Abstract
Distributed inverse solutions aim to realistically reconstruct the origin of interictal epileptic discharges (IEDs) from noninvasively recorded electroencephalography (EEG) and magnetoencephalography (MEG) signals. Our aim was to compare the performance of different distributed inverse solutions in localizing IEDs: coherent maximum entropy on the mean (cMEM), hierarchical Bayesian implementations of independent identically distributed sources (IID, minimum norm prior) and spatially coherent sources (COH, spatial smoothness prior). Source maxima (i.e., the vertex with the maximum source amplitude) of IEDs in 14 EEG and 19 MEG studies from 15 patients with focal epilepsy were analyzed. We visually compared their concordance with intracranial EEG (iEEG) based on 17 cortical regions of interest and their spatial dispersion around source maxima. Magnetic source imaging (MSI) maxima from cMEM were most often confirmed by iEEG (cMEM: 14/19, COH: 9/19, IID: 8/19 studies). COH electric source imaging (ESI) maxima co-localized best with iEEG (cMEM: 8/14, COH: 11/14, IID: 10/14 studies). In addition, cMEM was less spatially spread than COH and IID for ESI and MSI (p < 0.001 Bonferroni-corrected post hoc t test). Highest positive predictive values for cortical regions with IEDs in iEEG could be obtained with cMEM for MSI and with COH for ESI. Additional realistic EEG/MEG simulations confirmed our findings. Accurate spatially extended sources, as found in cMEM (ESI and MSI) and COH (ESI) are desirable for source imaging of IEDs because this might influence surgical decision. Our simulations suggest that COH and IID overestimate the spatial extent of the generators compared to cMEM.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amblard C, Lapalme E, Lina JM (2004) Biomagnetic source detection by maximum entropy and graphical models. IEEE Trans Biomed Eng 51:427–442. doi:10.1109/TBME.2003.820999
Andrade-Valenca LP, Dubeau F, Mari F, Zelmann R, Gotman J (2011) Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology 77:524–531. doi:10.1212/WNL.0b013e318228bee2
Baillet S, Mosher JC, Leahy RM (2001) Electromagnetic brain mapping. IEEE Signal Processing Magazine 18:14–30. doi:10.1109/79.962275
Bast T et al (2004) EEG and MEG source analysis of single and averaged interictal spikes reveals intrinsic epileptogenicity in focal cortical dysplasia. Epilepsia 45:621–631
Becker H et al (2014) EEG extended source localization: tensor-based vs. conventional methods. Neuroimage 96:143–157. doi:10.1016/j.neuroimage.2014.03.043
Birot G, Albera L, Wendling F, Merlet I (2011) Localization of extended brain sources from EEG/MEG: the ExSo-MUSIC approach. Neuroimage 56:102–113. doi:10.1016/j.neuroimage.2011.01.054
Brodbeck V et al (2011) Electroencephalographic source imaging: a prospective study of 152 operated epileptic patients. Brain 134:2887–2897. doi:10.1093/brain/awr243
Chen F, Hallez H, Staelens S (2010) Influence of skull conductivity perturbations on EEG dipole source analysis. Med Phys 37:4475. doi:10.1118/1.3466831
Chowdhury R, Zerouali Y, Lina JM, Kobayashi E, Grova C (2012) Multimodal EEG/MEG fusion within the maximum entropy on the mean (MEM) framework. In: 18th international conference on biomagnetism, BIOMAG 2012, Paris
Chowdhury R et al (2014) Localization of the spatial extent of the generators of epileptic discharges in EEG and MEG: comparison between 4-ExSo-MUSIC and MEM approaches. In: 19th international conference on biomagnetism, BIOMAG 2014, Halifax, Canada
Chowdhury RA, Lina J-M, Kobayashi E, Grova C (2013) MEG source localization of spatially extended generators of epileptic activity: comparing entropic and hierarchical Bayesian approaches. PLoS One 8:e55969. doi:10.1371/journal.pone.0055969.s004
Dalal SS, Rampp S, Willomitzer F, Ettl S (2014) Consequences of EEG electrode position error on ultimate beamformer source reconstruction performance. Frontiers in neuroscience 8:42. doi:10.3389/fnins.2014.00042
de Gooijer-van de Groep KL, Leijten FSS, Ferrier CH, Huiskamp GJM (2013) Inverse modeling in magnetic source imaging: comparison of MUSIC, SAM(g2), and sLORETA to interictal intracranial EEG. Human Brain Mapping 34:2032–2044. doi:10.1002/hbm.22049
De Tiege X et al (2012) Clinical added value of magnetic source imaging in the presurgical evaluation of refractory focal epilepsy. Journal of Neurology, Neurosurgery & Psychiatry. doi:10.1136/jnnp-2011-301166
Friston KJ, Penny W, Phillips C, Kiebel S, Hinton G, Ashburner J (2002) Classical and Bayesian inference in neuroimaging: theory. Neuroimage 16:465–483. doi:10.1006/nimg.2002.1090
Friston KJ et al (2008) Multiple sparse priors for the M/EEG inverse problem. NeuroImage 39:1104–1120. doi:10.1016/j.neuroimage.2007.09.048
Genow A et al (2004) Epilepsy surgery, resection volume and MSI localization in lesional frontal lobe epilepsy. NeuroImage 21:444–449. doi:10.1016/j.neuroimage.2003.08.029
Goldenholz DM, Ahlfors SP, Hämäläinen MS, Sharon D, Ishitobi M, Vaina LM, Stufflebeam SM (2009) Mapping the signal-to-noise-ratios of cortical sources in magnetoencephalography and electroencephalography. Hum Brain Mapp 30:1077–1086. doi:10.1002/hbm.20571
Goncalves SI, de Munck JC, Verbunt JPA, Bijma F, Heethaar RM, Lopes da Silva F (2003) In vivo measurement of the brain and skull resistivities using an eit-based method and realistic models for the head. IEEE Trans Bio-med Eng 50:754–767. doi:10.1109/TBME.2003.812164
Gramfort A, Papadopoulo T, Olivi E, Clerc M (2010) OpenMEEG: opensource software for quasistatic bioelectromagnetics. Biomedical engineering online 9:45. doi:10.1186/1475-925X-9-45
Grova C, Daunizeau J, Lina JM, Benar CG, Benali H, Gotman J (2006) Evaluation of EEG localization methods using realistic simulations of interictal spikes. Neuroimage 29:734–753. doi:10.1016/j.neuroimage.2005.08.053
Grova C et al (2013) Evaluation of the spatial extent of the sources of epileptic spikes in MEG. In: International conference on basic and clinical multimodal imaging (BACI), Geneva, 5–8 Sept 2013
Hämäläinen MS (1992) Magnetoencephalography: a tool for functional brain imaging. Brain Topogr 5:95–102
Hämäläinen MS, Ilmoniemi RJ (1994) Interpreting magnetic fields of the brain: minimum norm estimates. Med Biol Eng Compu 32:35–42
Heers M, Hedrich T, An D, Dubeau F, Gotman J, Grova C, Kobayashi E (2014) Spatial correlation of hemodynamic changes related to interictal epileptic discharges with electric and magnetic source imaging. Hum Brain Mapp 35:4396–4414. doi:10.1002/hbm.22482
Hillebrand A, Barnes GR (2011) Practical constraints on estimation of source extent with MEG beamformers. Neuroimage 54:2732–2740. doi:10.1016/j.neuroimage.2010.10.036
Iwasaki M, Pestana E, Burgess RC, Lüders HO, Shamoto H, Nakasato N (2005) Detection of epileptiform activity by human interpreters: blinded comparison between electroencephalography and magnetoencephalography. Epilepsia 46:59–68. doi:10.1111/j.0013-9580.2005.21104.x
Jung J et al (2013) The value of magnetoencephalography for seizure-onset zone localization in magnetic resonance imaging-negative partial epilepsy. Brain 136:3176–3186. doi:10.1093/brain/awt213
Knowlton RC et al (2008) Functional imaging: II. Prediction of epilepsy surgery outcome Annals of Neurology 64:35–41
Kobayashi K, Yoshinaga H, Ohtsuka Y, Gotman J (2005) Dipole modeling of epileptic spikes can be accurate or misleading. Epilepsia 46:397–408. doi:10.1111/j.0013-9580.2005.31404.x
Lantz G, Grave de Peralta R, Spinelli L, Seeck M, Michel CM (2003) Epileptic source localization with high density EEG: how many electrodes are needed? Clin Neurophysiol 114:63–69
Lapalme E, Lina JM, Mattout J (2006) Data-driven parceling and entropic inference in MEG. Neuroimage 30:160–171. doi:10.1016/j.neuroimage.2005.08.067
Lina JM, Chowdhury R, Lemay E, Kobayashi E, Grova C (2014) Wavelet-based localization of oscillatory sources from magnetoencephalography data. IEEE Trans Biomed Eng 61:2350–2364. doi:10.1109/TBME.2012.2189883
Lu Y, Yang L, Worrell GA, Brinkmann B, Nelson C, He B (2012) Dynamic imaging of seizure activity in pediatric epilepsy patients. Clin Neurophysiol 123:2122–2129. doi:10.1016/j.clinph.2012.04.021
Mamelak AN, Lopez N, Akhtari M, Sutherling WW (2002) Magnetoencephalography-directed surgery in patients with neocortical epilepsy. J Neurosurg 97:865–873. doi:10.3171/jns.2002.97.4.0865
Mangin J-F, Frouin V, Bloch I, Régis J, López-Krahe J (1995) From 3D magnetic resonance images to structural representations of the cortex topography using topology preserving deformations. Journal of Mathematical Imaging and Vision 5:297–318. doi:10.1007/BF01250286
Mattout J, Pelegrini-Issac M, Garnero L, Benali H (2005) Multivariate source prelocalization (MSP): use of functionally informed basis functions for better conditioning the MEG inverse problem. Neuroimage 26:356–373. doi:10.1016/j.neuroimage.2005.01.026
Megevand P et al (2014) Electric source imaging of interictal activity accurately localises the seizure onset zone. J Neurol Neurosurg Psychiatry 85:38–43. doi:10.1136/jnnp-2013-305515
Mikuni N et al (1997) Simultaneous recording of epileptiform discharges by MEG and subdural electrodes in temporal lobe epilepsy. NeuroImage 5:298–306. doi:10.1006/nimg.1997.0272
Molins A, Stufflebeam SM, Brown EN, Hamalainen MS (2008) Quantification of the benefit from integrating MEG and EEG data in minimum l2-norm estimation. Neuroimage 42:1069–1077. doi:10.1016/j.neuroimage.2008.05.064
Oishi M, Otsubo H, Kameyama S, Morota N, Masuda H, Kitayama M, Tanaka R (2002) Epileptic spikes: magnetoencephalography versus simultaneous electrocorticography. Epilepsia 43:1390–1395
Pascual-Marqui RD, Michel CM, Lehmann D (1994) Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. Int J Psychophysiol 18:49–65
Rikir E et al (2014) Electrical source imaging in cortical malformation-related epilepsy: a prospective EEG-SEEG concordance study. Epilepsia 55:918–932. doi:10.1111/epi.12591
Sohrabpour A, Lu Y, Kankirawatana P, Blount J, Kim H, He B (2014) Effect of EEG electrode number on epileptic source localization in pediatric patients. Clin Neurophysiol. doi:10.1016/j.clinph.2014.05.038
Steinstrater O, Sillekens S, Junghoefer M, Burger M, Wolters CH (2010) Sensitivity of beamformer source analysis to deficiencies in forward modeling. Hum Brain Mapp 31:1907–1927. doi:10.1002/hbm.20986
Sutherling WW, Mamelak AN, Thyerlei D, Maleeva T, Minazad Y, Philpott L, Lopez N (2008) Influence of magnetic source imaging for planning intracranial EEG in epilepsy. Neurology 71:990–996. doi:10.1212/01.wnl.0000326591.29858.1a
Tadel F, Baillet S, Mosher JC, Pantazis D, Leahy RM (2011) Brainstorm: a user-friendly application for MEG/EEG analysis. Comput Intell Neurosci 2011:879716. doi:10.1155/2011/879716
Tao JX, Ray A, Hawes-Ebersole S, Ebersole JS (2005) Intracranial EEG substrates of scalp EEG interictal spikes. Epilepsia 46:669–676. doi:10.1111/j.1528-1167.2005.11404.x
von Ellenrieder N, Beltrachini L, Muravchik CH, Gotman J (2014a) Extent of cortical generators visible on the scalp: effect of a subdural grid. Neuroimage. doi:10.1016/j.neuroimage.2014.08.009
von Ellenrieder N, Beltrachini L, Perucca P, Gotman J (2014b) Size of cortical generators of epileptic interictal events and visibility on scalp EEG. Neuroimage 94:47–54. doi:10.1016/j.neuroimage.2014.02.032
Wang G, Worrell G, Yang L, Wilke C, He B (2011) Interictal spike analysis of high-density EEG in patients with partial epilepsy. Clin Neurophysiol 122:1098–1105. doi:10.1016/j.clinph.2010.10.043
Wennberg R, Cheyne D (2014a) EEG source imaging of anterior temporal lobe spikes: validity and reliability. Clin Neurophysiol 125:886–902. doi:10.1016/j.clinph.2013.09.042
Wennberg R, Cheyne D (2014b) Reliability of MEG source imaging of anterior temporal spikes: analysis of an intracranially characterized spike focus. Clin Neurophysiol 125:903–918. doi:10.1016/j.clinph.2013.08.032
Yang L, Wilke C, Brinkmann B, Worrell GA, He B (2011) Dynamic imaging of ictal oscillations using non-invasive high-resolution EEG. Neuroimage 56:1908–1917. doi:10.1016/j.neuroimage.2011.03.043
Zelmann R, Lina JM, Schulze-Bonhage A, Gotman J, Jacobs J (2013) Scalp EEG is not a blur: it can see high frequency oscillations although their generators are small. Brain Topogr. doi:10.1007/s10548-013-0321-y
Zhu M, Zhang W, Dickens DL, King JA, Ding L (2013) Sparse MEG source imaging for reconstructing dynamic sources of interictal spikes in partial epilepsy. J Clin Neurophysiol 30:313–328. doi:10.1097/WNP.0b013e31829dda27
Zhu M, Zhang W, Dickens DL, Ding L (2014) Reconstructing spatially extended brain sources via enforcing multiple transform sparseness. Neuroimage 86:280–293. doi:10.1016/j.neuroimage.2013.09.070
Acknowledgments
The authors thank Ms. Manon Robert for her excellent assistance in EEG/MEG data acquisition. This project was supported by the CIHR (MOP-93614), Fonds de la recherche en santé du Quebec, Centres of Excellence for Commercialization and Research (CECR), American Epilepsy Society Early Career Physicians-Scientist Award and by the Savoy-Foundation. MH currently receives funding from the BrainLinks-BrainTools Cluster of Excellence funded by the German Research Foundation (DFG, grant number EXC 1086), which has not however supported any data acquisition or analysis related to the study.
Conflict of interest
None of the authors states any conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Heers, M., Chowdhury, R.A., Hedrich, T. et al. Localization Accuracy of Distributed Inverse Solutions for Electric and Magnetic Source Imaging of Interictal Epileptic Discharges in Patients with Focal Epilepsy. Brain Topogr 29, 162–181 (2016). https://doi.org/10.1007/s10548-014-0423-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-014-0423-1