Automatic detection of prominent interictal spikes in intracranial EEG: Validation of an algorithm and relationsip to the seizure onset zone

OBJECTIVE To develop an algorithm for the automatic quantitative description and detection of spikes in the intracranial EEG and quantify the relationship between prominent spikes and the seizure onset zone. METHODS An algorithm was developed for the quantification of time-frequency properties of spikes (upslope, instantaneous energy, downslope) and their statistical representation in a univariate generalized extreme value distribution. Its performance was evaluated in comparison to expert detection of spikes in intracranial EEG recordings from 10 patients. It was subsequently used in 18 patients to detect prominent spikes and quantify their spatial relationship to the seizure onset area. RESULTS The algorithm displayed an average sensitivity of 63.4% with a false detection rate of 3.2 per minute for the detection of individual spikes and an average sensitivity of 88.6% with a false detection rate of 1.4% for the detection of intracranial EEG contacts containing the most prominent spikes. Prominent spikes occurred closer to the seizure onset area than less prominent spikes but they overlapped with it only in a minority of cases (3/18). CONCLUSIONS Automatic detection and quantification of the morphology of spikes increases their utility to localize the seizure onset area. Prominent spikes tend to originate mostly from contacts located in the close vicinity of the seizure onset area rather than from within it. SIGNIFICANCE Quantitative analysis of time-frequency characteristics and spatial distribution of intracranial spikes provides complementary information that may be useful for the localization of the seizure-onset zone.

[1]  W. J. Williams,et al.  Energy based detection of seizures , 1993, Proceedings of the 15th Annual International Conference of the IEEE Engineering in Medicine and Biology Societ.

[2]  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.

[3]  T A Pedley,et al.  Propagation patterns of temporal spikes. , 1995, Electroencephalography and clinical neurophysiology.

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

[5]  Justin A. Blanco,et al.  Data mining neocortical high-frequency oscillations in epilepsy and controls. , 2011, Brain : a journal of neurology.

[6]  Scott B. Wilson,et al.  Spike detection: a review and comparison of algorithms , 2002, Clinical Neurophysiology.

[7]  Bin He,et al.  Cortical Activation Mapping of Epileptiform Activity Derived from Interictal ECoG Spikes , 2007, Epilepsia.

[8]  J. F. Kaiser,et al.  On a simple algorithm to calculate the 'energy' of a signal , 1990, International Conference on Acoustics, Speech, and Signal Processing.

[9]  J. Gotman,et al.  Automatic recognition and quantification of interictal epileptic activity in the human scalp EEG. , 1976, Electroencephalography and Clinical Neurophysiology.

[10]  Karl Rihaczek,et al.  1. WHAT IS DATA MINING? , 2019, Data Mining for the Social Sciences.

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

[12]  Ilker Yaylali,et al.  Detection of Interictal Spikes and Artifactual Data Through Orthogonal Transformations , 2005, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[13]  A. A. Dingle,et al.  Real-time Detection of Epileptiform Activity in the EEG: A Blinded Clinical Trial , 2000, Clinical EEG.

[14]  B. Litt,et al.  Interictal Eeg Spikes Identify the Region of Electrographic Seizure Onset in Some, but Not All, Pediatric Epilepsy Patients Conclusions: Our Data Suggest That Automated Ied Full-length Original Research , 2022 .

[15]  R. Duckrow,et al.  Spatial distribution of intracranially recorded spikes in medial and lateral temporal epilepsies , 2009, Epilepsia.

[16]  W. J. Williams,et al.  Cross Time-frequency Representation Of Electrocorticograms In Temporal Lobe Epilepsy , 1991 .

[17]  W. J. Williams,et al.  Time-frequency representation of electrocorticograms in temporal lobe epilepsy , 1992, IEEE Transactions on Biomedical Engineering.

[18]  S. Mukhopadhyay,et al.  A new interpretation of nonlinear energy operator and its efficacy in spike detection , 1998, IEEE Transactions on Biomedical Engineering.

[19]  C. Schäfer,et al.  Clinical relevance. , 2010, Deutsches Arzteblatt international.

[20]  S. Roberts EXTREME VALUE STATISTICS FOR NOVELTY DETECTION IN BIOMEDICAL DATA PROCESSING , 2000 .

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

[22]  Jean Gotman,et al.  Quantitative Interictal Subdural EEG Analyses in Children with Neocortical Epilepsy , 2003, Epilepsia.

[23]  D. Spencer,et al.  Intracranially recorded interictal spikes: Relation to seizure onset area and effect of medication and time of day , 2013, Clinical Neurophysiology.

[24]  Eishi Asano,et al.  Role of subdural electrocorticography in prediction of long-term seizure outcome in epilepsy surgery. , 2009, Brain : a journal of neurology.

[25]  Zhao Liu,et al.  Detection of High Frequency Oscillations with Teager Energy in an Animal Model of Limbic Epilepsy , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[26]  Shuang Wang,et al.  Ripple classification helps to localize the seizure‐onset zone in neocortical epilepsy , 2013, Epilepsia.

[27]  J. Gotman,et al.  High‐frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery , 2010, Annals of neurology.

[28]  Stephen J. Roberts,et al.  Extreme value statistics for novelty detection in biomedical signal processing , 2000 .

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

[30]  D. Massart,et al.  The Mahalanobis distance , 2000 .