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Coupling feature extraction method of resting state EEG Signals from amnestic mild cognitive impairment with type 2 diabetes mellitus based on weight permutation conditional mutual information

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Abstract

This study aimed to find a good coupling feature extraction method to effectively analyze resting state EEG signals (rsEEG) of amnestic mild cognitive impairment(aMCI) with type 2 diabetes mellitus(T2DM) and normal control (NC) with T2DM. A method of EEG signal coupling feature extraction based on weight permutation conditional mutual information (WPCMI) was proposed in this research. With the WPCMI method, coupling feature strength of two time series in Alpha1, Alpha2, Beta1, Beta2 and Gamma bands for aMCI with T2DM and NC with T2DM could be extracted respectively. Then selected three frequency bands coupling feature matrix with the help of multi-spectral image transformation method to map it as spectral image characteristics. And finally classified these characteristics through the convolution neural network method(CNN). For aMCI with T2DM and NC with T2DM, the highest classification accuracy of 96%, 95%, 95% could be achieved respectively in the combination of three frequency bands (Alpha1, Alpha2, Gamma), (Beta1, Beta2 and Gamma) and (Alpha2, Beta1, Beta2). This WPCMI method highlighted the coupling dynamic characteristics of EEG signals, and its classification performance was better than all previous methods in aMCI with T2DM diagnosis field. WPCMI method could be used as an effective biomarker to distinguish EEG signals of aMCI with T2DM and NC with T2DM. The coupling feature extraction method used in this paper provided a new perspective for the EEG analysis of aMCI with T2DM.

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References

  • Afshani F, Shalbaf A, Shalbaf R et al (2019) Frontal-temporal functional connectivity of EEG signal by standardized permutation mutual information during anesthesia. Cogn Neurodyn 13(6):531–540

    PubMed  PubMed Central  Google Scholar 

  • Andrzejak RG, Kreuz T (2011) Characterizing unidirectional couplings between point processes and flows. EPL (Europhys Lett) 96:50012

    Google Scholar 

  • Arkady Pikovsky MR, Kurths J (2003) Synchronization: A Universal Concept in Nonlinear Sciences. Cambridge University Press, Cambridge, p 411

    Google Scholar 

  • Babiloni C, Del PC, Lizio R, Marzano N, Infarinato F, Soricelli A, Salvatore E, Ferri R, Bonforte C, GJNoA. Tedeschi, (2014) Cortical sources of resting state electroencephalographic alpha rhythms deteriorate across time in subjects with amnesic mild cognitive impairment. Neurobiol Aging. 35(1):130–142

    PubMed  Google Scholar 

  • Babiloni C, Lizio R, Marzano N, Capotosto P, Soricelli A, Triggiani AI, Cordone S, Gesualdo L, Del Percio C (2016) Brain neural synchronization and functional coupling in Alzheimer’s disease as revealed by resting state EEG rhythms. Int J Psychophysiol 103:88–102

    PubMed  Google Scholar 

  • Bartolomei F, Wendling F, Bellanger JJ et al (2001) Neural networks involving the medial temporal structures in temporal lobe epilepsy. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 112(9):1746–1760

    CAS  Google Scholar 

  • Barnett L, Seth AK (2014) The MVGC multivariate Granger causality toolbox: a new approach to Granger-causal inference. J Neurosci Methods 223:50–68

    PubMed  Google Scholar 

  • Başar M, Duru A, Akan A. (2019). Investigation of Emotional Changes Using Features of EEG-Gamma Band and Different Classifiers. 2019 Medical Technologies Congress (TIPTEKNO), Izmir, Turkey.

  • Bashivan P, Rish I, Yeasin M, et al. (2016). Learning Representations from EEG with Deep Recurrent-Convolutional Neural Networks. International conference on learning representations.

  • Baskaran A, Milev R, Mcintyre RSJNDT (2013) A review of electroencephalographic changes in diabetes mellitus in relation to major depressive disorder. Neuropsychiatr Dis Treat 2013(9):143–150

    Google Scholar 

  • Bian Z, Li Q, Wang L, Lu C, Yin S, Li X (2014) Relative power and coherence of EEG series are related to amnestic mild cognitive impairment in diabetes. Front Aging Neurosci 6:11

    PubMed  PubMed Central  Google Scholar 

  • Brzezicka A, Kaminski M, Kaminski J et al (2011) Information transfer during a transitive reasoning task. Brain Topogr 24(1):1–8

    PubMed  Google Scholar 

  • Busse A, Hensel A, Gühne U, Angermeyer M (2006) Mild cognitive impairment: long-term course of four clinical subtypes. Neurol 67(12):2176

    CAS  Google Scholar 

  • Cantero JL, Atienza M, Cruz-Vadell A, Suarez-Gonzalez A, Gil-Neciga E (2009) Increased synchronization and decreased neural complexity underlie thalamocortical oscillatory dynamics in mild cognitive impairment. Neuroimage 46:938–948

    PubMed  Google Scholar 

  • Chai X, Weng X, Zhang Z, et al (2019) Quantitative EEG in mild cognitive impairment and alzheimer’s disease by AR-spectral and multi-scale entropy analysis. World Congr Med Phys Biomed Eng Singap 159–163

  • Chamanzar A, Shabany M, Malekmohammadi A et al (2017) Efficient hardware implementation of real-time low-power movement intention detector system using FFT and adaptive wavelet transform. IEEE Trans Biomed Circuits Syst 11(3):585–596

    PubMed  Google Scholar 

  • Cooray G, Nilsson E, Wahlin A, Brismar K, Brismar TJCN (2008) MO32 Effect of intensified metabolic control on cognitive performance and EEG in patients with type 2 diabetes. Clin Neurophysiol 119(08):S38–S38

    Google Scholar 

  • Cooray G, Nilsson E, Wahlin A, Laukka EJ, Brismar K, Brismar TJP (2011) Effects of intensified metabolic control on CNS function in type 2 diabetes. Psychoneuroendocrinol 36(1):77–86

    Google Scholar 

  • Cui D, Pu W, Liu J et al (2016) A new EEG synchronization strength analysis method: S-estimator based normalized weighted-permutation mutual information. Neural Netw 82(C):30–38

    PubMed  Google Scholar 

  • Cui D, Wang J, Bian Z (2015) Analysis of entropies based on empirical mode decomposition in amnesic mild cognitive impairment of diabetes mellitus. J Innov Opt Health Sci 8(5):1550010

    Google Scholar 

  • Darvas F, Ojemann JG, Sorensen LB (2009) Bi-phase locking—a tool for probing non-linear interaction in the human brain. Neuroimage 46:123–132

    CAS  PubMed  Google Scholar 

  • Dauwels J, Vialatte F, Cichocki AJCAR (2010) Diagnosis of Alzheimer’s disease from EEG signals: where are we standing? Curr Alzheimer Res 7(6):487–505

    CAS  PubMed  Google Scholar 

  • Deng B, Cai L, Li S et al (2017) Multivariate multi-scale weighted permutation entropy analysis of EEG complexity for Alzheimer’s disease. Cogn Neurodyn 11(3):217–231

    PubMed  Google Scholar 

  • Faes L, Erla S, Nollo G (2012) Measuring connectivity in linear multivariate processes: definitions, interpretation, and practical analysis. Comput Math Methods Med 2012:140513

    PubMed  PubMed Central  Google Scholar 

  • Faes L, Marinazzo D, Nollo G et al (2016) An Information-Theoretic Framework to Map the Spatiotemporal Dynamics of the Scalp Electroencephalogram. IEEE Trans Biomed Eng 63(12):2488–2496

    PubMed  Google Scholar 

  • Faes L, Nollo G, Porta A (2011) Information-based detection of nonlinear Granger causality in multivariate processes via a nonuniform embedding technique. Phys Rev E Stat Nonlin Soft Matter Phys 83:051112

    PubMed  Google Scholar 

  • Faes L, Porta A, Nollo G (2008) Mutual nonlinear prediction as a tool to evaluate coupling strength and directionality in bivariate time series: comparison among different strategies based on k nearest neighbors. Phys Rev E Stat Nonlin Soft Matter Phys 78:026201

    PubMed  Google Scholar 

  • Frenzel S, Pompe B (2007) Partial mutual information for coupling analysis of multivariate time series. Phys Rev Lett 99:204101

    PubMed  Google Scholar 

  • Ganguli M, Dodge H, Shen C, DeKosky S (2004) Mild cognitive impairment, amnestic type An epidemiologic study. Neurol 63(1):115

    Google Scholar 

  • Gispen WH, Biessels G-J (2000) Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci 23(11):542–549

    CAS  PubMed  Google Scholar 

  • Granger CWJ (1969) Investigating causal relations by econometric models and cross-spectral methods. Econometrica 37:15

    Google Scholar 

  • Hejazi M (2019) Prediction of epilepsy seizure from multi-channel electroencephalogram by effective connectivity analysis using Granger causality and directed transfer function methods. Cogn Neurodyn 13(5):461–473

    PubMed  PubMed Central  Google Scholar 

  • Shimada H, Miki T, Tamura A, Ataka S (2010) Neuropsychological status of elderly patients with diabetes mellitus. Diabet Res Clin Pract 87(3):224–227

    Google Scholar 

  • Huo Y (2015) A novel face recognition algorithm based on the multi-dimensional algorithm. Harbin University of Science and Technology, Harbin

    Google Scholar 

  • Hussain HJN (2007) Conversion from subtypes of mild cognitive impairment to Alzheimer dementia. Neurol 68(4):288–291

    Google Scholar 

  • Jin J, Xiao R, Daly I et al (2020) Internal feature selection method of CSP based on L1-Norm and Dempster-Shafer Theory. Trans Neural Netw Learning Syst. https://doi.org/10.1109/TNNLS.2020.3015505

    Article  Google Scholar 

  • Katarzyn J, Blinowska JZ (2010) Practical biomedical signal analysis using MATLAB. CRC Press, USA

    Google Scholar 

  • Knyazeva MG, Carmeli C, Khadivi A, Ghika J, Meuli R, Frackowiak RS (2013) Evolution of source EEG synchronization in early Alzheimer’s disease. Neurobiol Aging. 34(3):694–705

    PubMed  Google Scholar 

  • Kurths, A. P. M. R. J. (2003). Synchronization: A Universal Concept in Nonlinear Sciences. Cambridge Nonlinear Science Series (Vol. 12): Cambridge University Press.

  • Li X, Ouyang G (2010) Estimating coupling direction between neuronal populations with permutation conditional mutual information. Neuroimage 52:497–507

    PubMed  Google Scholar 

  • Li X, Yan Y, Wei W (2013) Identifying Patients with Poststroke Mild Cognitive Impairment by Pattern Recognition of Working Memory Load-Related ERP. Comput Math Methods Med. https://doi.org/10.1155/2013/658501

    Article  PubMed  PubMed Central  Google Scholar 

  • Luchsinger JA, Reitz C, Patel B, Tang MX, Manly JJ, Mayeux R (2007) Relation of diabetes to mild cognitive impairment. Arch Neurol. 64(4):570–575

    PubMed  Google Scholar 

  • Miao Y, Yin E, Allison BZ et al (2020) An ERP-based BCI with peripheral stimuli: validation with ALS patients. Cogn Neurodyn 14:21–33

    PubMed  Google Scholar 

  • Rosenblum MG, Pikovsk AS, Kurths J (1995) Phase synchronization of chaotic oscillators. Phys Rev Lett 76:4

    Google Scholar 

  • Moretti DV, Frisoni GB, Pievani M, Rosini S, Geroldi C, Binetti G et al (2008) Cerebrovascular disease and hippocampal atrophy are differently linked to functional coupling of brain areas: an EEG coherence study in MCI subjects. J Alzheimer’s Dis 14:28–99

    Google Scholar 

  • Muller A, Kraemer JF, Penzel T, Bonnemeier H, Kurths J, Wessel N (2016) Causality in physiological signals. Physiol Meas 37:R46-72

    PubMed  Google Scholar 

  • Palus M (1994) Coarse-grained entropy rates for characterization of complex time series. Physica D: Nonlinear Phenom 93(12):64–77

    Google Scholar 

  • Palus M, Komarek V, Hrncir Z, Sterbova K (2001) Synchronization as adjustment of information rates: detection from bivariate time series. Phys Rev E Stat Nonlin Soft Matter Phys 63:046211

    CAS  PubMed  Google Scholar 

  • Palus M, Stefanovska A (2003) Direction of coupling from phases of interacting oscillators: an information-theoretic approach. Phys Rev E Stat Nonlin Soft Matter Phys 67:055201

    PubMed  Google Scholar 

  • Pikovsky AS (1983) On the interaction of strange attractors. Condensed Matte 55:6

    Google Scholar 

  • Roberts R, Knopman D, Geda Y (2014) Association of diabetes with amnestic and nonamnestic mild cognitiveimpairment. Alzheimers Dement 10(1):18–26

    PubMed  Google Scholar 

  • Romero-Garcia R, Atienza M, Cantero JL (2014) Predictors of coupling between structural and functional cortical networks in normal aging. Hum Brain Mapp 35:2724–2740

    PubMed  Google Scholar 

  • Rudrauf D, Douiri A, Kovach C, Lachaux JP, Cosmelli D, Chavez M, Adam C, Renault B, Martinerie J, Le Van Quyen M (2006) Frequency flows and the time-frequency dynamics of multivariate phase synchronization in brain signals. Neuroimage 31:209–227

    PubMed  Google Scholar 

  • Rulkov NF, Sushchik MM, Tsimring LS, Abarbanel HDI (1995) Generalized synchronization of chaos in directionally coupled chaotic systems. Phys Rev E 51:980–994

    CAS  Google Scholar 

  • Schreiber T (2000) Measuring information transfer. Phys Rev Lett 85:4

    Google Scholar 

  • Seth AK (2010) A MATLAB toolbox for Granger causal connectivity analysis. J Neurosci Methods 186:262–273

    PubMed  Google Scholar 

  • Shoback and Dolores (2011) Greenspan’s basic and clinical endocrinology, 9th edn. McGraw-Hill Medical, NewYork

    Google Scholar 

  • Stam CJ, Jones BF, Nolte G, Breakspear M, Scheltens P (2007) Small-world networks and functional connectivity in Alzheimer’s disease. Cereb Cortex 17:92–99

    CAS  PubMed  Google Scholar 

  • Steriade M (2006) Grouping of brain rhythms in corticothalamic systems. Neurosci 137(4):1087–1106

    CAS  Google Scholar 

  • Strachan MW, Reynolds RM, Marioni RE, Price JF (2011) Cognitive function, dementia and type 2 diabetes mellitus in the elderly. Nat Rev Endocrinol 7(2):108–114

    CAS  PubMed  Google Scholar 

  • Stuart L, Walter M, Borisyuk R (2005) The correlation grid: analysis of synchronous spiking in multi-dimensional spike train data and identification of feasible connection architectures. Biosyst 79:223–233

    CAS  Google Scholar 

  • Sun J, Bollt EM (2014) Causation entropy identifies indirect influences, dominance of neighbors and anticipatory couplings. Physica D 267:49–57

    Google Scholar 

  • Sun H, Jin J, Kong W et al (2020) Novel channel selection method based on position priori weighted permutation entropy and binary gravity search algorithm. Cogn Neurodyn 15(1):114–156

    Google Scholar 

  • Tao H, Tian X. (2006). Coherence Characteristics of Gamma-band EEG during rest and cognitive task in MCI and AD. 2005 IEEE Engineering in Medicine and Biology 27th Annual Conference, pp 2747–2750, Shanghai, China.

  • Terry JR, Breakspear M (2003) An improved algorithm for the detection of dynamical interdependence in bivariate time-series. Biol Cybern 88:129–136

    PubMed  Google Scholar 

  • Vecchio F, Babiloni C (2011) Direction of Information Flow in Alzheimer’s Disease and MCI Patients. Int J Alzheimers Dis 2011:214580

    PubMed  PubMed Central  Google Scholar 

  • Wen D, Bian Z, Li Q et al (2016) Resting-state EEG coupling analysis of amnestic mild cognitive impairment with type 2 diabetes mellitus by using permutation conditional mutual information. Clin Neurophysiol 127(1):335–348

    PubMed  Google Scholar 

  • Wen D, Xue Q, Lu C (2014) A global coupling index of multivariate neural series with application to the evaluation of mild cognitive impairment. Neural Netw 56:1–9

    PubMed  Google Scholar 

  • Wen D, Yuan J, Zhou Y et al (2020a) The EEG Signal Analysis for Spatial Cognitive Ability Evaluation Based on Multivariate Permutation Conditional Mutual Information-Multi-Spectral Image. IEEE Trans Neural Syst Rehabil Eng 28(10):2113–2122

    PubMed  Google Scholar 

  • Wen D, Zhou Y, Li P et al (2020b) Resting-state EEG Signal Classification of Amnestic Mild Cognitive Impairment with Type 2 Diabetes Mellitus based on Multispectral Image and Convolutional Neural Network. J Neural Eng 17:036005

    PubMed  Google Scholar 

  • White DJ, Congedo M, Ciorciari J, Silberstein RB (2012) Brain oscillatory activity during spatial navigation: theta and gamma activity link medial temporal and parietal regions. J Cognitive Neurosci 24(3):686–697

    Google Scholar 

  • Winterhalder M, Schelter B, Hesse W, Schwab K, Leistritz L, Timmer J, Witte H (2006) Detection of directed information flow in biosignals. Biomed Tech (Berl) 51:281–287

    Google Scholar 

  • Yaffe K, Petersen R, Lindquist K, Kramer J (2006) Subtype of mild cognitive impairment and progression to dementia and death. Dement Geriatr Cogn Disord 22:312–319

    PubMed  Google Scholar 

  • Zhang X, Jin J, Li S et al (2021) Evaluation of color modulation in visual P300-speller using new stimulus patterns. Cogn Neurodyn. https://doi.org/10.1007/s11571-021-09669-y

    Article  PubMed  Google Scholar 

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Acknowledgment

This research was funded by National Natural Science Foundation of China (61876165, 61503326), Natural Science Foundation of Hebei Province in China (F2016203343), China Postdoctoral Science Foundation (2015M581317). The authors have no any potential conflicts.

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Liu, Y., Xu, X., Zhou, Y. et al. Coupling feature extraction method of resting state EEG Signals from amnestic mild cognitive impairment with type 2 diabetes mellitus based on weight permutation conditional mutual information. Cogn Neurodyn 15, 987–997 (2021). https://doi.org/10.1007/s11571-021-09682-1

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