Abstract
Frequency coupling in nervous system is believed to be associated with normal and impaired brain functions. However, most of the existing experiments have been concentrated on the coupling strength within frequency bands, while the coupling strength between different bands is ignored. In this work, we apply phase synchronization index (PSI) to investigate the cross-frequency coupling (CFC) of Electroencephalogram (EEG) signals. The PSI matrixes for the multi-channel EEG signals are calculated from interictal to ictal period in each sliding time window. The results show that CFC changes obviously once seizure occurs between the different bands, and such alteration is earlier than the appearance of clinical symptoms in seizure. Considering the similar role of the within-frequency coupling (WFC), we further reconstruct multi-layered brain networks, including CFC networks and WFC networks. The graph metrics are applied to investigate the variation of network structure of the epileptic brain. Significant decreases/increases of the local/global efficiency are found in δ–β, δ–α, θ–α and δ–θ bands from the CFC network, while WFC network shows a significant decline in the local efficiency in θ and α bands. These findings suggest that CFC may provide a new perspective to observe the alteration of brain structure when seizure occurs, and the investigation of functional connectivity across the full frequency spectrum can give us a deeper understanding of epileptic brains.
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References
Abasolo D, Hornero R, Espino P, Poza J, Sanchez CI, de la Rosa R (2005) Analysis of regularity in the EEG background activity of Alzheimer’s disease patients with approximate entropy. Clin Neurophysiol 116(8):1826–1834
Adebimpe A, Aarabi A, Bourel-Ponchel E, Mahmoudzadeh M, Wallois F (2016) EEG resting state functional connectivity analysis in children with benign epilepsy with centrotemporal spikes. Front Neurosci 10:143
Amiri M, Frauscher B, Gotman J (2016) Phase–amplitude coupling is elevated in deep sleep and in the onset zone of focal epileptic seizures. Front Hum Neurosci 10:387
Apkarian AV, Bushnell MC, Treede RD, Zubieta JK (2005) Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 9(4):463–484
Belluscio MA, Mizuseki K, Schmidt R, Kempter R et al (2012) Cross-frequency phase–phase coupling between θ and γ oscillations in the hippocampus. J Neurosci 32(2):423–435
Benbadis SR, Allen Hauser W (2000) An estimate of the prevalence of psychogenic non-epileptic seizures. Seizure 9(4):280–281
Benedek M, Bergner S, Koenen T, Fink A, Neubauer AC (2011) EEG α synchronization is related to top-down processing in convergent and divergent thinking. Neuropsychologia 49(12):3505–3511
Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34(4):537–541
Buckner RL, Sepulcre J, Talukdar T et al (2009) Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer’s disease. J Neurosci 29(6):1860–1873
Cai LH, Wei XL, Wang J, Yu HT, Deng B, Wang R (2018) Reconstruction of functional brain network in Alzheimer’s disease via cross-frequency phase synchronization. Neurocomputing 314:490–500
Canolty RT, Knight RT (2010) The functional role of cross-frequency coupling. Trends Cogn Sci 14(11):506–515
Donos C, Dumpelmann M, Schulze-Bonhage A (2015) Early seizure detection algorithm based on intracranial EEG and random forest classification. Int J Neural Syst 25(5):1550023
Edakawa K, Yanagisawa Kishima H, Fukuma R, Oshino S, Khoo HM et al (2016) Detection of epileptic seizures using phase–amplitude coupling in intracranial electroencephalography. Sci Rep 6:25422
Englot DJ, Gonzalez HFJ, Reynolds BB, Konrad PE, Jacobs ML, Gore JC, Landman BA, Morgan VL (2018) Relating structural and functional brainstem connectivity to disease measures in epilepsy. Neurology 91:e67–e77
Fraga FJ, Falk TH, Kanda PA, Anghinah R (2013) Characterizing Alzheimer’s disease severity via resting-awake EEG amplitude modulation analysis. PLoS ONE 8(8):e72240
Greter H, Mmbando B, Makunde W, Mnacho M, Matuja W, Kakorozya A, Suykerbuyk P, Colebunders R (2018) Evolution of epilepsy prevalence and incidence in a Tanzanian area endemic for onchocerciasis and the potential impact of community-directed treatment with ivermectin: a cross-sectional study and comparison over 28 years. BMJ Open 8(3):e017188
Guirgis M, Chinvarun Y, del Campo M, Carlen PL, Bardakjian BL (2015) Defining regions of interest using cross-frequency coupling in extratemporal lobe epilepsy patients. J Neural Eng 12(2):026011
Hortal E, Ubeda A, Ianez E, Azorin JM, Fernandez E (2016) EEG-based detection of starting and stopping during gait cycle. Int J Neural Syst 26(7):1650029
Iasemidis LD, Shiau DS, Chaovalitwongse W et al (2003) Adaptive epileptic seizure prediction system. IEEE Trans Biomed Eng 50(5):616–627
Ibrahim GM, Wong SM, Anderson RA et al (2014) Dynamic modulation of epileptic high frequency oscillations by the phase of slower cortical rhythms. Exp Neurol 251:30–38
Jacobs D, Hilton T, del Campo M, Carlen PL, Bardakjian BL (2018) Classification of pre-clinical seizure states using scalp EEG cross-frequency coupling features. IEEE Trans Biomed Eng 65(11):2440–2449
Jeong W, Jin SH, Kim M, Kim JS, Chung CK (2014) Abnormal functional brain network in epilepsy patients with focal cortical dysplasia. Epilepsy Res 108(9):1618–1626
Jiang YZ, Wu DR, Deng ZH et al (2017) Seizure classification from EEG signals using transfer learning, semi-supervised learning and TSK fuzzy system. IEEE Trans Neural Syst Rehabil Eng 25(12):2270–2284
Kannathal N, Choo ML, Acharya UR et al (2005) Entropies for detection of epilepsy in EEG. Comput Methods Programs Biomed 80(3):187–194
Kim HJ, Lee JH, Park CH, Hong HS, Choi YS, Yoo JH, Lee HW (2018) Role of language-related functional connectivity in patients with benign childhood epilepsy with centrotemporal spikes. J Clin Neurol 14:48–57
Kirmani BF (2013) Importance of video-EEG monitoring in the diagnosis of epilepsy in a psychiatric patient. Case Rep Neurol Med 2013:159842
Liao W, Zhang Z, Pan Z et al (2010) Altered functional connectivity and small-world in mesial temporal lobe epilepsy. Epilepsy Res 137:45–52
Lo JT (2010) Functional model of biological neural networks. Cogn Neurodyn 4(4):295–313
Malladi R, Johnson DH, Kalamangalam GP, Tandon N, Aazhang B (2018) Mutual information in frequency and its application to measure cross-frequency coupling in epilepsy. IEEE Trans Signal Process 66(11):3008–3023
Martis RJ, Acharya UR, Tan JH et al (2013) Application of intrinsic time-scale decomposition (ITD) to EEG signals for automated seizure prediction. Int J Neural Syst 23(5):1350023
Medvedev AV, Murro AM, Meador KJ (2011) Abnormal interictal gamma activity may manifest a seizure onset zone in temporal lobe epilepsy. Int J Neural Syst 21(2):103–114
Mormann F, Lehnertz K, David P, Elger CE (2000) Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Physica D 144(3–4):358–369
Müller V, Perdikis D, Oertzen TV et al (2016) Structure and topology dynamics of hyper-frequency networks during rest and auditory oddball performance. Front Comput Neurosci 10:108
Nariai H, Matsuzaki N, Juhasz C et al (2011) Ictal high-frequency oscillations at 80–200 Hz coupled with δ phase in epileptic spasms. Epilepsia 52(10):e130–e134
Nishida H, Takahashi M, Lauwereyns J (2014) Within-session dynamics of θ-gamma coupling and high-frequency oscillations during spatial alternation in rat hippocampal area CA1. Cogn Neurodyn 8(5):363–372
Ortega GJ, Menendez de la Prida L, Sola RG, Pastor J (2008) Synchronization clusters of interictal activity in the lateral temporal cortex of epileptic patients: intraoperative electrocorticographic analysis. Epilepsia 49(2):269–280
Palva JM, Palva S (2018) Functional integration across oscillation frequencies by cross-frequency phase synchronization. Eur J Neurosci 48(7):2399–2406
Percha B, Dzakpasu R, Zochowski M, Parent J (2005) Transition from local to global phase synchrony in small world neural network and its possible implications for epilepsy. Phys Rev E Stat Nonlinear Soft Matter Phys 72(3 Pt 1):031909
Ponten SC, Bartolomei F, Stam CJ (2007) Small-world networks and epilepsy: graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures. Clin Neurophysiol 118(4):918–927
Ponten SC, Douw L, Bartolomei F, Reijneveld JC, Stam CJ (2009) Indications for network regularization during absence seizures: weighted and unweighted graph theoretical analyses. Exp Neurol 217(1):197–204
Qu J, Wang R, Du Y, Cao J (2012) Synchronization study in ring-like and grid-like neuronal networks. Cogn Neurodyn 6(1):21–31
Reijneveld JC, Ponten SC, Berendse HW, Stam CJ (2007) The application of graph theoretical analysis to complex networks in the brain. Clin Neurophysiol 118(11):2317–2331
Rogasch NC, Fitzgerald PB (2013) Assessing cortical network properties using TMS-EEG. Hum Brain Mapp 34(7):1652–1669
Roper SN, Yachnis AT (2002) Cortical dysgenesis and epilepsy. Neuroscientist 8(4):356–371
Salvador R, Suckling J, Schwarzbauer C, Bullmore E (2005) Undirected graphs of frequency-dependent functional connectivity in whole brain networks. Philos Trans R Soc Lond B Biol Sci 360(1457):937–946
Samiee S, Levesque M, Avoli M, Baillet S (2018) Phase-amplitude coupling and epileptogenesis in an animal model of mesial temporal lobe epilepsy. Neurobiol Dis 114:111–119
Song J, Nair VA, Gaggl W, Prabhakaran V (2015) Disrupted brain functional organization in epilepsy revealed by graph theory analysis. Brain Connect 5(5):276–283
Srinivas KV, Jain R, Saurav S, Sikdar SK (2007) Small-world network topology of hippocampal neuronal network is lost, in an in vitro glutamate injury model of epilepsy. Eur J Neurosci 25(11):3276–3286
Szymanski C, Pesquita A, Brennan AA et al (2017) Teams on the same wavelength perform better: inter-brain phase synchronization constitutes a neural substrate for social facilitation. Neuroimage 152:425–436
Tecchio F, Cottone C, Porcaro C, Cancelli A, Di Lazzaro V, Assenza G (2018) Brain functional connectivity changes after transcranial direct current stimulation in epileptic patients. Front Neural Circuits 12:44
Tetzlaff R, Kunz R, Niederhofer C (2003) Cellular neural networks (CNN) with linear weight functions for a prediction of epileptic seizures. Int J Neural Syst 13(6):489–498
Thuraisingham RA, Tran Y, Craig A et al (2012) Frequency analysis of eyes open and eyes closed EEG signals using the Hilbert-Huang transform. IEEE Eng Med Biol Soc 2012:2865–2868
Villa AE, Tetko IV (2010) Cross-frequency coupling in mesiotemporal EEG recordings of epileptic patients. J Physiol Paris 104(3–4):197–202
Wacker M, Witte H (2011) On the stability of the n:m phase synchronization index. IEEE Trans Biomed Eng 58(2):332–338
Wang B, Meng L (2016) Functional brain network alterations in epilepsy: a magnetoencephalography study. Epilepsy Res 126:62–69
Weiss SA, Banks GP, McKhann GM Jr et al (2013) Ictal high frequency oscillations distinguish two types of seizure territories in humans. Brain 136(Pt 12):3796–3808
Weiss SA, Orosz I, Salamon N et al (2016) Ripples on spikes show increased phase-amplitude coupling in mesial temporal lobe epilepsy seizure-onset zones. Epilepsia 57(11):1916–1930
Yuan SS, Zhou WD, Chen LY (2018) Epileptic seizure prediction using diffusion distance and bayesian linear discriminate analysis on intracranial EEG. Int J Neural Syst 28(1):1750043
Zhang Y, Zhou W, Yuan S et al (2015) Seizure detection method based on fractal dimension and gradient boosting. Epilepsy Behav 43:30–38
Zheng CG, Zhang T (2013) Alteration of phase-phase coupling between θ and gamma rhythms in a depression-model of rats. Cogn Neurodyn 7(2):167–172
Acknowledgements
This work is supported by Tianjin Municipal Natural Science Foundation under Grants 13JCZDJC27900, Tangshan Science and Technology Planning Project (Grant No. 18130208A), and Key Research and Development Program Project of Hebei Province (Grant No. 18277773D). This work is also supported by the National Natural Science Foundation of China (Grant No. 61701336), the Natural Science Foundation of Tianjin, China (Grant No. 17JCQNJC00800) and the funding of Hong Kong Scholars Programs (Grant No. XJ2016006). The authors also gratefully acknowledge the financial support provided by Opening Fundation of Key Laboratory of Opto-technology and Intelligent Control (Lanzhou Jiaotong University), Ministry of Education (KFKT 2018-5).
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Yu, H., Zhu, L., Cai, L. et al. Variation of functional brain connectivity in epileptic seizures: an EEG analysis with cross-frequency phase synchronization. Cogn Neurodyn 14, 35–49 (2020). https://doi.org/10.1007/s11571-019-09551-y
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DOI: https://doi.org/10.1007/s11571-019-09551-y