Identification of epilepsy stages from ECoG using genetic programming classifiers

OBJECTIVE Epilepsy is a common neurological disorder, for which a great deal of research has been devoted to analyze and characterize brain activity during seizures. While this can be done by a human expert, automatic methods still lag behind. This paper analyzes neural activity captured with Electrocorticogram (ECoG), recorded through intracranial implants from Kindling model test subjects. The goal is to automatically identify the main seizure stages: Pre-Ictal, Ictal and Post-Ictal. While visually differentiating each stage can be done by an expert if the complete time-series is available, the goal here is to automatically identify the corresponding stage of short signal segments. METHODS AND MATERIALS The proposal is to pose the above task as a supervised classification problem and derive a mapping function that classifies each signal segment. Given the complexity of the signal patterns, it is difficult to a priori choose any particular classifier. Therefore, Genetic Programming (GP), a population based meta-heuristic for automatic program induction, is used to automatically search for the mapping functions. Two GP-based classifiers are used and extensively evaluated. The signals from epileptic seizures are obtained using the Kindling model of elicited epilepsy in rodent test subjects, for which a seizure was elicited and recorded on four separate days. RESULTS Results show that signal segments from a single seizure can be used to derive accurate classifiers that generalize when tested on different signals from the same subject; i.e., GP can automatically produce accurate mapping functions for intra-subject classification. A large number of experiments are performed with the GP classifiers achieving good performance based on standard performance metrics. Moreover, a proof-of-concept real-world prototype is presented, where a GP classifier is transferred and hard-coded on an embedded system using a digital-to-analogue converter and a field programmable gate array, achieving a low average classification error of 14.55%, sensitivity values between 0.65 and 0.97, and specificity values between 0.86 and 0.94. CONCLUSIONS The proposed approach achieves good results for stage identification, particularly when compared with previous works that focus on this task. The results show that the problem of intra-class classification can be solved with a low error, and high sensitivity and specificity. Moreover, the limitations of the approach are identified and good operating configurations can be proposed based on the results.

[1]  Mengjie Zhang,et al.  Using Gaussian distribution to construct fitness functions in genetic programming for multiclass object classification , 2006, Pattern Recognit. Lett..

[2]  Daniel Rivero,et al.  Automatic feature extraction using genetic programming: An application to epileptic EEG classification , 2011, Expert Syst. Appl..

[3]  George J. Vachtsevanos,et al.  Genetic programming of conventional features to detect seizure precursors , 2007, Eng. Appl. Artif. Intell..

[4]  C. Bigan,et al.  Time-frequency analysis of short segments of biomedical data , 2000 .

[5]  W. Löscher,et al.  Kindling as a model of drug-resistant partial epilepsy: selection of phenytoin-resistant and nonresistant rats. , 1991, The Journal of pharmacology and experimental therapeutics.

[6]  Marie Chavent,et al.  Detecting mental states of alertness with genetic algorithm variable selection , 2013, 2013 IEEE Congress on Evolutionary Computation.

[7]  Wolfgang Löscher,et al.  Anticonvulsant effect of fosphenytoin in amygdala-kindled rats: Comparison with phenytoin , 1998, Epilepsy Research.

[8]  GuoLing,et al.  Automatic feature extraction using genetic programming , 2011 .

[9]  B. Litt,et al.  For Personal Use. Only Reproduce with Permission from the Lancet Publishing Group. Review Prediction of Epileptic Seizures Are Seizures Predictable? Prediction of Epileptic Seizures , 2022 .

[10]  Brian Litt,et al.  Epileptic seizure prediction using hybrid feature selection over multiple intracranial EEG electrode contacts: a report of four patients , 2003, IEEE Transactions on Biomedical Engineering.

[11]  M. Teplan FUNDAMENTALS OF EEG MEASUREMENT , 2002 .

[12]  E. Bertram,et al.  The Relevance of Kindling for Human Epilepsy , 2007, Epilepsia.

[13]  John R. Koza,et al.  Genetic Programming II , 1992 .

[14]  A. Sotelo,et al.  Epilepsy stages diagnosis by Gabor atom density according to their aspect ratio , 2008, 2008 5th International Conference on Electrical Engineering, Computing Science and Automatic Control.

[15]  R. Racine,et al.  Modification of seizure activity by electrical stimulation. II. Motor seizure. , 1972, Electroencephalography and clinical neurophysiology.

[16]  Walter A. Kosters,et al.  Genetic Programming for data classification: partitioning the search space , 2004, SAC '04.

[17]  John R. Koza,et al.  Genetic programming 2 - automatic discovery of reusable programs , 1994, Complex Adaptive Systems.

[18]  Leonidas D. Iasemidis,et al.  Dynamical resetting of the human brain at epileptic seizures: application of nonlinear dynamics and global optimization techniques , 2004, IEEE Transactions on Biomedical Engineering.

[19]  Heitor Silvério Lopes,et al.  Genetic programming for epileptic pattern recognition in electroencephalographic signals , 2007, Appl. Soft Comput..

[20]  J. Barcia,et al.  Anticonvulsant and neurotoxic effects of intracerebroventricular injection of phenytoin, phenobarbital and carbamazepine in an amygdala-kindling model of epilepsy in the rat , 1999, Epilepsy Research.

[21]  Shie Qian,et al.  Time-frequency analysis of high-frequency activity at the start of epileptic seizures , 1997, Proceedings of the 19th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. 'Magnificent Milestones and Emerging Opportunities in Medical Engineering' (Cat. No.97CH36136).

[22]  Leonardo Trujillo,et al.  Epilepsy Ictal Stage Identification by 0-1 Test of Chaos , 2012 .

[23]  Heitor Silvério Lopes,et al.  Detection of epileptic events using genetic programming , 1997, Proceedings of the 19th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. 'Magnificent Milestones and Emerging Opportunities in Medical Engineering' (Cat. No.97CH36136).

[24]  Riccardo Poli,et al.  Foundations of Genetic Programming , 1999, Springer Berlin Heidelberg.

[25]  Margaret Fahnestock,et al.  Kindling and status epilepticus models of epilepsy: rewiring the brain , 2004, Progress in Neurobiology.

[26]  H. Beck,et al.  Effect of phenytoin on sodium and calcium currents in hippocampal CA1 neurons of phenytoin-resistant kindled rats , 2002, Neuropharmacology.

[27]  Brian Litt,et al.  Special issue on epileptic seizure prediction , 2003, IEEE Trans. Biomed. Eng..

[28]  Leonardo Trujillo,et al.  Analysis and Classification of Epilepsy Stages with Genetic Programming , 2012, EVOLVE.

[29]  D. Durand,et al.  Suppression and control of epileptiform activity by electrical stimulation: a review , 2001, Proc. IEEE.

[30]  G. Bergey,et al.  Time-frequency analysis using the matching pursuit algorithm applied to seizures originating from the mesial temporal lobe. , 1998, Electroencephalography and clinical neurophysiology.

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

[32]  Wolfgang Löscher,et al.  Animal Models of Limbic Epilepsies: What Can They Tell Us? , 2002, Brain pathology.

[33]  Leonardo Trujillo,et al.  Predicting problem difficulty for genetic programming applied to data classification , 2011, GECCO '11.

[34]  Brian Litt,et al.  Implantable devices for epilepsy: a clinical perspective , 2002, Proceedings of the Second Joint 24th Annual Conference and the Annual Fall Meeting of the Biomedical Engineering Society] [Engineering in Medicine and Biology.

[35]  G. Bergey,et al.  Characterization of epileptic seizure dynamics using Gabor atom density , 2003, Clinical Neurophysiology.

[36]  Mohamad Sawan,et al.  A Novel Low-Power-Implantable Epileptic Seizure-Onset Detector , 2011, IEEE Transactions on Biomedical Circuits and Systems.

[37]  E. Guijarro,et al.  Epoch Parameterization by Gabor Atom Density in Experimental Epilepsy , 2007, 2007 4th International Conference on Electrical and Electronics Engineering.

[38]  Houman Khosravani,et al.  The effects of high-frequency oscillations in hippocampal electrical activities on the classification of epileptiform events using artificial neural networks , 2006, Journal of neural engineering.