Simultaneous EEG-fMRI has proven to be useful in localizing interictal epileptic activity. However, the applicability of traditional GLM-based analysis is limited as interictal spikes are often not seen on the EEG inside the scanner. Therefore, we aim at extracting epileptic activity purely from the fMRI time series using independent component analysis (ICA). To our knowledge, we show for the first time that ICA can find sources related to epileptic activity in patients where no interictal spikes were recorded in the EEG. The epileptic components were identified retrospectively based on the known localization of the ictal onset zone (IOZ). We demonstrate that the selected components truly correspond to epileptic activity, as sources extracted from patients resemble significantly better the IOZ than sources found in healthy controls. Furthermore, we show that the epileptic components in patients with and without spikes recorded inside the scanner resemble the IOZ in the same degree. We conclude that ICA of fMRI has the potential to extend the applicability of EEG-fMRI for presurgical evaluation in epilepsy.
References
[1]
Debener S, Ullsperger M, Siegel M, Engel A (2006) Single–trial eeg–fmri reveals the dynamics of cognitive function. Trends in Cognitive Sciences 10: 558–563.
[2]
Mijovi？ B, Vanderperren K, Novitskiy N, Vanrumste B, Stiers P, et al. (2012) The “why” and “how” of jointica: Results from a visual detection task. NeuroImage 60: 1171–1185.
[3]
Thornton R, Rodionov R, Laufs H, Vulliemoz S, Vaudano A, et al. (2010) Imaging haemodynamic changes related to seizures: Comparison of eeg–based general linear model, independent component analysis of fmri and intracranial eeg. NeuroImage 53: 196–205.
[4]
Gotman J, Kobayashi E, Bagshaw AP, Bénar CG, Dubeau F (2006) Combining eeg and fmri: A multimodal tool for epilepsy research. Journal of Magnetic Resonance Imaging 23: 906–920.
[5]
Salek-Haddadi A, Diehl B, Hamandi K, Merschhemke M, Liston A, et al. (2006) Hemodynamic correlates of epileptiform discharges: An eeg–fmri study of 63 patients with focal epilepsy. Brain Research 1088: 148–166.
[6]
Zijlmans M, Huiskamp G, Hersevoort M, Seppenwoolde JH, van Huffelen AC, et al. (2007) Eeg–fmri in the preoperative work–up for epilepsy surgery. Brain 130: 2343–2353.
[7]
Cooper R, Winter A, Crow H, Walter W (1965) Comparison of subcortical, cortical and scalp activity using chronically indwelling electrodes in man. Electroencephalography and Clinical Neurophysiology 18: 217–228.
[8]
Marks DA, Katz A, Booke J, Spencer DD, Spencer SS (1992) Comparison and correlation of surface and sphenoidal electrodes with simultaneous intracranial recording: an interictal study. Electroencephalography and Clinical Neurophysiology 82: 23–29.
[9]
Tao JX, Ray A, Hawes-Ebersole S, Ebersole JS (2005) Intracranial eeg substrates of scalp eeg interictal spikes. Epilepsia 46: 669–676.
[10]
Bénar CG, Aghakhani Y, Wang Y, Izenberg A, Al-Asmi A, et al. (2003) Quality of eeg in simultaneous eeg-fmri for epilepsy. Clinical Neurophysiology 114: 569–580.
[11]
Grouiller F, Vercueil L, Krainik A, Segebarth C, Kahane P, et al. (2007) A comparative study of different artefact removal algorithms for eeg signals acquired during functional mri. NeuroImage 38: 124–137.
[12]
Vanderperren K, De Vos M, Ramautar J, Novitskiy N, Mennes M, et al. (2010) Removal of bcg artifacts from eeg recordings inside the mr scanner: A comparison of methodological and validation–related aspects. NeuroImage 50: 920–934.
[13]
Tousseyn S, Dupont P, Sunaert S, Van Paesschen W (2012) Evaluation of interictal eeg–fmri sensitivity and specificity for detection of the ictal onset zone in refractory focal epilepsy. In: American Epilepsy Society Annual Meeting, Abstract No.1.196. www.aesnet.org.
[14]
Grouiller F, Thornton RC, Groening K, Spinelli L, Duncan JS, et al. (2011) With or without spikes: localization of focal epileptic activity by simultaneous electroencephalography and functional magnetic resonance imaging. Brain 134: 2867–2886.
[15]
Mckeown M, Makeig S, Brown G, Jung T, Kindermann S, et al. (1998) Analysis of fmri data by blind separation into independent spatial components. Human Brain Mapping 6: 160–188.
[16]
van de Ven V, Formisano E, Prvulovic D, Roeder C, Linden D (2004) Functional connectivity as revealed by spatial independent component analysis of fmri measurements during rest. Human Brain Mapping 22: 165–178.
[17]
Calhoun V, Pekar J, McGinty V, Adali T, Watson T, et al. (2002) Different activation dynamics in multiple neural systems during simulated driving. Human Brain Mapping 16: 158–167.
[18]
Duann JR, Jung TP, Kuo WJ, Yeh TC, Makeig S, et al. (2002) Single–trial variability in event–related bold signals. NeuroImage 15: 823–835.
[19]
De Martino F, Gentile F, Esposito F, Balsi M, Di Salle F, et al. (2007) Classification of fmri independent components using ic–fingerprints and support vector machine classifiers. NeuroImage 34: 177–194.
[20]
Leite M, Leal A, Figueiredo P (2013) Transfer function between eeg and bold signals of epileptic activity. Frontiers in Neurology 4.
[21]
LeVan P, Tyvaert L, Moeller F, Gotman J (2010) Independent component analysis reveals dynamic ictal bold responses in eeg-fmri data from focal epilepsy patients. NeuroImage 49: 366–378.
[22]
Moeller F, LeVan P, Gotman J (2011) Independent component analysis (ica) of generalized spike wave discharges in fmri: Comparison with general linear model-based eeg-fmri. Human Brain Mapping 32: 209–217.
[23]
Rodionov R, De Martino F, Laufs H, Carmichael D, Formisano E, et al. (2007) Independent component analysis of interictal fmri in focal epilepsy: Comparison with general linear model–based eeg–correlated fmri. NeuroImage 38: 488–500.
[24]
Newey CR, Wong C, Wang ZI, Chen X, Wu, et al (2013) Optimizing spect siscom analysis to localize seizure-onset zone by using varying z scores. Epilepsia 54: 793–800.
[25]
Lee S, Lee SY, Yun CH, Lee HY, Lee JS, et al. (2006) Ictal spect in neocortical epilepsies: clinical usefulness and factors affecting the pattern of hyperperfusion. Neuroradiology 48: 678–684.
[26]
Dupont P, Van Paesschen W, Palmini A, Ambayi R, Van Loon J, et al. (2006) Ictal perfusion patterns associated with single mri–visible focal dysplastic lesions: Implications for the noninvasive delineation of the epileptogenic zone. Epilepsia 47: 1550–1557.
[27]
Kurian M, Spinelli L, Delavelle J, Chavez V, Habre W, et al. (2007) Multimodality imaging for focus localization in pediatric pharmacoresistant epilepsy. Epileptic Disorder 9: 20–31.
[28]
Labiner D, Weinand M, Brainerd C, Ahern G, Herring A, et al. (2002) Prognostic value of concordant seizure focus localizing data in the selection of temporal lobectomy candidates. Neurological Reseach 24: 747–755.
[29]
So E (2000) Integration of eeg, mri, and spect in localizing the seizure focus for epilepsy surgery. Epilepsia 43: 219–227.
[30]
Moosmann M, Sch？nfelder VH, Specht K, Scheeringa R, Nordby H, et al. (2009) Realignment parameter–informed artefact correction for simultaneous eeg–fmri recordings. NeuroImage 45: 1144–1150.
[31]
Allen PJ, Josephs O, Turner R (2000) A method for removing imaging artifact from continuous eeg recorded during functional mri. NeuroImage 12: 230–239.
[32]
Rissanen J (1983) A universal prior for integers and estimation by minimum description length. Annals of Statistics 11: 416–431.
[33]
Bell A, Sejnowski T (1995) An information–maximization approach to blind separation and blind deconvolution. Neural Comput 7: 1129–1159.
[34]
Calhoun V, Adali T, Pearlson G, Pekar J (2001) A method for making group inferences from functional mri data using independent component analysis. Human Brain Mapping 14: 140–151.
[35]
Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philosophical Transactions of the Royal Society B: Biological Sciences 360: 1001–1013.
[36]
Morgan V, Price R, Arain A, Modur P, Abou-Khalil B (2004) Resting functional mri with temporal clustering analysis for localization of epileptic activity without eeg. NeuroImage 21: 473–481.
[37]
Morgan V, Li Y, Abou-Khalil B, Gore J (2008) Development of 2dtca for the detection of irregular, transient bold activity. Human Brain Mapping 29: 57–69.
[38]
Khalidov I, Fadili J, Lazeyras F, Van De Ville D, Unser M (2011) Activelets: Wavelets for sparse representation of hemodynamic responses. Signal Processing 91: 2810–2821.
[39]
Lopes R, Lina J, Fahoum F, Gotman J (2012) Detection of epileptic activity in fmri without recording the eeg. NeuroImage 60: 1867–1879.
[40]
Damoiseaux J, Rombouts S, Barkhof F, Scheltens P, Stam C, et al. (2006) Consistent resting–state networks across healthy subjects. Proceedings of the National Academy of Sciences 103: 13848–13853.
[41]
Kiviniemi V, Kantola JH, Jauhiainen J, Hyvarinen A, Tervonen O (2003) Independent component analysis of nondeterministic fmri signal sources. NeuroImage 19: 253–260.
