Multiband entropy-based feature-extraction method for automatic identification of epileptic focus based on high-frequency components in interictal iEEG

Presurgical investigations for categorizing focal patterns are crucial, leading to localization and surgical removal of the epileptic focus. This paper presents a machine learning approach using information theoretic features extracted from high-frequency subbands to detect the epileptic focus from interictal intracranial electroencephalogram (iEEG). It is known that high-frequency subbands (>80 Hz) include important biomarkers such as high-frequency oscillations (HFOs) for identifying epileptic focus commonly referred to as the seizure onset zone (SOZ). In this analysis, the multi-channel interictal iEEG signals were splitted into segments and each segment was decomposed into multiple high-frequency subbands. The different types of entropy were calculated for each of the subbands and the sparse linear discriminant analysis (sLDA) was applied to select the prominent entropy features. Due to the imbalance of SOZ and non-SOZ channels in iEEG data, the use of machine learning techniques is always tricky. To deal with the imbalanced learning problem, an adaptive synthetic oversampling approach (ADASYN) with radial basis function kernel-based SVM was used to detect the focal segments. Finally, the epileptic focus was identified based on detection of focal segments on SOZ and non-SOZ channels. Eight patients were examined to observe the efficiency of the automatic detector. The experimental results and statistical tests indicate that the proposed automatic detector can identify the epileptic focus accurately and efficiently.

[1]  Claude E. Shannon,et al.  The mathematical theory of communication , 1950 .

[2]  C. F. Anderson,et al.  The sensitivity and specificity of nutrition-related variables in relationship to the duration of hospital stay and the rate of complications. , 1984, Mayo Clinic proceedings.

[3]  VetterliM.,et al.  Wavelets and Filter Banks , 1992 .

[4]  Martin Vetterli,et al.  Wavelets and filter banks: theory and design , 1992, IEEE Trans. Signal Process..

[5]  C. L. Nikias,et al.  Signal processing with higher-order spectra , 1993, IEEE Signal Processing Magazine.

[6]  S. Pincus Approximate entropy (ApEn) as a complexity measure. , 1995, Chaos.

[7]  Stan Matwin,et al.  Addressing the Curse of Imbalanced Training Sets: One-Sided Selection , 1997, ICML.

[8]  J. Richman,et al.  Physiological time-series analysis using approximate entropy and sample entropy. , 2000, American journal of physiology. Heart and circulatory physiology.

[9]  Claude E. Shannon,et al.  A mathematical theory of communication , 1948, MOCO.

[10]  K Lehnertz,et al.  Indications of nonlinear deterministic and finite-dimensional structures in time series of brain electrical activity: dependence on recording region and brain state. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[11]  B. Pompe,et al.  Permutation entropy: a natural complexity measure for time series. , 2002, Physical review letters.

[12]  Charles L. Wilson,et al.  Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. , 2002, Journal of neurophysiology.

[13]  Nitesh V. Chawla,et al.  SMOTE: Synthetic Minority Over-sampling Technique , 2002, J. Artif. Intell. Res..

[14]  Boualem Boashash,et al.  Time-Frequency Signal Analysis and Processing , 2002 .

[15]  Stan Matwin,et al.  Machine Learning for the Detection of Oil Spills in Satellite Radar Images , 1998, Machine Learning.

[16]  Hugo Vereecke,et al.  Spectral Entropy as an Electroencephalographic Measure of Anesthetic Drug Effect: A Comparison with Bispectral Index and Processed Midlatency Auditory Evoked Response , 2004, Anesthesiology.

[17]  Herna L. Viktor,et al.  Learning from imbalanced data sets with boosting and data generation: the DataBoost-IM approach , 2004, SKDD.

[18]  B. Litt,et al.  High-frequency oscillations and seizure generation in neocortical epilepsy. , 2004, Brain : a journal of neurology.

[19]  Roberto Hornero,et al.  Analysis of regularity in the EEG background activity of Alzheimer's disease patients with Approximate Entropy , 2005, Clinical Neurophysiology.

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

[21]  John S Duncan,et al.  Adult epilepsy , 2006, The Lancet.

[22]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[23]  Pierre LeVan,et al.  High‐Frequency Intracerebral EEG Activity (100–500 Hz) Following Interictal Spikes , 2006, Epilepsia.

[24]  Tom Fawcett,et al.  An introduction to ROC analysis , 2006, Pattern Recognit. Lett..

[25]  Shengcai Liao,et al.  Illumination Invariant Face Recognition Using Near-Infrared Images , 2007, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[26]  Tom Fawcett,et al.  ROC Graphs: Notes and Practical Considerations for Researchers , 2007 .

[27]  Brian Litt,et al.  Human and automated detection of high-frequency oscillations in clinical intracranial EEG recordings , 2007, Clinical Neurophysiology.

[28]  V. Srinivasan,et al.  Approximate Entropy-Based Epileptic EEG Detection Using Artificial Neural Networks , 2007, IEEE Transactions on Information Technology in Biomedicine.

[29]  Jean Gotman,et al.  Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. , 2007, Brain : a journal of neurology.

[30]  Jeffery A. Hall,et al.  Interictal high‐frequency oscillations (80–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain , 2008, Epilepsia.

[31]  Haibo He,et al.  ADASYN: Adaptive synthetic sampling approach for imbalanced learning , 2008, 2008 IEEE International Joint Conference on Neural Networks (IEEE World Congress on Computational Intelligence).

[32]  J. Pastor,et al.  Synchronization Clusters of Interictal Activity in the Lateral Temporal Cortex of Epileptic Patients: Intraoperative Electrocorticographic Analysis , 2008, Epilepsia.

[33]  Constantino Tsallis,et al.  Computational applications of nonextensive statistical mechanics , 2009 .

[34]  Haibo He,et al.  Learning from Imbalanced Data , 2009, IEEE Transactions on Knowledge and Data Engineering.

[35]  J. Gotman,et al.  High frequency oscillations (80–500 Hz) in the preictal period in patients with focal seizures , 2009, Epilepsia.

[36]  Cuntai Guan,et al.  Learning from other subjects helps reducing Brain-Computer Interface calibration time , 2010, 2010 IEEE International Conference on Acoustics, Speech and Signal Processing.

[37]  Sandipan Pati,et al.  Pharmacoresistant epilepsy: From pathogenesis to current and emerging therapies , 2010, Cleveland Clinic Journal of Medicine.

[38]  Ali H. Shoeb,et al.  Application of Machine Learning To Epileptic Seizure Detection , 2010, ICML.

[39]  Daniel Rivero,et al.  Epileptic seizure detection using multiwavelet transform based approximate entropy and artificial neural networks , 2010, Journal of Neuroscience Methods.

[40]  Ahmad Ayatollahi,et al.  EEG analysis based on wavelet-spectral entropy for epileptic seizures detection , 2010, 2010 3rd International Conference on Biomedical Engineering and Informatics.

[41]  Pietro Liò,et al.  A new approach for epileptic seizure detection: sample entropy based feature extraction and extreme learning machine , 2010 .

[42]  Qiang Yang,et al.  A Survey on Transfer Learning , 2010, IEEE Transactions on Knowledge and Data Engineering.

[43]  Trevor J. Hastie,et al.  Sparse Discriminant Analysis , 2011, Technometrics.

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

[45]  Duoqian Miao,et al.  Best basis-based wavelet packet entropy feature extraction and hierarchical EEG classification for epileptic detection , 2011, Expert Syst. Appl..

[46]  Jean Gotman,et al.  Ictal and interictal high frequency oscillations in patients with focal epilepsy , 2011, Clinical Neurophysiology.

[47]  I Kleinschmidt,et al.  Incidence of epilepsy , 2011, Neurology.

[48]  Matthias Dümpelmann,et al.  Automatic 80–250Hz “ripple” high frequency oscillation detection in invasive subdural grid and strip recordings in epilepsy by a radial basis function neural network , 2012, Clinical Neurophysiology.

[49]  Shengcai Liao,et al.  Efficient feature selection for linear discriminant analysis and its application to face recognition , 2012, Proceedings of the 21st International Conference on Pattern Recognition (ICPR2012).

[50]  Ralph G Andrzejak,et al.  Nonrandomness, nonlinear dependence, and nonstationarity of electroencephalographic recordings from epilepsy patients. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[51]  Julius Georgiou,et al.  Detection of epileptic electroencephalogram based on Permutation Entropy and Support Vector Machines , 2012, Expert Syst. Appl..

[52]  Cuntai Guan,et al.  Filter Bank Common Spatial Pattern Algorithm on BCI Competition IV Datasets 2a and 2b , 2012, Front. Neurosci..

[53]  S. Blanco,et al.  Comparison of Frequency Bands Using Spectral Entropy for Epileptic Seizure Prediction , 2013, ISRN neurology.

[54]  Ram Bilas Pachori,et al.  Epileptic seizure detection based on the instantaneous area of analytic intrinsic mode functions of EEG signals , 2013 .

[55]  Toshihisa Tanaka,et al.  Simultaneous Design of FIR Filter Banks and Spatial Patterns for EEG Signal Classification , 2013, IEEE Transactions on Biomedical Engineering.

[56]  Shahin Hakimian,et al.  Surgical Treatment of Epilepsy , 2013, Continuum.

[57]  Andreas Schulze-Bonhage,et al.  Differentiation of specific ripple patterns helps to identify epileptogenic areas for surgical procedures , 2014, Clinical Neurophysiology.

[58]  Jae-Kwon Kim,et al.  Classification of normal and epileptic seizure EEG signals using wavelet transform, phase-space reconstruction, and Euclidean distance , 2014, Comput. Methods Programs Biomed..

[59]  Nick C Fox,et al.  Gene-Wide Analysis Detects Two New Susceptibility Genes for Alzheimer's Disease , 2014, PLoS ONE.

[60]  J. H. Cross,et al.  ILAE Official Report: A practical clinical definition of epilepsy , 2014, Epilepsia.

[61]  U. Rajendra Acharya,et al.  Linear and nonlinear analysis of normal and CAD-affected heart rate signals , 2014, Comput. Methods Programs Biomed..

[62]  Moses O. Sokunbi,et al.  Nonlinear Complexity Analysis of Brain fMRI Signals in Schizophrenia , 2014, PloS one.

[63]  Xingyu Wang,et al.  Aggregation of Sparse Linear Discriminant analyses for Event-Related potential Classification in Brain-Computer Interface , 2014, Int. J. Neural Syst..

[64]  Byron M. Yu,et al.  Dimensionality reduction for large-scale neural recordings , 2014, Nature Neuroscience.

[65]  E. Carrette,et al.  Functional brain connectivity from EEG in epilepsy: Seizure prediction and epileptogenic focus localization , 2014, Progress in Neurobiology.

[66]  Zhijie Bian,et al.  Analysis of entropies based on empirical mode decomposition in amnesic mild cognitive impairment of diabetes mellitus , 2015 .

[67]  U. Rajendra Acharya,et al.  Application of Entropy Measures on Intrinsic Mode Functions for the Automated Identification of Focal Electroencephalogram Signals , 2015, Entropy.

[68]  P. Boonluksiri,et al.  Clinical Prediction Rule of Drug Resistant Epilepsy in Children , 2015, Journal of epilepsy research.

[69]  U. Rajendra Acharya,et al.  An Integrated Index for the Identification of Focal Electroencephalogram Signals Using Discrete Wavelet Transform and Entropy Measures , 2015, Entropy.

[70]  Stefano Di Gennaro,et al.  Detection of epileptiform activity in EEG signals based on time-frequency and non-linear analysis , 2015, Front. Comput. Neurosci..

[71]  Rajeev Sharma,et al.  Classification of epileptic seizures in EEG signals based on phase space representation of intrinsic mode functions , 2015, Expert Syst. Appl..

[72]  Gregory K. Bergey,et al.  Identification of seizure onset zone and preictal state based on characteristics of high frequency oscillations , 2015, Clinical Neurophysiology.

[73]  Tzyy-Ping Jung,et al.  High-speed spelling with a noninvasive brain–computer interface , 2015, Proceedings of the National Academy of Sciences.

[74]  Sridevi V. Sarma,et al.  Physiology of functional and effective networks in epilepsy , 2015, Clinical Neurophysiology.

[75]  Xingyu Wang,et al.  Optimizing spatial patterns with sparse filter bands for motor-imagery based brain–computer interface , 2015, Journal of Neuroscience Methods.

[76]  Haruhiko Kishima,et al.  Detection of Epileptic Seizures Using Phase–Amplitude Coupling in Intracranial Electroencephalography , 2016, Scientific Reports.

[77]  J. Blas,et al.  Management-Related Traffic as a Stressor Eliciting Parental Care in a Roadside-Nesting Bird: The European Bee-Eater Merops apiaster , 2016, PloS one.

[78]  Michel Le Van Quyen,et al.  RIPPLELAB: A Comprehensive Application for the Detection, Analysis and Classification of High Frequency Oscillations in Electroencephalographic Signals , 2016, PloS one.

[79]  Y. Chen,et al.  Combination of the Manifold Dimensionality Reduction Methods with Least Squares Support vector machines for Classifying the Species of Sorghum Seeds , 2016, Scientific Reports.

[80]  Justin Dauwels,et al.  Epileptiform spike detection via convolutional neural networks , 2016, 2016 IEEE International Conference on Acoustics, Speech and Signal Processing (ICASSP).

[81]  Toshihisa Tanaka,et al.  Robust Averaging of Covariances for EEG Recordings Classification in Motor Imagery Brain-Computer Interfaces , 2017, Neural Computation.

[82]  Nitesh V. Chawla,et al.  Automated epileptic seizure detection using improved correlation-based feature selection with random forest classifier , 2017, Neurocomputing.

[83]  Fabrice Wendling,et al.  Automatic Detection and Classification of High-Frequency Oscillations in Depth-EEG Signals , 2017, IEEE Trans. Biomed. Eng..

[84]  Toshihisa Tanaka,et al.  Epileptic focus localization based on bivariate empirical mode decomposition and entropy , 2017, 2017 Asia-Pacific Signal and Information Processing Association Annual Summit and Conference (APSIPA ASC).

[85]  Toshihisa Tanaka,et al.  Unsupervised frequency-recognition method of SSVEPs using a filter bank implementation of binary subband CCA , 2017, Journal of neural engineering.

[86]  B Santoso,et al.  Synthetic Over Sampling Methods for Handling Class Imbalanced Problems : A Review , 2017 .

[87]  Kenichiro Sato,et al.  The Prehospital Predictors of Tracheal Intubation for in Patients who Experience Convulsive Seizures in the Emergency Department , 2017, Internal medicine.

[88]  Ihsan Ullah,et al.  An Automated System for Epilepsy Detection using EEG Brain Signals based on Deep Learning Approach , 2018, Expert Syst. Appl..

[89]  Rui Cao,et al.  Epileptic Seizure Detection Based on EEG Signals and CNN , 2018, Front. Neuroinform..

[90]  Jiaqing Yan,et al.  Determining the Quantitative Threshold of High-Frequency Oscillation Distribution to Delineate the Epileptogenic Zone by Automated Detection , 2018, Front. Neurol..

[91]  Yue Gao,et al.  A Stacked Sparse Autoencoder-Based Detector for Automatic Identification of Neuromagnetic High Frequency Oscillations in Epilepsy , 2018, IEEE Transactions on Medical Imaging.

[92]  N. Ince,et al.  Stereotyped high-frequency oscillations discriminate seizure onset zones and critical functional cortex in focal epilepsy , 2018, Brain : a journal of neurology.

[93]  Lucia Rita Quitadamo,et al.  EPINETLAB: A Software for Seizure-Onset Zone Identification From Intracranial EEG Signal in Epilepsy , 2018, Front. Neuroinform..

[94]  U. Rajendra Acharya,et al.  Deep convolutional neural network for the automated detection and diagnosis of seizure using EEG signals , 2017, Comput. Biol. Medicine.

[95]  Xin Yao,et al.  A Systematic Study of Online Class Imbalance Learning With Concept Drift , 2017, IEEE Transactions on Neural Networks and Learning Systems.

[96]  Rasmus Larsen,et al.  SpaSM: A MATLAB Toolbox for Sparse Statistical Modeling , 2018 .

[97]  Toshihisa Tanaka,et al.  Multiband tangent space mapping and feature selection for classification of EEG during motor imagery , 2018, Journal of neural engineering.

[98]  Camilo J. Mininni,et al.  Seizure localization using pre ictal phase-amplitude coupling in intracranial electroencephalography , 2019, Scientific Reports.

[99]  A. V. Medvedev,et al.  A Long Short-Term Memory neural network for the detection of epileptiform spikes and high frequency oscillations , 2019, Scientific Reports.

[100]  Ying Liang,et al.  Automated Detection of High-Frequency Oscillations in Epilepsy Based on a Convolutional Neural Network , 2019, Front. Comput. Neurosci..

[101]  Han Yuan,et al.  Automated Detection of High Frequency Oscillations in Intracranial EEG Using the Combination of Short-Time Energy and Convolutional Neural Networks , 2019, IEEE Access.