The combination of EEG Source Imaging and EEG‐correlated functional MRI to map epileptic networks

Functional electrophysiologic techniques such as electroencephalography (EEG) and magnetoencephalography (MEG) give insights into the dynamics of the networks involved in the generation of interictal and ictal epileptic activity and their interaction with physiologic brain activity. With recent advances in methodology and clinical validation, EEG source imaging (ESI) may now be used to map epileptic activity as well as evoked responses to external stimuli. By its ability to show hemodynamic changes time locked to epileptic activity in the whole brain, EEG‐correlated functional magnetic resonance imaging (fMRI) (EEG‐fMRI) is the natural counterpart of ESI, circumventing some of its limitations, the former adding data from the depths of the brain, and the latter temporal resolution. To better understand the potential and limitations of both techniques, this review starts with a description of the neurophysiologic mechanisms that give rise to the measured signals, followed by validation studies based on comparison with intracranial EEG and surgical outcome. We then discuss analysis strategies to combine both techniques by reviewing studies in epilepsy, current methodologic development, and future directions of this fast‐developing field.

[1]  Klaas E. Stephan,et al.  Dynamic causal modelling: A critical review of the biophysical and statistical foundations , 2011, NeuroImage.

[2]  Karl J. Friston,et al.  Dynamic causal modeling , 2010, Scholarpedia.

[3]  M. Walker,et al.  EEG correlated functional MRI and postoperative outcome in focal epilepsy , 2010, Journal of Neurology, Neurosurgery & Psychiatry.

[4]  John S. Thornton,et al.  Feasibility of simultaneous intracranial EEG-fMRI in humans: A safety study , 2010, NeuroImage.

[5]  Jean Daunizeau,et al.  Bayesian multi-modal model comparison: A case study on the generators of the spike and the wave in generalized spike–wave complexes , 2010, NeuroImage.

[6]  M. Castelo‐Branco,et al.  ICA decomposition of EEG signal for fMRI processing in epilepsy , 2009, Human brain mapping.

[7]  Jose M. Sanchez-Bornot,et al.  Model driven EEG/fMRI fusion of brain oscillations , 2009, Human brain mapping.

[8]  Karl J. Friston,et al.  Causal Hierarchy within the Thalamo-Cortical Network in Spike and Wave Discharges , 2009, PloS one.

[9]  Christoph M. Michel,et al.  The spatio-temporal mapping of epileptic networks: Combination of EEG–fMRI and EEG source imaging , 2009, NeuroImage.

[10]  Christoph M. Michel,et al.  Combination of EEG–fMRI and EEG source analysis improves interpretation of spike-associated activation networks in paediatric pharmacoresistant focal epilepsies , 2009, NeuroImage.

[11]  L. Lemieux,et al.  BOLD correlates of interictal epileptic activity: additional contributions from continuous EEG Source Imaging , 2009, NeuroImage.

[12]  Jean Gotman,et al.  Hemodynamic changes preceding the interictal EEG spike in patients with focal epilepsy investigated using simultaneous EEG-fMRI , 2009, NeuroImage.

[13]  C. Michel,et al.  Accuracy of EEG source imaging of epileptic spikes in patients with large brain lesions , 2009, Clinical Neurophysiology.

[14]  Yevgeniy B. Sirotin,et al.  Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity. , 2009, Nature.

[15]  Stephanie Ortigue,et al.  Using ICA and realistic BOLD models to obtain joint EEG/fMRI solutions to the problem of source localization , 2009, NeuroImage.

[16]  D. Tucker,et al.  Localization of Extratemporal Seizure with Noninvasive Dense-Array EEG , 2008, Pediatric Neurosurgery.

[17]  C. Segebarth,et al.  Identifying Neural Drivers with Functional MRI: An Electrophysiological Validation , 2008, PLoS biology.

[18]  Jean Gotman,et al.  Effects of fluctuating physiological rhythms during prolonged EEG-fMRI studies , 2008, Clinical Neurophysiology.

[19]  Louis Lemieux,et al.  Safety of localizing epilepsy monitoring intracranial electroencephalograph electrodes using MRI: Radiofrequency-induced heating , 2008, Journal of magnetic resonance imaging : JMRI.

[20]  Christopher J. Aura,et al.  Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey , 2008, Nature Neuroscience.

[21]  Louis Lemieux,et al.  An investigation of the relationship between BOLD and perfusion signal changes during epileptic generalised spike wave activity. , 2008, Magnetic resonance imaging.

[22]  Richard Bowtell,et al.  Exploring the feasibility of simultaneous electroencephalography/functional magnetic resonance imaging at 7 T. , 2008, Magnetic resonance imaging.

[23]  Thomas Dierks,et al.  BOLD correlates of continuously fluctuating epileptic activity isolated by independent component analysis , 2008, NeuroImage.

[24]  Christoph M. Michel,et al.  A mouse model for studying large-scale neuronal networks using EEG mapping techniques , 2008, NeuroImage.

[25]  Geertjan Huiskamp,et al.  Interictal electromagnetic source imaging in focal epilepsy: practices, results and recommendations , 2008, Current opinion in neurology.

[26]  J Gotman,et al.  Different structures involved during ictal and interictal epileptic activity in malformations of cortical development: an EEG-fMRI study. , 2008, Brain : a journal of neurology.

[27]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[28]  Andreas Kleinschmidt,et al.  Recent advances in recording electrophysiological data simultaneously with magnetic resonance imaging , 2008, NeuroImage.

[29]  Oliver Granert,et al.  Changes in activity of striato–thalamo–cortical network precede generalized spike wave discharges , 2008, NeuroImage.

[30]  M. Cook,et al.  EEG source localization in focal epilepsy: Where are we now? , 2008, Epilepsia.

[31]  Jean Gotman,et al.  Concordance between distributed EEG source localization and simultaneous EEG-fMRI studies of epileptic spikes , 2008, NeuroImage.

[32]  John S. Duncan,et al.  BOLD and perfusion changes during epileptic generalised spike wave activity , 2008, NeuroImage.

[33]  L. Lemieux,et al.  Combined EEG-fMRI and tractography to visualise propagation of epileptic activity , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

[34]  G. Buzsáki,et al.  Inhibition and Brain Work , 2007, Neuron.

[35]  Stephan Wolff,et al.  Different Neuronal Networks Are Associated with Spikes and Slow Activity in Hypsarrhythmia , 2007, Epilepsia.

[36]  John S. Duncan,et al.  Independent component analysis of interictal fMRI in focal epilepsy: Comparison with general linear model-based EEG-correlated fMRI , 2007, NeuroImage.

[37]  Frédéric Grouiller,et al.  A comparative study of different artefact removal algorithms for EEG signals acquired during functional MRI , 2007, NeuroImage.

[38]  F. Leijten,et al.  EEG-fMRI in the preoperative work-up for epilepsy surgery. , 2007, Brain : a journal of neurology.

[39]  John S. Thornton,et al.  Functional MRI with active, fully implanted, deep brain stimulation systems: Safety and experimental confounds , 2007, NeuroImage.

[40]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[41]  H. Laufs,et al.  Electroencephalography/functional MRI in human epilepsy: what it currently can and cannot do , 2007, Current opinion in neurology.

[42]  Arno Villringer,et al.  Evaluating gradient artifact correction of EEG data acquired simultaneously with fMRI. , 2007, Magnetic resonance imaging.

[43]  Karl J. Friston,et al.  Dynamic causal modelling of evoked responses: The role of intrinsic connections , 2007, NeuroImage.

[44]  Jérémie Mattout,et al.  Symmetrical event-related EEG/fMRI information fusion in a variational Bayesian framework , 2007, NeuroImage.

[45]  Yingli Lu,et al.  BOLD changes occur prior to epileptic spikes seen on scalp EEG , 2007, NeuroImage.

[46]  M. Scherg,et al.  Combined spike-related functional MRI and multiple source analysis in the non-invasive spike localization of benign rolandic epilepsy , 2007, Clinical Neurophysiology.

[47]  Nelson J. Trujillo-Barreto,et al.  Modelling the role of excitatory and inhibitory neuronal activity in the generation of the BOLD signal , 2007, NeuroImage.

[48]  Alan Connelly,et al.  EEG‐fMRI in Children with Pharmacoresistant Focal Epilepsy , 2007, Epilepsia.

[49]  A. Villringer,et al.  Simultaneous EEG–fMRI , 2006, Neuroscience & Biobehavioral Reviews.

[50]  Alon Friedman,et al.  Propagation of interictal discharges in temporal lobe epilepsy: Correlation of spatiotemporal mapping with intracranial foramen ovale electrode recordings , 2006, Clinical Neurophysiology.

[51]  J. C. Jimenez,et al.  Nonlinear local electrovascular coupling. I: A theoretical model , 2006, Human brain mapping.

[52]  Hamid Soltanian-Zadeh,et al.  Integrated MEG/EEG and fMRI model based on neural masses , 2006, IEEE Transactions on Biomedical Engineering.

[53]  Fabrice Bartolomei,et al.  Electric Source Imaging in Frontal Lobe Epilepsy , 2006, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[54]  Lei Ding,et al.  Integration of EEG/MEG with MRI and fMRI , 2006, IEEE Engineering in Medicine and Biology Magazine.

[55]  Helmut Laufs,et al.  Where the BOLD signal goes when alpha EEG leaves , 2006, NeuroImage.

[56]  Karl J. Friston,et al.  EEG–fMRI of idiopathic and secondarily generalized epilepsies , 2006, NeuroImage.

[57]  John S. Duncan,et al.  Analysis of EEG–fMRI data in focal epilepsy based on automated spike classification and Signal Space Projection , 2006, NeuroImage.

[58]  J. Gotman,et al.  Combining EEG and fMRI: A multimodal tool for epilepsy research , 2006, Journal of magnetic resonance imaging : JMRI.

[59]  C. Michel,et al.  EEG Source Imaging in Pediatric Epilepsy Surgery: A New Perspective in Presurgical Workup , 2006, Epilepsia.

[60]  Jean Gotman,et al.  Negative BOLD responses to epileptic spikes , 2006, Human brain mapping.

[61]  Karl J. Friston,et al.  Hemodynamic correlates of epileptiform discharges: An EEG-fMRI study of 63 patients with focal epilepsy , 2006, Brain Research.

[62]  Jean Gotman,et al.  EEG–fMRI of epileptic spikes: Concordance with EEG source localization and intracranial EEG , 2006, NeuroImage.

[63]  M. Walker,et al.  EEG-fMRI mapping of asymmetrical delta activity in a patient with refractory epilepsy is concordant with the epileptogenic region determined by intracranial EEG. , 2006, Magnetic resonance imaging.

[64]  Olivier D. Faugeras,et al.  EEG-fMRI fusion of non-triggered data using Kalman filtering , 2006, 3rd IEEE International Symposium on Biomedical Imaging: Nano to Macro, 2006..

[65]  S. Bahar,et al.  Intrinsic optical signal imaging of neocortical seizures: the ‘epileptic dip’ , 2006, Neuroreport.

[66]  N. Logothetis,et al.  Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1 , 2006, Nature Neuroscience.

[67]  J. Gotman,et al.  Correspondence between EEG-fMRI and EEG dipole localisation of interictal discharges in focal epilepsy , 2006, NeuroImage.

[68]  Jean Gotman,et al.  Evaluation of EEG localization methods using realistic simulations of interictal spikes , 2006, NeuroImage.

[69]  J. Gotman,et al.  Grey matter heterotopia: what EEG-fMRI can tell us about epileptogenicity of neuronal migration disorders. , 2006, Brain : a journal of neurology.

[70]  Jean Gotman,et al.  Hemodynamic and metabolic responses to activation, deactivation and epileptic discharges , 2005, NeuroImage.

[71]  Karl J. Friston,et al.  Hemodynamic correlates of EEG: A heuristic , 2005, NeuroImage.

[72]  J. Ebersole,et al.  Intracranial EEG Substrates of Scalp EEG Interictal Spikes , 2005, Epilepsia.

[73]  J Gotman,et al.  Intrinsic epileptogenicity in polymicrogyric cortex suggested by EEG-fMRI BOLD responses , 2005, Neurology.

[74]  S. Meckes-Ferber,et al.  EEG dipole source localisation of interictal spikes acquired during routine clinical video-EEG monitoring , 2004, Clinical Neurophysiology.

[75]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[76]  Louis Lemieux,et al.  EEG/Functional MRI in Epilepsy: The Queen Square Experience , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[77]  Jean Gotman,et al.  EEG‐fMRI of focal epileptic spikes: Analysis with multiple haemodynamic functions and comparison with gadolinium‐enhanced MR angiograms , 2004, Human brain mapping.

[78]  Fabrice Bartolomei,et al.  Electric Source Imaging in Temporal Lobe Epilepsy , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[79]  Gonzalo Alarcón,et al.  Characteristics of scalp electrical fields associated with deep medial temporal epileptiform discharges , 2004, Clinical Neurophysiology.

[80]  J. Gotman,et al.  fMRI activation during spike and wave discharges in idiopathic generalized epilepsy. , 2004, Brain : a journal of neurology.

[81]  C. Michel,et al.  128-Channel EEG Source Imaging in Epilepsy: Clinical Yield and Localization Precision , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[82]  C. Michel,et al.  Propagation of Interictal Epileptiform Activity Can Lead to Erroneous Source Localizations: A 128-Channel EEG Mapping Study , 2003, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[83]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[84]  J. Gotman,et al.  A simulation study of the error in dipole source localization for EEG spikes with a realistic head model , 2003, Clinical Neurophysiology.

[85]  Karl J. Friston,et al.  Functional magnetic resonance imaging of human absence seizures , 2003, Annals of neurology.

[86]  Christoph M. Michel,et al.  Epileptic source localization with high density EEG: how many electrodes are needed? , 2003, Clinical Neurophysiology.

[87]  A. Shmuel,et al.  Sustained Negative BOLD, Blood Flow and Oxygen Consumption Response and Its Coupling to the Positive Response in the Human Brain , 2002, Neuron.

[88]  Bart Vanrumste,et al.  Ictal Source Localization in Presurgical Patients With Refractory Epilepsy , 2002, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[89]  Bin He,et al.  Boundary Element Method-Based Cortical Potential Imaging of Somatosensory Evoked Potentials Using Subjects' Magnetic Resonance Images , 2002, NeuroImage.

[90]  Louis Lemieux,et al.  Comparison of Spike-Triggered Functional MRI BOLD Activation and EEG Dipole Model Localization , 2001, NeuroImage.

[91]  S. Morand,et al.  Electric source imaging of human brain functions , 2001, Brain Research Reviews.

[92]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[93]  G Lantz,et al.  Space-oriented segmentation and 3-dimensional source reconstruction of ictal EEG patterns , 2001, Clinical Neurophysiology.

[94]  J Gotman,et al.  Dipole modeling of scalp electroencephalogram epileptic discharges: correlation with intracerebral fields , 2001, Clinical Neurophysiology.

[95]  E A Disbrow,et al.  Functional MRI at 1.5 tesla: a comparison of the blood oxygenation level-dependent signal and electrophysiology. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[96]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

[97]  C M Michel,et al.  EEG‐Triggered Functional MRI in Patients With Pharmacoresistant Epilepsy , 2000, Journal of magnetic resonance imaging : JMRI.

[98]  C. M. Michel,et al.  Temporal and spatial determination of EEG-seizure onset in the frequency domain , 2000, Clinical Neurophysiology.

[99]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[100]  R J Ilmoniemi,et al.  Spatiotemporal activity of a cortical network for processing visual motion revealed by MEG and fMRI. , 1999, Journal of neurophysiology.

[101]  M R Symms,et al.  EEG-triggered functional MRI of interictal epileptiform activity in patients with partial seizures. , 1999, Brain : a journal of neurology.

[102]  C D Binnie,et al.  Generation of scalp discharges in temporal lobe epilepsy as suggested by intraoperative electrocorticographic recordings , 1999, Journal of neurology, neurosurgery, and psychiatry.

[103]  J S Ebersole,et al.  EEG source modeling. The first word. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[104]  G. Glover Deconvolution of Impulse Response in Event-Related BOLD fMRI1 , 1999, NeuroImage.

[105]  G Lantz,et al.  Frequency domain EEG source localization of ictal epileptiform activity in patients with partial complex epilepsy of temporal lobe origin , 1999, Clinical Neurophysiology.

[106]  J. Ebersole,et al.  Visual and Quantitative Ictal EEG Predictors of Outcome After Temporal Lobectomy , 1999, Epilepsia.

[107]  Louis Lemieux,et al.  Identification of EEG Events in the MR Scanner: The Problem of Pulse Artifact and a Method for Its Subtraction , 1998, NeuroImage.

[108]  R. Buxton,et al.  Dynamics of blood flow and oxygenation changes during brain activation: The balloon model , 1998, Magnetic resonance in medicine.

[109]  T Landis,et al.  Non-invasive epileptic focus localization using EEG-triggered functional MRI and electromagnetic tomography. , 1998, Electroencephalography and clinical neurophysiology.

[110]  L. Lemieux,et al.  Recording of EEG during fMRI experiments: Patient safety , 1997, Magnetic resonance in medicine.

[111]  E. Ryding,et al.  Dipole reconstruction as a method for identifying patients with mesolimbic epilepsy , 1997, Seizure.

[112]  J. Ebersole,et al.  Intracranial EEG Substrates of Scalp Ictal Patterns from Temporal Lobe Foci , 1997, Epilepsia.

[113]  C. N. Guy,et al.  Intracerebral propagation of interictal activity in partial epilepsy: implications for source localisation. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[114]  S Warach,et al.  Monitoring the patient's EEG during echo planar MRI. , 1993, Electroencephalography and clinical neurophysiology.

[115]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[116]  P Gloor,et al.  Neuronal Generators and the Problem of Localization in Electroencephalography: Application of Volume Conductor Theory to Electroencephalography , 1985, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[117]  G. K. Williamson,et al.  A COMPARISON OF VACANCY AND INTERSTITIAL LOOPS IN GRAPHITE , 1961 .

[118]  Fernando Lopes da Silva,et al.  Comprar Niedermeyer's Electroencephalography, 6/e (Basic Principles, Clinical Applications, and Related Fields ) | Fernando Lopes Da Silva | 9780781789424 | Lippincott Williams & Wilkins , 2010 .

[119]  Karl J. Friston,et al.  EEG–fMRI Information Fusion: Biophysics and Data Analysis , 2009 .

[120]  L. Lemieux,et al.  EEG-correlated fMRI and Post-operative Outcome in Focal Epilepsy , 2009 .

[121]  B. He,et al.  A New Multimodal Imaging Strategy for integrating fMRI with EEG , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[122]  P. Nunez,et al.  On the Relationship of Synaptic Activity to Macroscopic Measurements: Does Co-Registration of EEG with fMRI Make Sense? , 2004, Brain Topography.

[123]  P M Rossini,et al.  Does cerebrovascular disease affect the coupling between neuronal activity and local haemodynamics? , 2004, Brain : a journal of neurology.

[124]  F Babiloni,et al.  Cortical Source Estimate of Combined High Resolution EEG and fMRI Data Related to Voluntary Movements , 2002, Methods of Information in Medicine.

[125]  Louis Lemieux,et al.  Role of functional magnetic resonance imaging in the evaluation of patients with malformations caused by cortical development. , 2002, Neurosurgery clinics of North America.

[126]  B. He,et al.  High-resolution spatio-temporal functional neuroimaging of brain activity. , 2002, Critical reviews in biomedical engineering.

[127]  Nelson J. Trujillo-Barreto,et al.  A symmetrical Bayesian model for fMRI and EEG/MEG neuroimage fusion , 2001 .

[128]  O. Blanke,et al.  The use of functional constraints for the neuroelectromagnetic inverse problem: alternatives and caveats. , 2001 .

[129]  J. Ebersole EEG source modeling. The last word. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.