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Complex network based models of ECoG signals for detection of induced epileptic seizures in rats

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Abstract

The automatic detection of seizures bears a considerable significance in epileptic diagnosis as it can efficiently lead to a considerable reduction of the workload of the medical staff. The present study aims at automatic detecting epileptic seizures in epileptic rats. To this end, seizures were induced in rats implementing the pentylenetetrazole model, with the electrocorticogram (ECoG) signals during, before and after the seizure periods being recorded. For this purpose, five algorithms for transforming time series into complex networks based on visibility graph (VG) algorithm were used. In this study, VG based methods were used for the first time to analyze ECoG signals in rats. Afterward, Standard measures in network science (graph properties) were made to examine the topological structure of these networks produced on the basis of ECoG signals. Then these measures were given to a classifier as input features so that the ECoG signals could be classified into seizure periods and seizure-free periods. Artificial Neural Network, considered a popular classifier, was used in this work. The experimental results showed that the method managed to detect epileptic seizure in rats with a high accuracy of 92.13%. Our proposed method was also applied to the recorded EEG signals from Bonn database to show the efficiency of the proposed method for human seizure detection.

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References

  • Abarbanel HDI, Brown R, Sidorowich JJ, Tsimring LS (1993) The analysis of observed chaotic data in physical systems. Rev Mod Phys 65:1331. https://doi.org/10.1103/RevModPhys.65.1331

    Article  Google Scholar 

  • Acharya UR, Sree SV, Suri JS (2011a) Automatic detection of epileptic EEG signals using higher ordercumulant features. Int J Neural Syst 21(5):403–414

    Article  PubMed  Google Scholar 

  • Acharya UR, Sree SV, Chattopadhyay S, Yu W, Ang PC (2011b) Application of recurrence quantification analysis for the automated identification of epileptic EEG signals. Int J Neural Syst 21(3):199–211

    Article  PubMed  Google Scholar 

  • Adeli H, Zhou Z, Dadmehr N (2003) Analysis of EEG records in an epileptic patient using wavelet transform. J Neurosci Methods 123(1):69–87

    Article  PubMed  Google Scholar 

  • Adeli H, Ghosh-Dastidar S, Dadmehr N (2007) A wavelet-chaos methodology for analysis of EEGs and EEG subbands to detect seizure and epilepsy. IEEE Trans Biomed Eng 54(2):205–211

    Article  PubMed  Google Scholar 

  • Ahadpour S, Sadra Y, ArastehFard Z (2014) Markov-binary visibility graph: a new method for analyzing complex systems. Inf Sci 274:286–302

    Article  Google Scholar 

  • Ahmadlou M, Adeli H, Adeli A (2010) New diagnostic EEG markers of the Alzheimer’s disease using visibility graph. J Neural Transm 117(9):1099–1109

    Article  PubMed  Google Scholar 

  • Asadi F, Mollakazemi MJ, Atyabi SA, Uzelac I, Ghaffari A (2015) Cardiac arrhythmia recognition with robust discrete wavelet-based and geometrical feature extraction via classifiers of SVM and MLP-BP and PNN neural networks. In: IEEE conference publications on 2015 computing in cardiology conference (CinC). https://doi.org/10.1109/cic.2015.7411065

  • Asvestas P, Matsopoulos GK, Nikita KS (1999) Estimation of fractal dimension of images using a fixed mass approach. Pattern Recognit Lett 20(3):347–354

    Article  Google Scholar 

  • Bergstrom RA, Choi JH, Manduca A, Shin HS, Worrell GA, Howe CL (2013) Automated identification of multiple seizure-related and interictalepileptiform event types in the EEG of mice. Sci Rep 3:1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Besio WG, Liu X, Liu Y, Sun YL, Medvedev AV, Koka K (2011) Algorithm for automatic detection of pentylenetetrazole-induced seizures in rats. Conf Proc IEEE Eng Med Biol Soc 2011:8283–8286

    CAS  PubMed  Google Scholar 

  • Bezsudnov IV, Snarskii AA (2014) From the time series to the complex networks: the parametric natural visibility graph. Physica A 414:53–60

    Article  Google Scholar 

  • Buteneers P, Verstraetena D, van Mierlo P, Wyckhuys T, Stroobandt D, Raedt R, Hallez H, Schrauwena B (2011) Automatic detection of epileptic seizures on the intra-cranial electroencephalogram of rats using reservoir computing. Artif Intell Med 53(3):215–223

    Article  PubMed  Google Scholar 

  • Chawla NV, Japkowicz N, Kotcz A (2004) Editorial: special issue on learning from imbalanced data sets. ACM SIGKDD Explor Newslett 6(1):1–6. https://doi.org/10.1145/1007730.1007733

    Article  Google Scholar 

  • Chua CK, Chandran V, Acharya RU, Mi LCh (2009) Cardiac health diagnosis using higher order spectra and support vector machine. Open Med Inform J 3:1–8

    Article  PubMed  PubMed Central  Google Scholar 

  • Chua KC, Chandran V, Acharya UR, Lim CM (2011) Application of higher order spectra to identify epileptic EEG. J Med Syst 35(6):1563–1571

    Article  PubMed  Google Scholar 

  • Danober L, Deransart C, Depaulis A, Vergne M, Marescaux C (1998) Pathophysiological mechanisms of genetic absence epilepsy in the rat. Prog Neurobiol 55(1):27–57

    Article  CAS  PubMed  Google Scholar 

  • De Deyn PP, D’Hooge R, Marescau B, Pei YQ (1992) Chemical models of epilepsy with some reference to their applicability in the development of anticonvulsants. Epilepsy Res 12(2):87–110

    Article  PubMed  Google Scholar 

  • Dedeurwaerdere S (2005) Neuromodulation in experimental animal models of epilepsy. In: PhD thesis. Ghent University, Ghent

  • del Sol A, Fujihashi H, Amoros D, Nussinov R (2006) Residues crucial for maintaining short paths in network communication mediate signaling in proteins. Mol Syst Biol. https://doi.org/10.1038/msb4100063

    Article  PubMed  PubMed Central  Google Scholar 

  • Donner RV, Small M, Donges JF, Marwan N, Zou Y, Xiang R, Kurths J (2011) Recurrence-based time series analysis by means of complex network methods. Int J Bifurc Chaos 21(4):1019–1046

    Article  Google Scholar 

  • Fanselow EE, Reid AP, Nicolelis MA (2000) Reduction of pentylenetetrazole-induced seizure activity in awake rats by seizure-triggered trigeminal nerve stimulation. J Neurosci 20(21):8160–8168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feltane A, Faye Boudreaux-Bartels G, Besio W (2013) Automatic seizure detection in rats using Laplacian EEG and verification with human seizure signals. Ann Biomed Eng 41(3):645–654

    Article  PubMed  Google Scholar 

  • Firpi H, Goodman ED, Echuaz J (2007) Epileptic seizure detection using genetically programmed artificial features. IEEE Trans Biomed Eng 54(2):212–224

    Article  PubMed  Google Scholar 

  • Gotman J, Gloor P (1976) Automatic recognition and quantification of interictal epileptic activity in the human scalp EEG. Electroencephalogr Clin Neurophysiol 41(5):513–529

    Article  CAS  PubMed  Google Scholar 

  • Gutin G, Mansour T, Severini S (2011) A characterization of horizontal visibility graphs and combinatorics on words. Physica A 390(12):2421–2428

    Article  CAS  Google Scholar 

  • Harreby KR, Sevcencu C, Struijik JJ (2011) Early seizure detection in rats based on vagus nerve activity. Med Biol Eng Comput 49(2):143–151

    Article  PubMed  Google Scholar 

  • Higuchi T (1988) Approach to an irregular time series on the basis of the fractal theory. Physica D 31(2):277–283

    Article  Google Scholar 

  • Institute of Medical Biometry, Informatics and Epidemiology of the “MedizinischeEinrichtungen der Universität Bonn”: http://www.meb.uni-bonn.de/epileptology/science/physik/eeg.data.html

  • Kabir E, Siuly S, Cao J, Wang H (2018) A computer aided analysis scheme for detecting epileptic seizure from EEG data. Int J Comput Intell Syst 11(1):663–671

    Article  Google Scholar 

  • Katz MJ (1988) Fractals and the analysis of waveforms. Comput Biol Med 18(3):145–156

    Article  CAS  PubMed  Google Scholar 

  • Kelwade JP, Salankar SS (2016) Comparative study of neural networks for prediction of cardiac arrhythmias. In: 2016 International conference on automatic control and dynamic optimization techniques (ICACDOT). https://doi.org/10.1109/icacdot.2016.7877749

  • Kim J, Wilhelm T (2008) What is a complex graph? Physica A 387(11):2637–2652

    Article  Google Scholar 

  • Klioueva IA, van Luijtelaar EL, Chepurnova NE, Chepurnov SA (2001) PTZ-induced seizures in rats: effects of age and strain. Physiol Behav 72(3):421–426

    Article  CAS  PubMed  Google Scholar 

  • Kristiansen K, Courtois G (1949) Rhythmic electrical activity from isolated cerebral cortex. Electroencephalogr Clin Neurophysiol 1(3):265–272

    Article  CAS  PubMed  Google Scholar 

  • Kudo M, Sklansky J (2000) Comparison of algorithms that select features for pattern classifiers. Pattern Recognit 33(1):25–41

    Article  Google Scholar 

  • Lacasa L, Toral R (2010) Description of stochastic and chaotic series using visibility graphs. Phys Rev E 82:036120

    Article  CAS  Google Scholar 

  • Lacasa L, Luque B, Ballesteros F, Luque J, Nuno JC (2008) From time series to complex networks: the visibility graph. Natl Acad Sci USA 105(13):4972–4975

    Article  CAS  Google Scholar 

  • Lacasa L, Luque B, Nuno JC, Luque J (2009) The visibility graph: a new method for estimating the Hurst exponent of fractional Brownian motion. EPL (Europhys Lett) 86(3):30001

    Article  CAS  Google Scholar 

  • Lacasa L, Nunez AM, Roldan E, Parrondo JMR, Luque B (2012) Time series irreversibility: a visibility graph approach. Eur Phys J B 85:1–12. https://doi.org/10.1140/epjb/e2012-20809-8

    Article  Google Scholar 

  • Last M, Kandel A, Maimon O (2001) Information-theoretic algorithm for feature selection. Pattern Recognit Lett 22(6–7):799–811

    Article  Google Scholar 

  • Lenjani M, Hashemi MR (2009) A novel arbitration scheme for bandwidth and jitter guarantees in asynchronous NoCs. In: 2009 14th international CSI computer conference. https://doi.org/10.1109/csicc.2009.5349426

  • Lenjani M, Hashemi MR (2014) Tree-based scheme for reducing shared cache miss rate lever aging regional, statistical and temporal similarities. IET Comput Digital Tech 8(1):30–48

    Article  Google Scholar 

  • Loscher W, Schmidt D (1988) Which animal models should be used in the search for new antiepileptic drugs? A proposal based on experimental and clinical considerations. Epilepsy Res 2(3):145–181

    Article  CAS  PubMed  Google Scholar 

  • Luque B, Lacasa L, Balleteros F, Luque J (2009) Horizontal visibility graphs: exact results for random time series. Phys Rev E 80:046103

    Article  CAS  Google Scholar 

  • Luque B, Lacasa L, Ballesteros FJ, Robledo A (2011) Feigenbaum graphs: a complex network perspective of chaos. PLoS One 6:e22411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makeyev O, Liu X, Luna-Munguía H, Rogel-Salazar G, Mucio-Ramirez S, Liu Y, Sun YL, Kay SM, Besio WG (2012a) Toward a noninvasive automatic seizure control system in rats with transcranial focal stimulations via tripolar concentric ring electrodes. IEEE Trans Neural Syst Rehabil Eng 20(4):422–431

    Article  PubMed  PubMed Central  Google Scholar 

  • Makeyev O, Liu X, Luna-Munguia H, Rogel-Salazar G, Mucio-Ramirez S, Liu Y, Sun YL, Kay SM, Besio WG (2012) Toward an automatic seizure control system in rats through transcranial focal stimulation via tripolar concentric ring electrodes. In: Proceedings of 65th annual meeting of the American epilepsy society, vol 12, pp 29–30

  • Mirski MA, Tsai YC, Rossell LA, Thakor NV, Sherman DL (2003) Anterior thalamicmediation of experimental seizures: selective EEG spectral coherence. Epilepsia 44(3):355–365

    Article  PubMed  Google Scholar 

  • Mohammadpoory Z, Nasrolahzadeh M, Haddadnia J (2017) Epileptic seizure detection in EEG signals based on the weighted visibility graph entropy. Seizure Eur J Epilepsy 50:202–208

    Article  Google Scholar 

  • Mohsini KA, Farooq O, Khan YU, Tripathi M (2017) Bispectral analysis of EEG during non-convulsive seizures. In: 2017 international conference on multimedia, signal processing and communication technologies (IMPACT). https://doi.org/10.1109/mspct.2017.8364006

  • Mookiah MRK, Acharya UR, Lim CM, Petznick A, Suri JS (2012) Data mining technique for automated diagnosis of glaucoma using higher order spectra and wavelet energy features. Knowl-Based Syst 33:73–82

    Article  Google Scholar 

  • Moxon K, Kuzmick V, Lafferty J, Serfass A, Szperka D, Zale B, Johnson J, Nagvajara P (2001) Real-time seizure detection system using multiple single-neuron recordings. In: 2001 conference proceedings of the 23rd annual international conference of the IEEE engineering in medicine and biology society, Istanbul, Turkey. https://doi.org/10.1109/iembs.2001.1019101

  • Muni DP, Pal NR, Das J (2006) Genetic programming for simultaneous feature selection and classifier design. IEEE Trans Syst Man Cybern Part B Cybern 36(1):1100–1103

    Article  Google Scholar 

  • Nakariyakul S, Casasent DP (2009) An improvement on floating search algorithms for feature subset selection. Pattern Recogn 42(9):1932–1940

    Article  Google Scholar 

  • Nasrolahzadeh M, Mohammadpoori Z, Haddadnia J (2015a) Optimal way to find the frame length of the speech signal for diagnosis of Alzheimer’s disease with PSO. Asian J Math Comput Res 2(1):33–41

    Google Scholar 

  • Nasrolahzadeh M, Mohhamadpoori Z, Haddadnia J (2015b) Adaptive neuro-fuzzy inference system for classification of speech signals in alzheimer’s disease using acoustc and non-linear characteristics. Asian J Math Comput Res 3(2):122–131

    Google Scholar 

  • Nasrolahzadeh M, Mohhamadpoori Z, Haddadnia J (2015c) Alzheimer’s disease diagnosis using spontaneous speech signals and hybrid features. Asian J Math Comput Res 7(4):322–331

    Google Scholar 

  • Nasrolahzadeh M, Mohhamadpoory Z, Haddadnia J (2016) A novel method for early diagnosis of Alzheimer’s disease based on higher-order spectral estimation of spontaneous speech signals. Cognit Neurodyn 10(6):495–503

    Article  Google Scholar 

  • Nasrolahzadeh M, Mohhamadpoory Z, Haddadnia J (2018) Higher-order spectral analysis of spontaneous speech signals in Alzheimer’s disease. Cognit Neurodyn 12(6):583–596

    Article  Google Scholar 

  • Nasrolahzadeh M, Mohammadpoory Z, Haddadnia J (2019) Analysis of heart rate signals during meditation using visibility graph complexity. Cognit Neurodyn 13(1):45–52

    Article  Google Scholar 

  • Ni XH, Jiang ZQ, Zhou WX (2009) Degree distributions of the visibility graphs mapped from fractional Brownian motions and multifractal random walks. Phys Lett A 373(42):3822–3826

    Article  CAS  Google Scholar 

  • Nicolaou N, Georgiou J (2012) Detection of epileptic electroencephalogram based on permutation entropy and support vector machines. Expert Syst Appl 39(1):202–209

    Article  Google Scholar 

  • Niknazar M, Mousavi SR, Motaghi S, Dehghani A, Vosoughi Vahdat B, Shamsollahi MB, Sayyah M, Noorbakhsh SM (2013) A unified approach for detection of induced epileptic seizures in rats using ECoG signals. Epilepsy Behav 27(2):355–364

    Article  CAS  PubMed  Google Scholar 

  • Nunez AM, Lacasa L, Gomez JP, Luque B (2012) Visibility algorithms: a short review. In: Zhang YG (ed.) New frontiers in graph theory. Intech Press, ch. 6

  • Paul J, Patel CB, Al-Nashash H, Zhang N, Ziai WC, Mirski MA, Sherman DL (2003) Prediction of PTZ-induced seizures using wavelet-based residual entropy of cortical and subcortical field potentials. IEEE Trans Biomed Eng 50(5):640–648

    Article  PubMed  Google Scholar 

  • Pei X, Wang J, Deng B, Wei X, Yu H (2014) WLPVG approach to the analysis of EEG-based functional brain network under manual acupuncture. Cognit Neurodyn 8(5):417–428

    Article  Google Scholar 

  • Polat K, Günes S (2007) Classification of epileptic form EEG using a hybrid system based on decision tree classifier and fast Fourier transform. Appl Math Comput 187(2):1017–1026

    Google Scholar 

  • Racine RJ (1972) Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol 32(3):281–294

    Article  CAS  PubMed  Google Scholar 

  • Ramgopal S, Thome-Souza S, Jackson M, Kadish NE, Sánchez Fernández I, Klehm J, Bosl W, Reinsberger C, Schachter S, Loddenkemper T (2014) Seizure detection, seizure prediction, and closed-loop warning systems in epilepsy. Epilepsy Behav 37:291–307

    Article  PubMed  Google Scholar 

  • Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. NeuroImage 52(3):1059–1069

    Article  PubMed  Google Scholar 

  • Schenk J, Kaiser M, Rigoll G (2009) Selecting features in on-line handwritten whiteboard note recognition: SFS or SFFS?. In: 2009 10th international conference on document analysis and recognition. https://doi.org/10.1109/icdar.2009.130

  • Sherman D, Zhang N, Garg S, Thakor NV, Mirski MA, Anderson Whith M, Hinich MJ (2011) Detection of nonlinear interactions of EEG alpha waves in the brain by a new coherence measure and its application to epilepsy and anti-epileptic drug therapy. Int J Neural Syst 21(2):115–126

    Article  PubMed  PubMed Central  Google Scholar 

  • Siuly S, Kabir E, Wang H, Zhang Y (2015) Exploring sampling in the detection of multicategory EEG signals. Comput Math Methods Med 2015:1–12

    Article  Google Scholar 

  • Siuly S, Wang H, Zhang Y (2016) Detection of motor imagery EEG signals employing Naïve Bayes based learning process. Measurement 86:148–158

    Article  Google Scholar 

  • Srinivas D, Radhakrishnan M, Chakrabarti D, Lakshmegowda M, Manohar N (2018) Intraoperative seizures detected as increased Bispectral Index values during posterior fossa surgeries. J Neuroanaesthesiol Crit Care 5(01):26–29

    Article  Google Scholar 

  • Srinivasan V, Eswaran C, Siraam N (2007) Approximate entropy based epileptic EEG detection using artificial neural networks. IEEE Trans Inf Technol Biomed 11(3):288–295

    Article  PubMed  Google Scholar 

  • Supriya S, Siuly S, Wang H, Cao J, Zhang Y (2016) Weighted visibility graph with complex network features in the detection of epilepsy. IEEE Access 4:6554–6566

    Article  Google Scholar 

  • Tang X, Xia L, Liao Y, Liu W, Peng Y, Gao T, Zeng Y (2013) New approach to epileptic diagnosis using visibility graph of high-frequency signal. Clin EEG Neurosci 44(2):150–156

    Article  PubMed  Google Scholar 

  • Tanq Y, Durand D (2012) A tunable support vector machine assembly classifier for epileptic seizure detection. Exp Syst Appl 39(4):3925–3938

    Article  Google Scholar 

  • Töllner K, Twele F, Löscher W (2016) Evaluation of the pentylenetetrazole seizure threshold test in epileptic mice as surrogate model for drug testing against pharmacoresistant seizures. Epilepsy Behav 57(Pt A):95–104

    Article  PubMed  Google Scholar 

  • Vieira SM, Mendonca LF, Farinha GL, Sousa JMC (2013) Modified binary PSO for feature selection using SVM applied to mortality prediction of septic patients. Appl Soft Comput 13(8):3494–3504

    Article  Google Scholar 

  • Wang J, Zuo X, He Y (2010) Graph-based network analysis of resting-state functional MRI. Front Syst Neurosci 4:16. https://doi.org/10.3389/fnsys.2010.00016

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiang J, Li C, Li H, Cao R, Wang B, Han X, Chen J (2015) The detection of epileptic seizure signals based on fuzzy entropy. J Neurosci Methods 243:18–25

    Article  PubMed  Google Scholar 

  • Yan J, Wang Y, Ouyang G, Yu T, Li X (2016) Using max entropy ratio of recurrence plot to measure electrocorticogram changes in epilepsy patients. Physica A 443:109–116

    Article  Google Scholar 

  • Zhou TT, Jin ND, Gao ZK, Luo YB (2012) Limited penetrable visibility graph for establishing complex network from time series. Acta Phys Sin 6(3):030506

    Google Scholar 

  • Zhu G, Li Y, Wen P (2012) Analysing epileptic EEGs with a visibility graph algorithm. In: 2012 5th international conference on biomedical engineering and informatics. https://doi.org/10.1109/bmei.2012.6513212

  • Zhu G, Li Y, Wen PP, Wang S (2013) Xi M (2013) Epileptic o genic focus detection in intracranial EEG based on delay permutation entropy. AIP Conf Proc 1559:31. https://doi.org/10.1063/1.4824993

    Article  Google Scholar 

  • Zhu G, Li Y, Wen PP (2014) Epileptic seizure detection in EEGs signals using a fast weighted horizontal visibility algorithm. Comput Methods Programs Biomed 115(2):64–75

    Article  PubMed  Google Scholar 

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Appendix

Appendix

Fractal dimension, largest Lyapunove exponent and Bispectrum

In this section, three methods used in work are briefly introduced.

1. FD: fractal systems have self-similarity characteristic. Self-similarity can be measured by the number of basic building units that form a pattern, and this measure is defined as the FD. Several algorithms have been proposed for FD estimation (Lacasa et al. 2009; Higuchi 1988; Katz 1988; Asvestas et al. 1999), and in this work Higuchi (Higuchi 1988) method were used.

2. LLE: LE is a measure of the exponential divergence/convergence of initially nearby trajectories in the phase space (Abarbanel et al. 1993). Since there was only time series, a pseudo phase space or Reconstructed Phase Space (RPS) of the system is constructed using Time Delay Embedding (TDE) method.

Suppose {xi} represents the time series. The RPS is created with a time delay \(\tau\) and an embedding dimension m. The RPS matrix is formed as follows (Nasrolahzadeh et al. 2015):

$$\left[ {\begin{array}{*{20}l} {x_{0} } \hfill & {x_{\tau } } \hfill & \cdots \hfill & {x_{{\left( {n - 1} \right)\tau }} } \hfill \\ {x_{1} } \hfill & {x_{1 + \tau } } \hfill & \cdots \hfill & {x_{{1 + \left( {n - 1} \right)\tau }} } \hfill \\ {x_{2} } \hfill & {x_{2 + \tau } } \hfill & \cdots \hfill & {x_{{2 + \left( {n - 1} \right)\tau }} } \hfill \\ \vdots \hfill & \vdots \hfill & \vdots \hfill & \vdots \hfill \\ \end{array} } \right]$$

Parameter \(\tau\) can be obtained through a number of different methods. In this study, “finding of the mutual information function” method was used for estimation of \(\tau\).

After the optimal lag has been selected, the dimension (m) is estimated by Cao’s method (Nasrolahzadeh et al. 2015).The number of Lyapunov exponents is equal to (that of) the embedding dimension of the attractor. For a system to have at least one positive LE (which implies that the largest Lyapanove exponent (LLE) is greater than zero) leads to be chaotic.

Consider two nearest neighboring points in the phase space at time 0 and t, the distances of the points in the ith direction from these points are shown by \({\delta x}_{\text{i}} (0)\) and \({\delta x}_{\text{i}} (\text{t})\), respectively. The Lyapunov exponent is defined by the mean growth rate \(\uplambda_{\text{i}}\) of the initial distance;

$$\frac{{\delta x_{i} (t)}}{{\delta x_{\varvec{i}} (0)}} = 2^{{\lambda_{i} t}} ,\quad \forall t \to \infty ,$$
(14)
$$\lambda_{\text{i}} = \mathop {\lim }\limits_{t \to \infty } \frac{1}{t}\log_{2} \frac{{\delta x_{i} (t)}}{{\delta x_{\varvec{i}} (0)}},$$
(15)

Two general methods used for the calculation of the LE from time series are the geometrical and Jacobian approaches. In this paper, the first method was used. The first is based on following the time-evolution of nearby points in the phase space. This algorithm estimates the LLE only (Nasrolahzadeh et al. 2015).

3. BIS: BIS is the Fourier transform of the third order correlation of the time series and is defined as:

$$B\left( {f_{1} ,f_{2} } \right) = E\left[ {X\left( {f_{1} } \right)X\left( {f_{2} } \right)X^{*} \left( {f_{1} + f_{2} } \right)} \right],$$
(16)

where X is the Fourier transform of the signal x, X* is the complex conjugate of X and E[] is an average over an ensemble of realizations of a random signal (Nasrolahzadeh et al. 2016).

Equation (16) shows the bispectrum is a function of two frequency variables and complex-valued.

Bispectrum can be estimated through various methods (Chua et al. 2009). In this paper, direct (FFT-based) (Nasrolahzadeh et al. 2018) is used to estimate Bispectrum.

The extracted bispectral based features in this study are:

  1. 1.

    Mean of bispectral magnitude:

    $${\text{M}}_{\text{avg}} = \frac{1}{\text{L}}\mathop \sum \limits_{\varOmega } \left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|,$$
    (17)

    where L is the number of points within the region \(\varOmega .\)

  2. 2.

    Max of bispectral magnitude within the region.

    $${\text{Max}} = {}_{\varOmega }^{ \hbox{max} } \left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|,$$
    (18)
  3. 3.

    Min of bispectral magnitude within the region.

    $${\text{Min}} = {}_{\varOmega }^{ \hbox{min} } \left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|,$$
    (19)
  4. 4.

    The sum of the logarithmic amplitudes of the bispectrum (Mookiah et al. 2012):

    $${\text{H}} = \mathop \sum \limits_{\varOmega } {\text{Log}}\left( {\left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|} \right),$$
    (20)
  5. 5.

    Bispectral phase entropy (Ph) (Mookiah et al. 2012):

    $${\text{Min}} = {}_{\varOmega }^{ \hbox{min} } \left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|,$$
    (21)

    where

    $$\text{p}\left( {\uppsi_{\text{n}} } \right) = \frac{1}{\text{L}}\mathop \sum \limits_{\varOmega } I\left( {\upphi\left( {\text{B}\left( {\text{f}_{1} ,\text{f}_{2} } \right)} \right) \in\uppsi_{\text{n}} } \right),$$
    (22)
    $$\uppsi_{\text{n}} = \left\{ {\upphi |-\uppi + \frac{{2\uppi{\text{n}}}}{\text{N}} \le\upphi < - \pi + \frac{{2\uppi\left( {{\text{n}} + 1} \right)}}{\text{N}}} \right\},$$
    (23)

    n = 0, 1, …, N − 1where \(\phi\) is the phase angle of the bispectrum, and l(.) is a function which obtains a value of 1 when \(\phi\) is within the range bin \(\uppsi_{\text{n}}\) depicted by in Eq. (23).

  6. 6.

    Bispectrum entropies (Mookiah et al. 2012):

    $${\text{P}}_{1} = - \mathop \sum \limits_{{\rm k}} {\text{p}}_{{\rm k}} {\text{logp}}_{{\rm k}} ,$$
    (24)

    where

    $${\text{p}}_{\text{k}} = \frac{{\left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|}}{{\mathop \sum \nolimits_{\varOmega } \left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|}},$$
    (25)
    $${\text{P}}_{2} = - \mathop \sum \limits_{{\rm i}} {\text{q}}_{{\rm i}} {\text{logq}}_{{\rm i}} ,$$
    (26)

    where

    $${\text{q}}_{\text{i}} = \frac{{\left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|^{2} }}{{\mathop \sum \nolimits_{\varOmega } \left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|^{2} }},$$
    (27)
    $${\text{P}}_{3} = - \mathop \sum \limits_{{\rm n}} {\text{r}}_{{\rm n}} {\text{logr}}_{{\rm n}} ,$$
    (28)

    where

    $${\text{r}}_{\text{n}} = \frac{{\left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|^{3} }}{{\mathop \sum \nolimits_{\varOmega } \left| {{\text{B}}\left( {{\text{f}}_{1} ,{\text{f}}_{2} } \right)} \right|^{3} }},$$
    (29)

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Mohammadpoory, Z., Nasrolahzadeh, M., Mahmoodian, N. et al. Complex network based models of ECoG signals for detection of induced epileptic seizures in rats. Cogn Neurodyn 13, 325–339 (2019). https://doi.org/10.1007/s11571-019-09527-y

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  • DOI: https://doi.org/10.1007/s11571-019-09527-y

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