Abstract
This study investigates the performance of a convolutional neural network (CNN) algorithm on epilepsy diagnosis. Without pathology, diagnosis involves long and costly electroencephalographic (EEG) monitoring. Novel approaches may overcome this by comparing brain connectivity using graph metrics. This study, however, uses deep learning to learn connectivity patterns directly from easily acquired EEG data. A CNN algorithm was applied on directed Granger causality (GC) connectivity measures, derived from 50 s of resting-state surface EEG recordings from 30 subjects with epilepsy and a 30 subject control group. The trained CNN filters reflected reduced delta band connectivity in frontal regions and increased left lateralized frontal-posterior gamma band connectivity. A diagnosis accuracy of 85% (F1 score 85%) was achieved by an ensemble of CNN models, each trained on differently prepared data from different electrode combinations. Appropriate preparation of connectivity data enables generic CNN algorithms to be used for detection of multiple discriminative epileptic features. Differential patterns revealed in this study may help to shed light on underlying altered cognitive abilities in epilepsy patients. The accuracy achieved in this study shows that, in combination with other methods, this approach could prove a valuable clinical decision support system for epilepsy diagnosis.
Graphical abstract
1: EEG measurements and subsequent connectivity calculation, 2: training of a neural network on resulting connectivity matrices, 3: extraction of most efficient CNN filters, which are neuromarker for epilepsy
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References
Cilasun MH, Yalcin H (2016) A deep learning approach to EEG based epilepsy seizure determination
Hussein R (2019) Scalp and intracranial EEG quantitative analysis robust detection and prediction of epileptic seizures. The University of British Colombia
Gadhoumi K, Lina JM, Mormann F, Gotman J (2016) Seizure prediction for therapeutic devices: a review. J. Neurosci. Methods
Zhang Y, Yang S, Liu Y et al (2018) Integration of 24 feature types to accurately detect and predict seizures using scalp EEG signals. Sensors (Switzerland). https://doi.org/10.3390/s18051372
Yadollahpour A, Jalilifar M (2014) Seizure prediction methods: a review of the current predicting techniques. Biomed Pharmacol J. https://doi.org/10.13005/bpj/466
Smith SJM (2005) EEG in the diagnosis, classification, and management of patients with epilepsy. Neurol. Pract.
Bernhardt BC, Bonilha L, Gross DW (2015) Network analysis for a network disorder: the emerging role of graph theory in the study of epilepsy. Epilepsy Behav.
Ktena SI, Parisot S, Ferrante E, et al (2017) Distance metric learning using graph convolutional networks: application to functional brain networks. In: Lecture Notes in Computer Science (including subseries Lecture Notes in Artificial Intelligence and Lecture Notes in Bioinformatics)
Anirudh R, Thiagarajan JJ (2019) Bootstrapping graph convolutional neural networks for autism spectrum disorder classification. In: ICASSP, IEEE International Conference on Acoustics, Speech and Signal Processing - Proceedings
Yang J, Zhu Q, Zhang R et al (2020) Unified brain network with functional and structural data. Lecture Notes in Computer Science (including subseries Lecture Notes in Artificial Intelligence and Lecture Notes in Bioinformatics). Springer, Cham., pp 114–123
Huang J, Zhou L, Wang L, Zhang D (2020) Attention-diffusion-bilinear neural network for brain network analysis. IEEE Trans Med Imaging. https://doi.org/10.1109/TMI.2020.2973650
Protopapa F, Siettos CI, Myatchin I, Lagae L (2016) Children with well controlled epilepsy possess different spatio-temporal patterns of causal network connectivity during a visual working memory task. Cogn Neurodyn. https://doi.org/10.1007/s11571-015-9373-x
Dasgupta A, Das R, Nayak L, De RK (2015) Analyzing epileptogenic brain connectivity networks using clinical EEG data. In: Proceedings - 2015 IEEE International Conference on Bioinformatics and Biomedicine, BIBM 2015
Sargolzaei S, Cabrerizo M, Sargolzaei A et al (2015) A probabilistic approach for pediatric epilepsy diagnosis using brain functional connectivity networks. BMC Bioinformatics. https://doi.org/10.1186/1471-2105-16-S7-S9
Rajaei H, Cabrerizo M, Sargolzaei S, et al (2015) Pediatric epilepsy: clustering by functional connectivity using phase synchronization. In: IEEE Biomedical Circuits and Systems Conference: Engineering for Healthy Minds and Able Bodies, BioCAS 2015 - Proceedings
Coito A, Michel CM, Van Mierlo P et al (2016) Directed functional brain connectivity based on EEG source imaging: methodology and application to temporal lobe epilepsy. IEEE Trans Biomed Eng. https://doi.org/10.1109/TBME.2016.2619665
Verhoeven T, Coito A, Plomp G et al (2018) Automated diagnosis of temporal lobe epilepsy in the absence of interictal spikes. NeuroImage Clin. https://doi.org/10.1016/j.nicl.2017.09.021
Marino AC, Yang GJ, Tyrtova E et al (2019) Resting state connectivity in neocortical epilepsy: the epilepsy network as a patient-specific biomarker. Clin Neurophysiol. https://doi.org/10.1016/j.clinph.2018.11.016
Dumlu SN, Ademoğlu A, Sun W (2020) Investigation of functional variability and connectivity in temporal lobe epilepsy: a resting state fMRI study. Neurosci Lett. https://doi.org/10.1016/j.neulet.2020.135076
Clemens B, Puskás S, Bessenyei M et al (2011) EEG functional connectivity of the intrahemispheric cortico-cortical network of idiopathic generalized epilepsy. Epilepsy Res. https://doi.org/10.1016/j.eplepsyres.2011.04.011
Dupont S, Samson Y, Van de Moortele PF et al (2002) Bilateral hemispheric alteration of memory processes in right medial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry. https://doi.org/10.1136/jnnp.73.5.478
Vlooswijk MCG, Jansen JFA, de Krom MCFTM, et al (2010) Functional MRI in chronic epilepsy: associations with cognitive impairment. Lancet Neurol.
Zhang Z, Lu G, Zhong Y et al (2010) Altered spontaneous neuronal activity of the default-mode network in mesial temporal lobe epilepsy. Brain Res. https://doi.org/10.1016/j.brainres.2010.01.042
Buckner RL, Carroll DC (2007) Self-projection and the brain. Trends Cogn Sci. https://doi.org/10.1016/j.tics.2006.11.004
Liao W, Zhang Z, Pan Z et al (2011) Default mode network abnormalities in mesial temporal lobe epilepsy: a study combining fMRI and DTI. Hum Brain Mapp. https://doi.org/10.1002/hbm.21076
Obeid I, Picone J (2016) The temple university hospital EEG data corpus. Front Neurosci. https://doi.org/10.3389/fnins.2016.00196
Shah V, von Weltin E, Lopez S et al (2018) The temple university hospital seizure detection corpus. Front Neuroinform. https://doi.org/10.3389/fninf.2018.00083
Rijnders B (2021) Machine learning and EEG in epilepsy [Master’s Thesis, Yeditepe University]. Open Access. https://acikbilim.yok.gov.tr/handle/20.500.12812/340593
Tadel F, Baillet S, Mosher JC et al (2011) Brainstorm: a user-friendly application for MEG/EEG analysis. Comput Intell Neurosci. https://doi.org/10.1155/2011/879716
Stam CJ (2014) Modern network science of neurological disorders. Nat. Rev. Neurosci.
Van Diessen E, Diederen SJH, Braun KPJ, et al (2013) Functional and structural brain networks in epilepsy: what have we learned? Epilepsia
Jiang LW, Qian RB, Fu XM et al (2018) Altered attention networks and DMN in refractory epilepsy: a resting-state functional and causal connectivity study. Epilepsy Behav. https://doi.org/10.1016/j.yebeh.2018.06.045
Wang B, Meng L (2016) Functional brain network alterations in epilepsy: a magnetoencephalography study. Epilepsy Res. https://doi.org/10.1016/j.eplepsyres.2016.06.014
Wu X, Li R, Fleisher AS et al (2011) Altered default mode network connectivity in Alzheimer’s disease—a resting functional MRI and Bayesian network study. Hum Brain Mapp. https://doi.org/10.1002/hbm.21153
Doucet G, Osipowicz K, Sharan A et al (2013) Extratemporal functional connectivity impairments at rest are related to memory performance in mesial temporal epilepsy. Hum Brain Mapp. https://doi.org/10.1002/hbm.22059
Bettus G, Guedj E, Joyeux F et al (2009) Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms. Hum Brain Mapp. https://doi.org/10.1002/hbm.20625
Xia LVZ, Hong HD, Ye W et al (2014) Alteration of functional connectivity within visuospatial working memory-related brain network in patients with right temporal lobe epilepsy: a resting-state fMRI study. Epilepsy Behav. https://doi.org/10.1016/j.yebeh.2014.04.001
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The authors acknowledge Ali Uslu and Dr. Seda Dumlu for their proofreading assistance.
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Rijnders, B., Korkmaz, E.E. & Yildirim, F. Hybrid machine learning method for a connectivity-based epilepsy diagnosis with resting-state EEG. Med Biol Eng Comput 60, 1675–1689 (2022). https://doi.org/10.1007/s11517-022-02560-w
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DOI: https://doi.org/10.1007/s11517-022-02560-w