Abstract
Interictal high-frequency oscillations (HFOs) recorded in intracranial electroencephalographic (iEEG) signals are reliable biomarkers for the epileptogenic zone. Visual identification of these particular events is manually time-consuming and is subject to clinicians’ expertise. Moreover, differentiating them from other transient events such as interictal epileptic spikes (IESs) presents a considerable challenge. Hence, various approaches have been developed with the aim of extracting automatically discriminant features for HFOs and IESs events. Typically, these approaches are based on machine learning (ML) algorithms, but their efficiency strongly depends on the computed features. To address this limitation, we explore deep learning (DL), as a powerful framework, for the classification of HFOs and IESs and propose a novel convolutional neural network (CNN) architecture for HFOs multi-classification. Time–frequency (TF)-based images, computed using the Stockwell transform of the events of interest, are used as inputs to the CNN-based approach. Furthermore, data augmentation (DA) is adopted to improve the generalization of the proposed CNN model. The numerical simulations on epileptic iEEG signals demonstrate that the proposed approach yields superior results when the DA is employed.
Similar content being viewed by others
Data availability
The data that have been used are confidential.
References
Jacobs, J., Staba, R., Asano, E., Otsubo, H., Wu, J.Y., Zijlmans, M., Mohamed, I., Kahane, P., Dubeau, F., Navarro, V., Gotman, J.: High-frequency oscillations (HFOs) in clinical epilepsy. Prog. Neurobiol.. Neurobiol. 98(3), 302–315 (2012). https://doi.org/10.1016/j.pneurobio.2012.03.001
Peng, G., Nourani, M., Harvey, J., Dave, H.: Feature selection using F-statistic values for EEG signal analysis. In: 42th Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC), pp. 5963–5966 (2020)
Zijlmans, M., Jiruska, P., Zelmann, R., Leijen, F.S.S., Jefferys, J., Gorman, J.: High-frequency oscillations as a new biomarker in epilepsy. Ann. Neurol. 71(2), 169–178 (2012). https://doi.org/10.1002/ana.22548
Jrad, N., Kachenoura, A., Merlet, I., Bartolomei, F., Nica, A., Biraben, A., Wendling, F.: Automatic detection and classification of high-frequency oscillations in depth-EEG signals. IEEE Trans. Biomed. Eng. 64(9), 2230–2240 (2017)
Roehri, N., Bartolomei, F.: Are high-frequency oscillations better biomarkers of the epileptogenic zone than spikes? Curr. Opin. Neuro. 17(1), 213–219 (2019)
Lachner-Piza, D., Jacobs, J., Bruder, J.C., Schulze-Bonhage, A., Stieglitz, T., Dümpelmann, M.: Automatic detection of high-frequency-oscillations and their sub-groups co-occurring with interictal-epileptic-spikes. J. Neural. Eng. 17(1) (2020)
Sciaraffa, N., Klados, M.A., Borghini, G., Flumeri, G.D., Babiloni, F., Aricò, P.: Double-step machine learning based procedure for HFOs detection and classification. Brain 10(4) (2020)
Blanco, J.A., Stead, M., Krieger, A., Viventi, J., Marsh, W.R., Lee, K.H., Worrell, G.A., Litt, B.: Unsupervised classification of high-frequency oscillations in human neocortical epilepsy and control patients. J. Neurophysiol.Neurophysiol. 104(5), 2900–2912 (2010)
Liu, S., Sha, Z., Sencer, A., Aydoseli, A., Bebek, N., Abosch, A., Henry, T., Gurses, C., Ince, N.F.: Exploring the time-frequency content of high frequency oscillations for automated identification of seizure onset zone in epilepsy. J. Neural Eng. 13(2) (2016)
Shin, H.C., Roth, H.R., Gao, M., Lu, L., Xu, Z., Nogues, I., Yao, J., Mollura, D., Summers, R.M.: Deep convolutional neural networks for computer-aided detection: CNN architectures, dataset characteristics and transfer learning. IEEE Trans. Med. Imaging 35(5), 1285–1298 (2016)
Bou Nassif, A., Shahin, I., Attili, I., Azzeh, M., Shaalan, K.: Speech recognition using deep neural networks: a systematic review. IEEE Access. 7, 19143–19165 (2019)
Ahad Tawhid, M.N., Siuly, S., Wang, H., Whittaker, F., Wang, K., Zang, Y.: A spectrogram image based intelligent technique for automatic detection of autism spectrum disorder from EEG. PLoS ONE 16(6), 2021 (2019). https://doi.org/10.1371/journal.pone.0253094.eCollection
Rashed-Al-Mahfuz, M., Moni, M.A., Uddin, S., Alyami, S.A., Summers, M.A., Eapen, V.: A deep convolutional neural network method to detect seizures and characteristic frequencies using epileptic electroencephalogram (EEG) data. IEEE J. Trans. Eng. Health Med. 9, 1–12 (2021)
Soleimani, M., Vahidi, A., Vaseghi, B.: Two-dimensional stockwell transform and deep convolutional neural network for multi-class diagnosis of pathological brain. IEEE Trans. Neural Syst. Rehabil. Eng.Rehabil. Eng. 29, 163–172 (2021)
Sun, J., Cao, R., Zhou, M., Hussain, W., Wang, B., Xue, J., Xiang, J.: Hybrid deep neural network for classification of schizophrenia using EEG Data. Sci. Rep. 11(1), 4706 (2021). https://doi.org/10.1038/s41598-021-83350-6
Jadhav, P., Rajguru, G., Datta, D., Mukhopadhyay, S.: Automatic sleep stage classification using time–frequency images of CWT and transfer learning using convolution neural network. Biocybern. Biomed. Eng. 40(1), 494–504 (2020)
Zuo, R., Wei, J., Li, X., Li, C., Zhao, C., Ren, Z., Liang, Y., Geng, X., Jiang, C., Yang, X., Zhang, X.: (2019) Automated detection of high-frequency oscillations in epilepsy based on a convolutional neural network. Front. Comput. Neurosci.Comput. Neurosci. 13, 6 (2019). https://doi.org/10.3389/fncom.2019.00006.eCollection
Lai, D., Zhang, X., Ma, K., Chen, Z., Chen, W., Zhang, H., Yuan, D.L.: Automated detection of high frequency oscillations in intracranial eeg using the combination of short-time energy and convolutional neural networks. IEEE Access. 7, 82501–82511 (2019)
Zhao, B., Hu, W., Zhang, C., Wang, X., Yao, W., Liu, C., Mo, J., Yang, X., Ma, Y., Shao, X., Zhang, K., Zhang, J.: Integrated automatic detection, classification and imaging of high frequency oscillations with stereoelectroencephalography. Front. Neurosci.Neurosci. 14, 465 (2020). https://doi.org/10.3389/fnins.2020.00546
Nadalin, J.K., Eden, U.T., Han, X., Richardson, R.M., Chu, C.J., Kramer, M.A.: Application of a convolutional neural network for fully-automated detection of spike ripples in the scalp electroencephalogram. J. Neurosci.Neurosci. 360, 109239 (2021). https://doi.org/10.1016/j.jneumeth.2021.109239
Katz, J., Abel, T.J.: Stereoelectroencephalography versus subdural electrodes for localization of the epileptogenic zone: what is the evidence? Neurotherapeutics 16, 59–66 (2019). https://doi.org/10.1007/s13311-018-00703-2
Peng, G., Nourani, M., Dave, H., Harvey, J.: Modeling and analysis of seizure network using SEEG for pre-surgery evaluation. In: 22nd IEEE International Conference on Bioinformatics and Bioengineering (BIBE), pp. 327–332 (2022).
Stockwell, R.G., Mansinha, L., Lowe, R.P.: Localization of the complex spectrum: the S transform. IEEE Trans. Signal Process. 44(4), 998–1001 (1996)
Krikid, F., Karfoul, A., Chaibi, S., Kachenoura, A., Nica, A., Kachouri, A., Le Bouquin Jeannès, R.: Classification of high frequency oscillations in intracranial EEG signals based on coupled time-frequency and image-related features. Biomed. Signal Proc. Con. 73(3)
Burnos, S., Hilfiker, P., Sürücü, O., Scholkmann, F., Krayenbühl, N., Grunwald, T., Sarthein, J.: Human intracranial high frequency oscillations (HFOs) detected by automatic time-frequency analysis. PLoS ONE 9(4), e94381 (2014). https://doi.org/10.1371/journal.pone.0094381
Migliorelli, C., Bachiller, A., Alonso, J.F., Romero, S., Aparicio, J., Van Jacobs-Le, J., Mañanas, M.A., San Antonio-Arce, V.: SGM: a novel time-frequency algorithm based on unsupervised learning improves high-frequency oscillation detection in epilepsy. J. Neural Eng. 17(2), 026032 (2020). https://doi.org/10.1088/1741-2552/ab8345
Jmour, N., Zayen, S., Abdelkarim, A.: Convolutional neural networks for image classification. In: International Conference on Advanced Systems and Electric Technologies (IC_ASET), pp. 397–402 (2018)
Szegedy, C., Liu, W., Jia, Y., Sermanet, P., Reed, S., Anguelov, D., Erhan, D., Vanhoucke, V., Rabinovich, R.: Going deeper with convolutions. IEEE Conference on Computer Vision and Pattern Recognition, pp. 1–9 (2015)
Simonyan, K., Zisserman, A.: Very deep convolutional networks for large-scale image recognition. arXiv:1409.1556. [Online]. http://arxiv.org/abs/1409.1556 (2014)
Shorten, C., Khoshgoftaar, T.M.: A survey on image data augmentation for deep learning. J Big Data 60(6) (2019)
Ioffe, S., Szegedy, C.: Batch normalization: accelerating deep network training by reducing internal covariate shift. In: Proceedings of the 32nd International Conference on Machine Learning (Lille), pp. 448–456 (2015)
Zhang, K., Xu, G., Han, Z., Ma, K., Zheng, X., Chen, L., Duan, N., Zhang, S.: Data augmentation for motor imagery signal classification based on a hybrid neural network. Sensors 20, 6 (2020). https://doi.org/10.3390/s20164485
Ssekidde, P., Steven Eyobu, O., Seog Han, D., Oyana, T.J.: Augmented CWT features for deep learning-based indoor localization using WiFi RSSI data. Appl. Sci. 11(4) (2021)
Garcea, F., Serra, A., Lamberti, F., Morra, L.: Data augmentation for medical imaging: a systematic literature review. Comput. Biol. Med.. Biol. Med. 152, 106391 (2023). https://doi.org/10.1016/j.compbiomed.2022.106391
Khosla, C., Saini, B.S. (2020) Enhancing performance of deep learning models with different data augmentation techniques: a survey. In: International Conference on Intelligent Engineering and Management (ICIEM), pp. 79–85
Moreno-Barea, F.J., Strazzera, F., Jerez, J.M., Urda, D., Franco, L.: Forward noise adjustment scheme for data augmentation. In: IEEE Symposium Series on Computational Intelligence (SSCI), pp. 728–734 (2018).
Acknowledgements
The study presented in this paper was conducted as a component of the PHC (Partenariat Hubert Curien) Project CREDIADIC No. 41711PK, CMCU Code 19G1411.
Author information
Authors and Affiliations
Contributions
Conceptualization: [Fatma Krikid]; Methodology: [Fatma Krikid, Ahmad Karfoul]; Formal analysis and investigation: [Fatma Krikid, Ahmad Karfoul]; Writing - original draft preparation: [Fatma Krikid]; Writing - review and editing: [Ahmad Karfoul, Sahbi Chaibi, Régine Le Bouquin Jeannès, Abdennaceur Kachouri]; Resources: [Anca Nica, Amar Kachenoura], Supervision: [Ahmad Karfoul, Régine Le Bouquin Jeannès].
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Krikid, F., Karfoul, A., Chaibi, S. et al. Multi-classification of high-frequency oscillations in intracranial EEG signals based on CNN and data augmentation. SIViP 18, 1099–1109 (2024). https://doi.org/10.1007/s11760-023-02808-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11760-023-02808-4