BOLD mapping of human epileptic spikes recorded during simultaneous intracranial EEG-fMRI: The impact of automated spike classification

Objectives: Simultaneous intracranial EEG and functional MRI (icEEG‐fMRI) can be used to map the haemodynamic (BOLD) changes associated with the generation of IEDs. Unlike scalp EEG‐fMRI, in most patients who undergo icEEG‐fMRI, IEDs recorded intracranially are numerous and show variability in terms of field amplitude and morphology. Therefore, visual marking can be highly subjective and time consuming. In this study, we applied an automated spike classification algorithm, Wave_clus (WC), to IEDs marked visually on icEEG data acquired during simultaneous fMRI acquisition. The motivation of this work is to determine whether using a potentially more consistent and unbiased automated approach can produce more biologically meaningful BOLD patterns compared to the BOLD patterns obtained based on the conventional, visual classification. Methods: We analysed simultaneous icEEG‐fMRI data from eight patients with severe drug resistant epilepsy, and who subsequently underwent resective surgery that resulted in a good outcome: confirmed epileptogenic zone (EZ). For each patient two fMRI analyses were performed: one based on the conventional visual IED classification and the other based on the automated classification. We used the concordance of the IED‐related BOLD maps with the confirmed EZ as an indication of their biological meaning, which we compared for the automated and visual classifications for all IED originating in the EZ. Results: Across the group, the visual and automated classifications resulted in 32 and 24 EZ IED classes respectively, for which 75% vs 83% of the corresponding BOLD maps were concordant. At the single‐subject level, the BOLD maps for the automated approach had greater concordance in four patients, and less concordance in one patient, compared to those obtained using the conventional visual classification, and equal concordance for three remaining patients. These differences did not reach statistical significance. Conclusion: We found automated IED classification on icEEG data recorded during fMRI to be feasible and to result in IED‐related BOLD maps that may contain similar or greater biological meaning compared to the conventional approach in the majority of the cases studied. We anticipate that this approach will help to gain significant new insights into the brain networks associated with IEDs and in relation to postsurgical outcome. HighlightsIcEEG‐fMRI provides a unique insight into the generators of IEDs.Visual IED marking can be highly subjective and time consuming.An automated spike classification algorithm, Wave_clus, can minimise subjectivity.The BOLD maps associated with IEDs classified using Wave_clus may commonly have equal or greater biological meaning than those obtained using conventional, visual classification.

[1]  Jean Gotman,et al.  The hemodynamic response to interictal epileptic discharges localizes the seizure‐onset zone , 2017, Epilepsia.

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

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

[4]  Jean Gotman,et al.  Negative BOLD Response to Interictal Epileptic Discharges in Focal Epilepsy , 2013, Brain Topography.

[5]  D. Spencer,et al.  Invasive EEG in Presurgical Evaluation of Epilepsy , 2008 .

[6]  M. Walker,et al.  Mapping human preictal and ictal haemodynamic networks using simultaneous intracranial EEG-fMRI , 2016, NeuroImage: Clinical.

[7]  Andrew B. Gardner,et al.  Comparison of novel computer detectors and human performance for spike detection in intracranial EEG , 2007, Clinical Neurophysiology.

[8]  G. Jackson,et al.  How wrong can we be? The effect of inaccurate mark-up of EEG/fMRI studies in epilepsy , 2009, Clinical Neurophysiology.

[9]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[10]  H. Lüders,et al.  Proposal for a New Classification of Outcome with Respect to Epileptic Seizures Following Epilepsy Surgery , 2001 .

[11]  Jörn Diedrichsen,et al.  Detecting and adjusting for artifacts in fMRI time series data , 2005, NeuroImage.

[12]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[13]  J. Hogg Magnetic resonance imaging. , 1994, Journal of the Royal Naval Medical Service.

[14]  Fabrice Wendling,et al.  What is the concordance between the seizure onset zone and the irritative zone? A SEEG quantified study , 2016, Clinical Neurophysiology.

[15]  M. Walker,et al.  Epileptic Networks in Focal Cortical Dysplasia Revealed Using Electroencephalography–Functional Magnetic Resonance Imaging , 2011, Annals of neurology.

[16]  Bradley G. Goodyear,et al.  Co-localization between the BOLD response and epileptiform discharges recorded by simultaneous intracranial EEG-fMRI at 3 T , 2015, NeuroImage: Clinical.

[17]  Hitten P. Zaveri,et al.  Automatic detection of prominent interictal spikes in intracranial EEG: Validation of an algorithm and relationsip to the seizure onset zone , 2014, Clinical Neurophysiology.

[18]  Patricia Figueiredo,et al.  A study of the electro-haemodynamic coupling using simultaneously acquired intracranial EEG and fMRI data in humans , 2016, NeuroImage.

[19]  J Gotman,et al.  Automatic detection of seizures and spikes. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[20]  L. Lemieux,et al.  With or without spikes: localization of focal epileptic activity by simultaneous electroencephalography and functional magnetic resonance imaging. , 2011, Brain : a journal of neurology.

[21]  C E Elger,et al.  Visual and Automatic Investigation of Epileptiform Spikes in Intracranial EEG Recordings , 1999, Epilepsia.

[22]  Sebastien Ourselin,et al.  A novel scheme for the validation of an automated classification method for epileptic spikes by comparison with multiple observers , 2017, Clinical Neurophysiology.

[23]  C. Elger,et al.  Clinical Relevance of Quantified Intracranial Interictal Spike Activity in Presurgical Evaluation of Epilepsy , 2000, Epilepsia.

[24]  Louis Lemieux,et al.  Simultaneous intracranial EEG and fMRI of interictal epileptic discharges in humans , 2011, NeuroImage.

[25]  D. Nair,et al.  Subdural electrode analysis in focal cortical dysplasia , 2007, Neurology.

[26]  J. Bellanger,et al.  A method to identify reproducible subsets of co-activated structures during interictal spikes. Application to intracerebral EEG in temporal lobe epilepsy , 2005, Clinical Neurophysiology.

[27]  Louis Lemieux,et al.  Classification of EEG abnormalities in partial epilepsy with simultaneous EEG–fMRI recordings , 2014, NeuroImage.

[28]  Jeffrey A. Loeb,et al.  High inter-reviewer variability of spike detection on intracranial EEG addressed by an automated multi-channel algorithm , 2012, Clinical Neurophysiology.

[29]  R. Quian Quiroga,et al.  Unsupervised Spike Detection and Sorting with Wavelets and Superparamagnetic Clustering , 2004, Neural Computation.

[30]  Jerome Engel,et al.  Outcome with respect to epileptic seizures. , 1993 .

[31]  L. Lemieux,et al.  Combined EEG-fMRI and ESI improves localisation of paediatric focal epilepsy , 2017 .

[32]  J. Gotman,et al.  Contribution of EEG/fMRI to the definition of the epileptic focus , 2012, Neurology.

[33]  M. Lüders General principles of pre-surgical evaluation , 2008 .

[34]  John S. Thornton,et al.  Simultaneous intracranial EEG–fMRI in humans: Protocol considerations and data quality , 2012, NeuroImage.

[35]  Prasanna Jayakar,et al.  Subdural EEG Patterns in Children With Taylor-Type Cortical Dysplasia: Comparison With Nondysplastic Lesions , 2005, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[36]  L. Lemieux,et al.  Interictal Functional Connectivity of Human Epileptic Networks Assessed by Intracerebral EEG and BOLD Signal Fluctuations , 2011, PLoS ONE.

[37]  L. Lemieux,et al.  Combined electroencephalography–functional magnetic resonance imaging and electrical source imaging improves localization of pediatric focal epilepsy , 2017, Annals of neurology.

[38]  Louis Lemieux,et al.  EEG-fMRI in the presurgical evaluation of temporal lobe epilepsy , 2015, Journal of Neurology, Neurosurgery & Psychiatry.

[39]  Bradley G Goodyear,et al.  Intracranial EEG‐fMRI analysis of focal epileptiform discharges in humans , 2012, Epilepsia.

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

[41]  J. Gotman,et al.  EEG-fMRI , 2009, Neurology.

[42]  Jeffery A. Hall,et al.  Electroencephalography/functional magnetic resonance imaging responses help predict surgical outcome in focal epilepsy , 2013, Epilepsia.

[43]  H. Lüders,et al.  The epileptogenic zone: general principles. , 2006, Epileptic disorders : international epilepsy journal with videotape.

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

[45]  Richard D. Jones,et al.  Detection of epileptiform discharges in the EEG by a hybrid system comprising mimetic, self-organized artificial neural network, and fuzzy logic stages , 1999, Clinical Neurophysiology.

[46]  Fabrice Wendling,et al.  Simultaneous Intracranial EEG-fMRI Shows Inter-Modality Correlation in Time-Resolved Connectivity Within Normal Areas but Not Within Epileptic Regions , 2017, Brain Topography.

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

[48]  W T Blume,et al.  Proposal for a New Classification of Outcome with Respect to Epileptic Seizures Following Epilepsy Surgery , 2001, Epilepsia.

[49]  M. Walker,et al.  Mapping preictal and ictal haemodynamic networks using video-electroencephalography and functional imaging. , 2012, Brain : a journal of neurology.

[50]  Pablo Valenti,et al.  Automatic detection of interictal spikes using data mining models , 2006, Journal of Neuroscience Methods.

[51]  Frederick Andermann,et al.  Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results , 1995, Annals of neurology.

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

[53]  Bradley G. Goodyear,et al.  Feasibility of an intracranial EEG–fMRI protocol at 3T: Risk assessment and image quality , 2012, NeuroImage.