cortex. J Neurosurg 105:588–594
Liu AK, Dale AM, Belliveau JW (2002) Monte Carlo simulation studies of EEG and MEG localization accuracy. Hum Brain Mapp 16:47–62
Maestu F, Campo P, Garcia-Morales I et al (2009) Biomagnetic profiles of verbal memory success in patients with mesial temporal lobe epilepsy. Epilepsy Behav 16:527–533
Makela JP (2014) Bioelectric measurements: magnetoencephalography. In: Brahme A (ed) Comprehensive biomedical physics. Elsevier, Amsterdam, pp 47–72
Makela JP, Forss N, Jaaskelainen J et al (2006) Magnetoencephalography in neurosurgery. Neurosurgery 59:493–510 (discussion 510–491)
Makela JP, Kirveskari E, Seppa M et al (2001) Three-dimensional integration of brain anatomy and function to facilitate intraoperative navigation around the sensorimotor strip. Hum Brain Mapp 12:180–192
Morioka T, Mizushima A, Yamamoto T et al (1995) Functional mapping of the sensorimotor cortex: combined use of magnetoencephalography, functional MRI, and motor evoked potentials. Neuroradiology 37:526–530
Morioka T, Yamamoto T, Mizushima A et al (1995) Comparison of magnetoencephalography, functional MRI, and motor evoked potentials in the localization of the sensory-motor cortex. Neurol Res 17:361–367
Nagarajan S, Kirsch H, Lin P et al (2008) Preoperative localization of hand motor cortex by adaptive spatial filtering of magnetoencephalography data. J Neurosurg 109:228–237
Paiva WS, Fonoff ET, Marcolin MA et al (2012) Cortical mapping with navigated transcranial magnetic stimulation in low-grade glioma surgery. Neuropsychiatr Dis Treat 8:197–201
Papanicolaou AC, Rezaie R, Narayana S et al (2017) On the relative merits of invasive and non-invasive pre-surgical brain mapping: New tools in ablative epilepsy surgery. Epilepsy Res. https://doi.org/10.1016/j.eplepsyres.2017.07.002
Papanicolaou AC, Rezaie R, Narayana S et al (2014) Is it time to replace the Wada test and put awake craniotomy to sleep? Epilepsia 55:629–632
Papanicolaou AC, Simos PG, Breier JI et al (1999) Magnetoencephalographic mapping of the language-specific cortex. J Neurosurg 90:85–93
Papanicolaou AC, Simos PG, Castillo EM et al (2004) Magnetocephalography: a noninvasive alternative to the Wada procedure. J Neurosurg 100:867–876
Perrine K, Gershengorn J, Brown ER et al (1993) Material-specific memory in the intracarotid amobarbital procedure. Neurology 43:706–711
Picht T, Schmidt S, Brandt S et al (2011) Preoperative functional mapping for rolandic brain tumor surgery: comparison of navigated transcranial magnetic stimulation to direct cortical stimulation. Neurosurgery 69:581–588 (discussion 588)
Picht T, Schmidt S, Woitzik J et al (2011) Navigated brain stimulation for preoperative cortical mapping in paretic patients: case report of a hemiplegic patient. Neurosurgery 68:E1475–E1480 (discussion E1480)
Pirmoradi M, Beland R, Nguyen DK et al (2010) Language tasks used for the presurgical assessment of epileptic patients with MEG. Epileptic Disord 12:97–108
Powell GE, Polkey CE, Canavan AG (1987) Lateralisation of memory functions in epileptic patients by use of the sodium amytal (Wada) technique. J Neurol Neurosurg Psychiatr 50:665–672
Powell HW, Richardson MP, Symms MR et al (2007) Reorganization of verbal and nonverbal memory in temporal lobe epilepsy due to unilateral hippocampal sclerosis. Epilepsia 48:1512–1525
Puce A, Hamalainen MS (2017) A review of issues related to data acquisition and analysis in EEG/MEG studies. Brain Sci 7:E58. https://doi.org/10.3390/brainsci7060058
Quigg M (2015) Taking sides: physician’s perceptions on the use of the Wada test in epilepsy surgery-Q-PULSE survey commentary. Epilepsy Curr 15:225
Rausch R, Babb TL, Engel J Jr. et al (1989) Memory following intracarotid amobarbital injection contralateral to hippocampal damage. Arch Neurol 46:783–788
Rezaie R, Narayana S, Schiller K et al (2014) Assessment of hemispheric dominance for receptive language in pediatric patients under sedation using magnetoencephalography. Front Hum Neurosci 8:657
Riggs L, Moses SN, Bardouille T et al (2009) A complementary analytic approach to examining medial temporal lobe sources using magnetoencephalography. Neuroimage 45:627–642
Roberts TP, Rowley HA (1997) Mapping of the sensorimotor cortex: functional MR and magnetic source imaging. AJNR Am J Neuroradiol 18:871–880
Rosenow F, Luders H (2001) Presurgical evaluation of epilepsy. Brain 124:1683–1700
Rouleau I, Robidoux J, Labrecque R et al (1997) Effect of focus lateralization on memory assessment during the intracarotid amobarbital procedure. Brain Cogn 33:224–241
Salmelin R (2007) Clinical neurophysiology of language: the MEG approach. Clin Neurophysiol 118:237–254
Schiffbauer H, Berger MS, Ferrari P et al (2002) Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. J Neurosurg 97:1333–1342
Schwartz TH (2007) Neurovascular coupling and epilepsy: hemodynamic markers for localizing and predicting seizure onset. Epilepsy Curr 7:91–94
Seghier ML, Patel E, Prejawa S et al (2016) The PLORAS database: a data repository for predicting language outcome and recovery after stroke. Neuroimage 124:1208–1212
Shimizu H, Nakasato N, Mizoi K et al (1997) Localizing the central sulcus by functional magnetic resonance imaging and magnetoencephalography. Clin Neurol Neurosurg 99:235–238
Sidhu MK, Stretton J, Winston GP et al (2013) A functional magnetic resonance imaging study mapping the episodic memory encoding network in temporal lobe epilepsy. Brain 136:1868–1888
Simos PG, Papanicolaou AC, Breier JI et al (1999) Localization of language-specific cortex by using magnetic source imaging and electrical stimulation mapping. J Neurosurg 91:787–796
Solomon J, Boe S, Bardouille T (2015) Reliability for non-invasive somatosensory cortex localization: Implications for pre-surgical mapping. Clin Neurol Neurosurg 139:224–229
Stufflebeam SM, Tanaka N, Ahlfors SP (2009) Clinical applications of magnetoencephalography. Hum Brain Mapp 30:1813–1823
Sutherling WW, Crandall PH, Darcey TM et al (1988) The magnetic and electric fields agree with intracranial localizations of somatosensory cortex. Neurology 38:1705–1714
Towle VL, Khorasani L, Uftring S et al (2003) Noninvasive identification of human central sulcus: a comparison of gyral morphology, functional MRI, dipole localization, and direct cortical mapping. Neuroimage 19:684–697
Trimmel K, Sachsenweger J, Lindinger G et al (2017) Lateralization of language function in epilepsy patients: a high-density scalp-derived event-related potentials (ERP) study. Clin Neurophysiol 128:472–479
Trotta N, Goldman S, Legros B et al (2011) Metabolic evidence for episodic memory plasticity in the nonepileptic temporal lobe of patients with mesial temporal epilepsy. Epilepsia 52:2003–2012
Van Poppel M, Wheless JW, Clarke DF et al (2012) Passive language mapping with magnetoencephalography in pediatric patients with epilepsy. J Neurosurg Pediatr 10:96–102
Ver Hoef LW, Sawrie S, Killen J et al (2008) Left mesial temporal sclerosis and verbal memory: a magnetoencephalography study. J Clin Neurophysiol 25:1–6
Vitikainen AM, Lioumis P, Paetau R et al (2009) Combined use of non-invasive techniques for improved functional localization for a selected group of epilepsy surgery candidates. Neuroimage 45:342–348
Wada J, Rasmussen T (1960) Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance. J Neurosurg 17:266–282
Willemse RB, De Munck JC, Van’t Ent D et al (2007) Magnetoencephalographic study of posterior tibial nerve stimulation in patients with intracranial lesions around the central sulcus. Neurosurgery 61:1209–1217 (discussion 1217–1208)
Willemse RB, De Munck JC, Verbunt JP et al (2010) Topographical organization of mu and Beta band activity associated with hand and foot movements in patients with perirolandic lesions. Open Neuroimag J 4:93–99
Willemse RB, Hillebrand A, Ronner HE et al (2016) Magnetoencephalographic study of hand and foot sensorimotor organization in 325 consecutive patients evaluated for tumor or epilepsy surgery. Neuroimage Clin 10:46–53
Wyllie E, Naugle R, Chelune G et al (1991) Intracarotid amobarbital procedure: II. Lateralizing value in evaluation for temporal lobectomy. Epilepsia 32:865–869
Yousry TA, Schmid UD, Alkadhi H et al (1997) Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120(Pt 1):141–157
Funding
T. Coolen is a Clinical Master Specialist Applicant to a PhD at the Fonds de la Recherche Scientifique (FRS-FNRS, Brussels, Belgium). A.M. Dumitrescu benefits from financial support of the Fonds Erasme (Research Convention “Les Voies du Savoir”, Brussels, Belgium). M. Bourguignon is supported by the program Attract of Innoviris (grant 2015-BB2B-10), by the Spanish Ministry of Economy and Competitiveness (grant PSI2016-77175-P), and by the Marie Skłodowska-Curie Action of the European Commission (grant 743562). X. De Tiège is Postdoctorate Clinical Master Specialist at the FRS-FNRS. The MEG project at the CUB Hôpital Erasme is financially supported by the Fonds Erasme (Research Convention “Les Voies du Savoir”).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
X. De Tiège is a consultant for Elekta MEGIN. T. Coolen, A.M. Dumitrescu, M. Bourguignon, V. Wens and C. Urbain declare that they have no competing interests.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.
Additional information
T. Coolen and A.M. Dumitrescu contributed equally to this work.
Rights and permissions
About this article
Cite this article
Coolen, T., Dumitrescu, A.M., Bourguignon, M. et al. Presurgical electromagnetic functional brain mapping in refractory focal epilepsy. Z. Epileptol. 31, 203–212 (2018). https://doi.org/10.1007/s10309-018-0189-7
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10309-018-0189-7