Research PaperNo Access

Separating Inhibitory and Excitatory Responses of Epileptic Brain to Single-Pulse Electrical Stimulation

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- Discussion on S. Shirani, A. Valentin, G. Alarcon, F. Kazi and S. Sanei, Separating Inhibitory and Excitatory Responses of Epileptic Brain to Single-Pulse Electrical Stimulation, International Journal of Neural Systems, Vol. 33, No. 2 (2023) 2350008

Department of Computer Science, School of Science and Technology, Nottingham Trent University, UK

Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King’s College London, UK

E-mail Address: [email protected]

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Gonzalo Alarcon

The University of Manchester, Oxford Rd, Manchester, UK

E-mail Address: [email protected]

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Farhana Kazi

Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King’s College London, UK

E-mail Address: [email protected]

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, and

Saeid Sanei

Department of Computer Science, School of Science and Technology, Nottingham Trent University, UK

E-mail Address: [email protected]

Corresponding author.

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https://doi.org/10.1142/S0129065723500089Cited by:2 (Source: Crossref)

Abstract

To enable an accurate recognition of neuronal excitability in an epileptic brain for modeling or localization of epileptic zone, here the brain response to single-pulse electrical stimulation (SPES) has been decomposed into its constituent components using adaptive singular spectrum analysis (SSA). Given the response at neuronal level, these components are expected to be the inhibitory and excitatory components. The prime objective is to thoroughly investigate the nature of delayed responses (elicited between 100ms–1 s after SPES) for localization of the epileptic zone. SSA is a powerful subspace signal analysis method for separation of single channel signals into their constituent uncorrelated components. The consistency in the results for both early and delayed brain responses verifies the usability of the approach.

Keywords:

References

1. C. Behr, M. Goltzene, G. Kosmalski, E. Hirsch and P. Ryvlin, Epidemiology of epilepsy, Rev. Neurol. 172(1) (2016) 27–36. Crossref, Medline, Web of Science, Google Scholar
2. L. Forsgren, E. Beghi, A. Oun and M. Sillanpää, The epidemiology of epilepsy in Europe—A systematic review, Eur. J. Neurol. 12(4) (2005) 245–253. Crossref, Medline, Web of Science, Google Scholar
3. U. R. Acharya, S. V. Sree, G. Swapna, R. J. Martis and J. S. Suri, Automated EEG analysis of epilepsy: A review, Knowl.-Based Syst. 45 (2013) 147–165. Crossref, Web of Science, Google Scholar
4. G. Alarcón, J. Martinez, S. V. Kerai, M. E. Lacruz, R. Q. Quiroga, R. P. Selway, M. P. Richardson, J. J. G. Seoane and A. Valentín, In vivo neuronal firing patterns during human epileptiform discharges replicated by electrical stimulation, Clin. Neurophysiol. 123(9) (2012) 1736–1744. Crossref, Medline, Web of Science, Google Scholar
5. B. Abdi-Sargezeh, A. Valentin, G. Alarcon and S. Sanei, Incorporating uncertainty in data labeling into automatic detection of interictal epileptiform discharges from concurrent scalp-EEG via multi-way analysis, Int. J. Neural Syst. 31(08) (2021) 2150019. Link, Web of Science, Google Scholar
6. H. S. Nogay and H. Adeli, Detection of epileptic seizure using pretrained deep convolutional neural network and transfer learning, Eur. Neurol. 83(6) (2020) 602–614. Crossref, Medline, Web of Science, Google Scholar
7. A. Bhattacharya, T. Baweja and S. Karri, Epileptic seizure prediction using deep transformer model, Int. J. Neural Syst. 32(02) (2022) 2150058. Link, Web of Science, Google Scholar
8. A. Olamat, P. Ozel and A. Akan, Synchronization analysis in epileptic EEG signals via state transfer networks based on visibility graph technique, Int. J. Neural Syst. 32(02) (2022) 2150041. Link, Web of Science, Google Scholar
9. H. Bruining et al., Measurement of excitation-inhibition ratio in autism spectrum disorder using critical brain dynamics, Sci. Rep. 10(1) (2020) 1–15. Crossref, Medline, Web of Science, Google Scholar
10. O. Kinouchi and M. Copelli, Optimal dynamical range of excitable networks at criticality, Nat. Phys. 2(5) (2006) 348–351. Crossref, Web of Science, Google Scholar
11. G. G. Turrigiano and S. B. Nelson, Homeostatic plasticity in the developing nervous system, Nat. Rev. Neurosci. 5(2) (2004) 97–107. Crossref, Medline, Web of Science, Google Scholar
12. K. Staley, Molecular mechanisms of epilepsy, Nat. Neurosci. 18(3) (2015) 367–372. Crossref, Medline, Web of Science, Google Scholar
13. L.-R. Shao, C. W. Habela and C. E. Stafstrom, Pediatric epilepsy mechanisms: Expanding the paradigm of excitation/inhibition imbalance, Children 6(2) (2019) 23. Crossref, Medline, Google Scholar
14. A. Valentín, G. Alarcón, M. Honavar, J. J. G. Seoane, R. P. Selway, C. E. Polkey and C. D. Binnie, Single pulse electrical stimulation for identification of structural abnormalities and prediction of seizure outcome after epilepsy surgery: A prospective study, Lancet Neurol. 4(11) (2005) 718–726. Crossref, Medline, Web of Science, Google Scholar
15. G. Alarcón, D. Jiménez-Jiménez, A. Valentín and D. Martín-López, Characterizing EEG cortical dynamics and connectivity with responses to single pulse electrical stimulation (SPES), Int. J. Neural Syst. 28(06) (2018) 1750057. Link, Web of Science, Google Scholar
16. D. Flanagan, A. Valentín, J. J. García Seoane, G. Alarcón and S. G. Boyd, Single-pulse electrical stimulation helps to identify epileptogenic cortex in children, Epilepsia 50(7) (2009) 1793–1803. Crossref, Medline, Web of Science, Google Scholar
17. A. Valentin, M. Anderson, G. Alarcon, J. G. Seoane, R. Selway, C. Binnie and C. Polkey, Responses to single pulse electrical stimulation identify epileptogenesis in the human brain in vivo, Brain 125(8) (2002) 1709–1718. Crossref, Medline, Web of Science, Google Scholar
18. A. Valentin, G. Alarcon, J. J. Garcia-Seoane, M. Lacruz, S. Nayak, M. Honavar, R. P. Selway, C. Binnie and C. Polkey, Single-pulse electrical stimulation identifies epileptogenic frontal cortex in the human brain, Neurology 65(3) (2005) 426–435. Crossref, Medline, Web of Science, Google Scholar
19. J. Engel, Surgical Treatment of the Epilepsies (Raven Press, 1987). Google Scholar
20. V. Kokkinos, G. Alarcón, R. P. Selway and A. Valentín, Role of single pulse electrical stimulation (SPES) to guide electrode implantation under general anaesthesia in presurgical assessment of epilepsy, Seizure 22(3) (2013) 198–204. Crossref, Medline, Web of Science, Google Scholar
21. J. Engel, Update on surgical treatment of the epilepsies: Summary of the second international palm desert conference on the surgical treatment of the epilepsies (1992), Neurology 43(8) (1993) 1612–1612. Crossref, Medline, Web of Science, Google Scholar
22. J. B. Elsner and A. A. Tsonis, Singular Spectrum Analysis: A New Tool in Time Series Analysis (Springer Science and Business Media, 1996). Crossref, Google Scholar
23. S. Sanei and H. Hassani, Singular Spectrum Analysis of Biomedical Signals (CRC Press, 2015). Crossref, Google Scholar
24. S. Sanei, T. K. Lee and V. Abolghasemi, A new adaptive line enhancer based on singular spectrum analysis, IEEE Trans. Biomed. Eng. 59(2) (2011) 428–434. Crossref, Medline, Web of Science, Google Scholar
25. F. Ghaderi, H. R. Mohseni and S. Sanei, Localizing heart sounds in respiratory signals using singular spectrum analysis, IEEE Trans. Biomed. Eng. 58(12) (2011) 3360–3367. Crossref, Medline, Web of Science, Google Scholar
26. S. Kouchaki, S. Sanei, E. L. Arbon and D.-J. Dijk, Tensor based singular spectrum analysis for automatic scoring of sleep EEG, IEEE Trans. Neural Syst. Rehabil. Eng. 23(1) (2014) 1–9. Crossref, Medline, Web of Science, Google Scholar
27. S. Sanei, M. Ghodsi and H. Hassani, An adaptive singular spectrum analysis approach to murmur detection from heart sounds, Med. Eng. Phys. 33(3) (2011) 362–367. Crossref, Medline, Web of Science, Google Scholar
28. M. Ghil and N. Jiang, Recent forecast skill for the el nino/southern oscillation, Geophys. Res. Lett. 25(2) (1998) 171–174. Crossref, Web of Science, Google Scholar
29. K. Patterson, H. Hassani, S. Heravi and A. Zhigljavsky, Multivariate singular spectrum analysis for forecasting revisions to real-time data, J. Appl. Stat. 38(10) (2011) 2183–2211. Crossref, Web of Science, Google Scholar
30. A. Olenko, K. T. Wong, H. Mir and H. Al-Nashash, Generalised correlation index for quantifying signal morphological similarity, Electron. Lett. 52 (22) (2016) 1832–1834. Crossref, Web of Science, Google Scholar
31. D. Nayak, A. Valentín, R. P. Selway and G. Alarcón, Can single pulse electrical stimulation provoke responses similar to spontaneous interictal epileptiform discharges? Clin. Neurophysiol. 125(7) (2014) 1306–1311. Crossref, Medline, Web of Science, Google Scholar
32. A. C. Paulk et al., Local and distant cortical responses to single pulse intracranial stimulation in the human brain are differentially modulated by specific stimulation parameters, Brain Stimul. 15(2) (2022) 491–508. Crossref, Medline, Web of Science, Google Scholar