Alterations of β-γ coupling of scalp electroencephalography during epilepsy_Journal of Biomedical Engineering

Authors：

LI Kaijie ¹ , LU Junfeng ¹ , YU Renping ^1,2 , ZHANG Rui ^1,2 ,  CHEN Mingming ^1,2

1. Henan Key Laboratory of Brain Science and Brain-Computer Interface Technology, School of Electrical and Information Engineering, Zhengzhou University, Zhengzhou 450001, P. R. China;
2. Research Center for Intelligent Science and Engineering Technology of Traditional Chinese Medicine, School of Electrical and Information Engineering, Zhengzhou University, Zhengzhou 450001, P. R. China;

Corresponding author：

CHEN Mingming, Email: mmchen@zzu.edu.cn

Keywords：

Epilepsy; Scalp electroencephalography; Phase-amplitude coupling; Modulation index

DOI：

10.7507/1001-5515.202212024

Video：

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Uncovering the alterations of neural interactions within the brain during epilepsy is important for the clinical diagnosis and treatment. Previous studies have shown that the phase-amplitude coupling (PAC) can be used as a potential biomarker for locating epileptic zones and characterizing the transition of epileptic phases. However, in contrast to the θ-γ coupling widely investigated in epilepsy, few studies have paid attention to the β-γ coupling, as well as its potential applications. In the current study, we use the modulation index (MI) to calculate the scalp electroencephalography (EEG)-based β-γ coupling and investigate the corresponding changes during different epileptic phases. The results show that the β-γ coupling of each brain region changes with the evolution of epilepsy, and in several brain regions, the β-γ coupling decreases during the ictal period but increases in the post-ictal period, where the differences are statistically significant. Moreover, the alterations of β-γ coupling between different brain regions can also be observed, and the strength of β-γ coupling increases in the post-ictal period, where the differences are also significant. Taken together, these findings not only contribute to understanding neural interactions within the brain during the evolution of epilepsy, but also provide a new insight into the clinical treatment.

Citation： LI Kaijie, LU Junfeng, YU Renping, ZHANG Rui, CHEN Mingming. Alterations of β-γ coupling of scalp electroencephalography during epilepsy. Journal of Biomedical Engineering, 2023, 40(4): 700-708, 717. doi: 10.7507/1001-5515.202212024 Copy

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18.	Tort A B, Komorowski R, Eichenbaum H, et al. Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. Journal of Neurophysiology, 2010, 104(2): 1195-1210..
19.	Kullback S, Leibler R A. On information and sufficiency. The Annals of Mathematical Statistics, 1951, 22(1): 79-86..
20.	Hülsemann M J, Naumann E, Rasch B. Quantification of phase-amplitude coupling in neuronal oscillations: comparison of phase-locking value, mean vector length, modulation index, and generalized-linear-modeling-cross-frequency-coupling. Frontiers in Neuroscience, 2019, 13: 573..
21.	Canolty R T, Knight R T. The functional role of cross-frequency coupling. Trends in Cognitive Sciences, 2010, 14(11): 506-515..
22.	van der Meij R, Kahana M, Maris E. Phase–amplitude coupling in human electrocorticography is spatially distributed and phase diverse. Journal of Neuroscience, 2012, 32(1): 111-123..
23.	Schroeder C E, Lakatos P. Low-frequency neuronal oscillations as instruments of sensory selection. Trends in Neurosciences, 2009, 32(1): 9-18..
24.	Amemiya S, Redish A D. Hippocampal theta-gamma coupling reflects state-dependent information processing in decision making. Cell Reports, 2018, 22(12): 3328-3338..
25.	Köster M, Finger H, Graetz S, et al. Theta-gamma coupling binds visual perceptual features in an associative memory task. Scientific Reports, 2018, 8(1): 17688..
26.	Liang W K, Tseng P, Yeh J R, et al. Frontoparietal beta amplitude modulation and its interareal cross-frequency coupling in visual working memory. Neuroscience, 2021, 460: 69-87..
27.	Edakawa K, Yanagisawa T, Kishima H, et al. Detection of epileptic seizures using phase–amplitude coupling in intracranial electroencephalography. Scientific Reports, 2016, 6: 25422..
28.	Guggisberg A G, Kirsch H E, Mantle M M, et al. Fast oscillations associated with interictal spikes localize the epileptogenic zone in patients with partial epilepsy. Neuroimage, 2008, 39(2): 661-668..
29.	Lundstrom B N, Brinkmann B H, Worrell G A. Low frequency novel interictal EEG biomarker for localizing seizures and predicting outcomes. Brain Communications, 2021, 3(4): fcab231..

1. Rudebeck P H, Rich E L. Orbitofrontal cortex. Current Biology, 2018, 28(18): R1083-R1088..
2. Beghi E. The epidemiology of epilepsy. Neuroepidemiology, 2020, 54(2): 185-191..
3. Löscher W. Animal models of intractable epilepsy. Progress in Neurobiology, 1997, 53(2): 239-258..
4. Casson A J, Yates D C, Smith S J, et al. Wearable electroencephalography. What is it, why is it needed, and what does it entail?. IEEE Engineering in Medicine and Biology Magazine, 2010, 29(3): 44-56..
5. Das K, Daschakladar D, Roy P P, et al. Epileptic seizure prediction by the detection of seizure waveform from the pre-ictal phase of EEG signal. Biomedical Signal Processing and Control, 2020, 57: 101720..
6. Lopes M A, Perani S, Yaakub S N, et al. Revealing epilepsy type using a computational analysis of interictal EEG. Scientific Reports, 2019, 9(1): 10169..
7. Mormann F, Lehnertz K, David P, et al. Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Physica D: Nonlinear Phenomena, 2000, 144(3-4): 358-369..
8. Voytek B, D'Esposito M, Crone N, et al. A method for event-related phase/amplitude coupling. Neuroimage, 2013, 64: 416-424..
9. Liang Z, Jin X, Ren Y, et al. Propofol anesthesia decreased the efficiency of long-range cortical interaction in humans. IEEE Transactions on Biomedical Engineering, 2021, 69(1): 165-175..
10. Ma H, Wang Z, Li C, et al. Phase–amplitude coupling and epileptogenic zone localization of frontal epilepsy based on intracranial EEG. Frontiers in Neurology, 2021, 12: 718683..
11. Jansen N A, Perez C, Schenke M, et al. Impaired θ-γ coupling indicates inhibitory dysfunction and seizure risk in a dravet syndrome mouse model. Journal of Neuroscience, 2021, 41(3): 524-537..
12. Salimpour Y, Mills K A, Hwang B Y, et al. Phase-targeted stimulation modulates phase-amplitude coupling in the motor cortex of the human brain. Brain Stimulation, 2022, 15(1): 152-163..
13. Rampp S, Rössler K, Hamer H, et al. Dysmorphic neurons as cellular source for phase-amplitude coupling in focal cortical dysplasia type II. Clinical Neurophysiology, 2021, 132(3): 782-792..
14. Mihály I, Orbán-Kis K, Gáll Z, et al. Amygdala low-frequency stimulation reduces pathological phase-amplitude coupling in the pilocarpine model of epilepsy. Brain Sciences, 2020, 10(11): 856..
15. Shoeb A H. Application of machine learning to epileptic seizure onset detection and treatment. Cambridge: Massachusetts Institute of Technology, 2009: 157-162..
16. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 2004, 134(1): 9-21..
17. Chaumon M, Bishop D V, Busch N A. A practical guide to the selection of independent components of the electroencephalogram for artifact correction. Journal of Neuroscience Methods, 2015, 250: 47-63..
18. Tort A B, Komorowski R, Eichenbaum H, et al. Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. Journal of Neurophysiology, 2010, 104(2): 1195-1210..
19. Kullback S, Leibler R A. On information and sufficiency. The Annals of Mathematical Statistics, 1951, 22(1): 79-86..
20. Hülsemann M J, Naumann E, Rasch B. Quantification of phase-amplitude coupling in neuronal oscillations: comparison of phase-locking value, mean vector length, modulation index, and generalized-linear-modeling-cross-frequency-coupling. Frontiers in Neuroscience, 2019, 13: 573..
21. Canolty R T, Knight R T. The functional role of cross-frequency coupling. Trends in Cognitive Sciences, 2010, 14(11): 506-515..
22. van der Meij R, Kahana M, Maris E. Phase–amplitude coupling in human electrocorticography is spatially distributed and phase diverse. Journal of Neuroscience, 2012, 32(1): 111-123..
23. Schroeder C E, Lakatos P. Low-frequency neuronal oscillations as instruments of sensory selection. Trends in Neurosciences, 2009, 32(1): 9-18..
24. Amemiya S, Redish A D. Hippocampal theta-gamma coupling reflects state-dependent information processing in decision making. Cell Reports, 2018, 22(12): 3328-3338..
25. Köster M, Finger H, Graetz S, et al. Theta-gamma coupling binds visual perceptual features in an associative memory task. Scientific Reports, 2018, 8(1): 17688..
26. Liang W K, Tseng P, Yeh J R, et al. Frontoparietal beta amplitude modulation and its interareal cross-frequency coupling in visual working memory. Neuroscience, 2021, 460: 69-87..
27. Edakawa K, Yanagisawa T, Kishima H, et al. Detection of epileptic seizures using phase–amplitude coupling in intracranial electroencephalography. Scientific Reports, 2016, 6: 25422..
28. Guggisberg A G, Kirsch H E, Mantle M M, et al. Fast oscillations associated with interictal spikes localize the epileptogenic zone in patients with partial epilepsy. Neuroimage, 2008, 39(2): 661-668..
29. Lundstrom B N, Brinkmann B H, Worrell G A. Low frequency novel interictal EEG biomarker for localizing seizures and predicting outcomes. Brain Communications, 2021, 3(4): fcab231..

Journal of Biomedical Engineering

Alterations of β-γ coupling of scalp electroencephalography during epilepsy

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