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**Non-linear analysis of EEG signals at various sleep stages
**

Rajendra Acharya U. a,∗, Oliver Faust a, N. Kannathal a, TjiLeng Chua a, Swamy Laxminarayan b

a

Department of Electronics and Computer Engineering, School of Engineering, Ngee Ann Polytechnic, 535 Clementi Road, Singapore 599489, Singapore b Biomedical Research Institute & Institute of Rural Health, Idaho Sate University, USA

Received 14 January 2005 ; received in revised form 15 June 2005; accepted 17 June 2005 KEYWORDS

Correlation dimension; Sleep stages; Approximate entropy; Hurst exponent; Fractal dimension; Lyapunov Exponent

Summary Application of non-linear dynamics methods to the physiological sciences demonstrated that non-linear models are useful for understanding complex physiological phenomena such as abrupt transitions and chaotic behavior. Sleep stages and sustained ﬂuctuations of autonomic functions such as temperature, blood pressure, electroencephalogram (EEG), etc., can be described as a chaotic process. The EEG signals are highly subjective and the information about the various states may appear at random in the time scale. Therefore, EEG signal parameters, extracted and analyzed using computers, are highly useful in diagnostics. The sleep data analysis is carried out using non-linear parameters: correlation dimension, fractal dimension, largest Lyapunov entropy, approximate entropy, Hurst exponent, phase space plot and recurrence plots. These non-linear parameters quantify the cortical function at different sleep stages and the results are tabulated. © 2005 Elsevier Ireland Ltd. All rights reserved.

1. Introduction

Non-linear dynamical analysis has emerged as a novel method for the study of complex systems in the past few decades. The non-linear analysis method is effectively applied to electroencephalogram (EEG) to study the dynamics of the complex underlying behavior [1]. The growth of this method as a tool for mental health evaluation mainly rests

∗

Corresponding author. E-mail address: aru@np.edu.sg (R. Acharya U.).

on the non-invasive nature of EEG. The approach is based on the principles of non-linear dynamics and deterministic chaos that involves the characterization of the system attractors with its invariant parameters. This method is far more superior to the traditional linear methods such as the Fourier transforms and power spectral analysis [2]. Yet, since the EEG signal is non-stationary and noisy, all such studies should be carried out with care and caution [3]. Analysis of sleep EEGs is a very important research branch of medicine, because of its clinical applications (such as diagnosis of schizophrenia) and in brain dynamics research.

0169-2607/$ — see front matter © 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.cmpb.2005.06.011

Recently. The recordings were obtained from Caucasian males and females (21—35 years old) without any medication.1. extremely slow brain waves called delta waves begin to appear. Efforts have been made in determining non-linear parameters like correlation dimension for pathological signals and it has been shown that they are useful indicators of pathologies. Fell et al. In this work. but the frequency will be less than 2 Hz. By stage 4 (deep sleep. In this work. the brain produces delta waves. NonREM sleep encompasses the deeper stages of sleep (sleep stages 1 and 2. The technique has been extended here to identify the abnormalities of different types. Non-linear dynamics theory opens new window for understanding behavior of EEG. interspersed with smaller. This sample size is sufﬁcient for accurate analysis and gives better sample sizes distribution across the various sleep states. a data resource. In stage 4. Subjects The EEG data for analysis were obtained from the Sleep-EDF Database available from the PhysioBank. where the eye movements stop and our brain waves become slower. It is very difﬁcult to wake someone during stages 3 and 4. has long been recognized in the area of non-linear analysis. have studied the sleep stages using the spectral analysis and nonlinear techniques [22. In this state. have used neural network to classify the various sleep stages by extracting the features from the genetic algorithms [18]. measures such as correlation dimension. EEG signal will have the frequency 1—3 Hz and amplitude will be high. . which exhibits typically complex dynamics. The nonlinear dynamical techniques are based on the concept of chaos and it has been applied to many areas including the areas of medicine and biology. Eyes move very slowly. whereas REM sleep is a highly activated state of the brain accompanied by dreaming. EEG models were proposed by Freeman [11] for neocortical dynamics. Hurst exponent (H). fractal dimension (FD). The recordings were taken for 24 h from eight subjects. The correlation dimensions decreased from the ‘awake’ stage to sleep stages 1—3 and increased during rapid eye movement sleep. In analysis of EEG data. And they found statistically signiﬁcant differences between the values of L1 for different sleep stages [21]. namely correlation dimension (CD). In each sleep cycle. Sleep 2 stage is the light sleep state. The most consistent signiﬁcant change is the decrease in theta power.U. In sleep 0 (awake) stage. Several features of these approaches have been proposed to detect the hidden important dynamical properties of the physiological phenomenon. faster waves. phase space plot and recurrence plots (RP). The sleep stages are coded according to Rechtschaffen and Kales based on Fpz-Cz/Pz-Oz EEG [25]. Baumgaurt-Schmitt et al. Fell et al. The subject’s eyes move rapidly along with the occasional muscular twitches in sleep 5 (REM) stage. Theta wave is more predominant in this sleep stage. different chaotic A. Sleep patterns in humans undergo a marked change from birth to old age. Lyapunov exponent and entropy are used in recent literature [12—17]. largest Lyapunov entropy (LLE). slow wave sleep).38 Sleep is not a uniform state. the polysomnography of a healthy male subject was analyzed by evaluating the correlation dimensions. The voltage is low and the ‘‘beta waves’’ are prominent. Dingli et al. The theory of chaos has been used to detect some cardiac arrhythmia such as ventricular ﬁbrillation [10]. Recently. the patient’s eyes are open and the EEG is rapidly varying. approximate entropy (ApEn). but is characterized by a cyclic alternating pattern of non-rapid eye movement (REM) and REM sleep [4—9]. They concluded that nonlinear measures yield additional information. which improves the ability to discriminate sleep stages. we study the six different types of sleep signals using the non-linear parameters. Special waves ‘K-complexes’ and sleep spindles begin to appear. and increase for REM sleep [19. The analysis of these biological signals is complicated due to its highly irregular and non-stationary property. Methodology 2. the amplitude of EEG will be high.20]. and slow wave sleep with sleep stages 3 and 4). In stage 3 (deep sleep). Sleep EEG for 80 h is extracted from the recordings and sampled at 100 Hz. the correlation dimensions decrease for slow wave sleep. the maximum available samples for different sleep states were taken from the PhysioBank. Rajendra et al. have calculated the ﬁrst Lyapunov exponents (L1 ) for different sleep EEG signal in 15 healthy subjects corresponding to the sleep stages 1—4 and REM. EEG amplitude is medium and EEG frequency is 4—7 Hz. during NREM sleep is either associated with an increase in high frequencies (alpha and sigma) or delta increase [24]. the EEG frequency will be 6—8 Hz and alpha waves are more predominant in the sleep 1 (drowsiness) stage. except for sleep state 0. have shown the spectral analysis technique for the detection of cortical activity changes in sleep apnoea subjects. which together are called deep sleep.23]. 2. The importance of the biological time-series analysis. where 1500 samples were selected.

the corresponding embedding dimension is unknown. then the separation between the two . This measure is ﬁnally obtained as follows: ApEn(m. Here. The software used for analysis is CDA Pro Data analyzer [31]. but not a necessary condition for dynamical reconstruction [29]. passes closely to a state it was previously in and diverges. The time-domain signal is embedded in the phase space. and examined there in. The delay interval T is calculated using the minimal mutual information technique [26. r the radial distance around each reference point Xi . Thus. Phase space plot In this approach. Nevertheless. m is set to 2 and r is set to 15% of the standard deviation of each time-series.3. where m speciﬁes the pattern length and r is the effective ﬁlter. 1 L−m+1 (3) 2. ApEn quantiﬁes the (log) likelihood that sets of patterns that are close on next incremental comparison. Correlation dimension was calculated using the fundamental deﬁnition CD = lim r→0 × i=1 m log Ci (r) log C(r) log(r) N x=1 (1) Thus. We estimated CD using an approach based Grassberger—Procaccia algorithm [28]. and the Y-axis representing the EEG sample after a delay x(k + T). For this study. It estimates the average number of data points within a radius r of the data point Xy . max provides a measure of the rate of this (typically exponent) divergence [35]. L) = 1 L−m L−m L−m i=1 m+1 log Ci (r) − 2. a random signal has a very low regularity and produces a high ApEn value. where the correlation integral C(r) is given by 1 C(r) = (N − Ámin )(N − Ámin − 1) N 2.33]. there are very few reported results [34] of the application of ApEn. Largest Lyapunov exponent ( max ) × y=x+Ámin (r − |Xx − Xy |) (2) where Xx and Xy are the points of the trajectory in the phase space. r. the time taken for the autocorrelation function to ﬁrst decay to 1/e. Approximate entropy is a measure of complexity and is applied to relatively short and noisy data [32.2. during its orbit.Non-linear analysis of EEG signals at various sleep stages In sleep 1 state. If the time-series is highly irregular. a phase space plot is obtained with the X-axis representing the EEG sample x(k). Approximate entropy Approximate entropy is deﬁned as the logarithmic likelihood that the patterns of the data that are close to each other will remain close for the next comparison with a longer pattern.4. the Heaviside function and Ámin is the average correlation time. Smaller values of ApEn imply a greater likelihood that certain patterns of measurements will be followed by similar measurements. 1000 samples in sleep 2—4 state and in sleep 5 state 900 samples (maximum available) were extracted from PhysioBank for our study. In EEG analysis. N the number of data points in phase space. ApEn provides a generalized measure of regularity. Two parameters m and r must be chosen prior to the computation of ApEn. an embedding dimension of 10 was chosen [30. that are function of time and each of which will generate an orbit in that space using some equation or system of equations. Correlation dimension Correlation dimension describes the dimensionality of the underlying process in relation to its geometrical reconstruction in phase space. On the other hand.31]. It deﬁnes the averaged rate of divergence (or convergence) of two neighboring trajectories. A deterministic signal with high regularity has a higher probability of remaining close for longer vectors of the series and hence has a very small ApEn value.27]. one has to compute the correlation integral Cm (r) (with embedding dimension m and time lag 1). the occurrence of similar patterns in the future is less likely. Largest Lyapunov exponent reﬂects the sensitivity of the system to the initial conditions. If the attractor. For two points in a space X0 and X0 + x0 . the dimensionality of the attractor is usually unknown for experimental data and therefore. 800 samples (maximum available). Other authors have veriﬁed that the embedding theorem restriction is only a sufﬁcient. In the present work. 39 2. A method of estimating the embedding dimension from the phase space patterns was proposed by Grassberger and Procaccia [28]. It has been observed that the patterns emerging on the screen can be correlated to the various sleep states.5.

Hurst exponent is used to evaluate the presence or absence of long-range dependence and its degree in a time-series. t) will behave erratically. Many algorithms are available to determine the FD of the waveform. The FD emerges to provide a measure of how much space an object occupies between Euclidean dimensions.. However. In this work.5. The mean exponential rate of divergence of two initially close orbits is characterized by = lim 1 ln t→˛ t x(X0 .6. Normalizing the distances DKatz is then given by. Fractal dimension The term ‘‘fractal’’ was ﬁrst introduced by Mandelbrot [36]. is deﬁned as: log(R/S) H= log(T ) (5) 2. Katz algorithm Using Katz’s method [37]. If H = 0. Katz’s approach solves this problem by creating a general unit or yardstick: the average step or average distance between successive points. d can be expressed as d = max( x(1). DKatz = log10 (L) log10 (d) (6) where T is the duration of the sample of data and R/S is the corresponding value of rescaled range. The FD of a waveform represents a powerful tool for transient detection. . n = 1. resembles the whole set. looked at smaller scales. algorithm proposed by Katz is implemented for analysis of EEG signals. the topological or Euclidean dimension of an object is known as the number of directions each differential of the object occupies in space.5. their level of ‘‘space-ﬁlling’’ is different. t). This number. This deﬁnition of dimension works well for geometrical objects whose level of detail. . local trends (non-stationarities) are often present in physiological data and may compromise the ability of some methods to measure self-similarity. The FD compares the actual number of units that compose a curve with the minimum number of units required to reproduce a pattern of the same spatial extent. and vice-versa). Rajendra et al. This feature has been used in the analysis of ECG and EEG to identify and distinguish speciﬁc states of physiological function. The Hurst exponent. Mathematically. H. the time-series produced by a fractional (fractal) Gaussian process.8. where E is the Euclidean dimension. Hurst exponent The Hurst exponent is a measure that has been widely used to evaluate the self-similarity and correlation properties of fractional Brownian noise. if the timeseries increases. For chaotic data set.7. DKatz = log10 (L/a) log10 (d/a) (7) . H is related to the fractal dimension D: H = E + 1 − D. the timeseries covers more ‘‘distance’’ than a random walk (if the time-series increases. This separation is also a function of the location of the initial value and has the form x(X0 . is useful for distinguishing among the various types of orbits. 2. and that information is not given by the topological dimension. N. point i is the one that maximizes the distance with respect to the ﬁrst point. The concept of fractal dimension that refers to a non-integer or fractional dimension originates from fractal geometry. called the Lyapunov exponent ‘‘ ’’. it is more probable that it will continue to increase). . the FD of a curve can be deﬁned as. The above expression is obtained from the Hurst’s generalized equation of time-series that is also valid for Brownian motion. where k is a constant. In traditional geometry. the time-series covers less ‘‘distance’’ than a random walk (i. The Hurst exponent is a measure of the smoothness of a fractal time-series based on the asymptotic behavior of the rescaled range of the process. H can be estimated by taking the slope of (R/S) plotted versus n in a log—log scale. 2.e. the function x(X0 . Given a timeseries x(n). the behavior of the time-series is similar to a random walk. FDs computed in this fashion depend upon the measurement units used. it is more probable that then it will decrease. a. Considering the distance between each point of the sequence and the ﬁrst. when considering two fractals of the same topological dimension. x(i) ). If the units are different. if H < 0.5. A fractal is a set of points that when where L is the total length of the curve or sum of distances between successive points and d is the diameter estimated as the distance between the ﬁrst point of the sequence and the point of the sequence that provides the farthest distance. However. It is given by R/S = k × TH .U.40 orbits x will also be a function of time. then so are the FDs. t) | X0 | (4) A. if H > 0. complexity or ‘‘space-ﬁlling’’ is the same.

11. indicating 2. in the recurrence plot. These plots disclose distance relationships between points on a dynamical system providing a faithful representation of the time dependencies (correlations) contained in the data [38]. randomize the phases while keeping the magnitudes intact. The ‘‘surrogate’’ data sets are created from the original data. and then make the invert Fourier transform. FD and H have higher value for the sleep 0 (awake) state due to the highly active cortex and desynchronized EEG signals. All the results are presented as mean ± S. with ‘‘p’’-values in Table 1. the variation is very high. Hence. Hurst exponent (H). Largest Lyapunov exponents ( max ) provide a measure of the rate of this divergence. we choose r(i) such that the ball of radius r(i) centered at s(i) in RdE contains reasonable number of other points s(j) of the orbit. Results The ApEn.10. ANOVA uses variances to decide whether the means are different. this value falls gradually due to the reduction in the variability of EEG signals and the cortex becomes more inactive. taking into account how many subjects there are in the groups. Non-linear dynamics using surrogate data For the noisy and short time-series.e. The resulting plot is the recurrence plot. Recently. an embedding dimension dE . i. The recurrence plot is an N × N square. Next. correlation dimension. is chosen by method of delays [39]. This value is increased for sleep 3 and 5 states due to more variation involved as compared to the other states. If the difference between the real and the surrogate dimension is signiﬁcantly larger than the standard deviation of the surrogate dimensions calculated from different sets. original and surrogate data sets. In this state. ANOVA test The p-value can be obtained using analysis of variance between groups (ANOVA) test. The reduction in FD values characterizes the reduction in brain system complexity for the subjects during the sleep activity. This is a graphical tool for the diagnosis of drift and hidden periodicities in the time evolution of dynamical systems. This is obtained using the Chaos Data Analyzer [31]. because of the decrease in the frequency. CD. for example. In sleep 0 state. Then. The practical way to do this is to take the Fourier transform of the original data. there are many yellow strips (presence of beta activity). it is particularly useful in the analysis of physiological data. therefore. Recurrence plot Recurrence plots are a valuable tool for assessing the geometry of the dynamics exploiting non-linear dependencies even in non-stationary time-series. The results of these were subjected to ANOVA test with more than 95% conﬁdence interval giving excellent ‘p’-values in all cases. they can indicate the presence of the non-linear dynamics in completely random systems. but they are random in all other respects. This test uses the variation (variance) within the groups and translate into variation (i.e. j) whenever s(j) is sufﬁciently close to s(i). then it is a strong indication of the non-linear structure in the investigated time-series. where a dot is placed at (i. standard chaotic dynamics algorithms can give spurious results. but they contain exactly the same linear correlations as that in the original time-series. If the observed differences are high. 2. The mean CD decreases from the awake state to stages of 1—4 and then increases during the rapid eye movement sleep. In this state. using the same algorithm for both. the surrogate data techniques have been developed to distinguish the chaotic systems from the linearly correlated noise [40]. one can compute any chaos parameter. 3. the ApEn will be lowest due to the very low variation in the EEG signals. In sleep 1—4 states. is obtained for all data sets.D. then it is considered to be statistically signiﬁcant. The FD decreases from sleep 0 to 1—4 states.9. which are unnoticeable otherwise. Finally. Let s(i) be the ith point on the orbit describing a dynamical system in dE -dimensional space. The self-similarity parameter. And this FD increases in sleep 5 state due to increase in the frequency. LLE. The resulting time-series have the same power spectrum as the initial data set. j) for which s(j) is in the ball of radius r(i) centered at s(j). It has a maximum value in state 3 from which it decreases in the states 3 and 4 and has maximum value in state 5 indicating higher self-similarity. differences) between the groups. To obtain a recurrence plot from timeseries s(n). we plot at each point (i. In sleep 4 state. the variation is slightly more and as a result the ApEn increases. The sleep 5 state is the REM state. This value gradually decreases from state 1 to 2.Non-linear analysis of EEG signals at various sleep stages 41 2. . This change in the CD for different sleep states is attributed for their signal variability. The ‘‘surrogate’’ data are completely stochastic. the EEG signal becomes highly random.

81 ± 0.74 ± 0.67 6.34 0.063 0. these blue and green patches decreases indicating the decrease in the frequency and also the presence of delta wave.03 0.51 ± ± ± ± ± Sleep 1 Sleep 2 Sleep 3 Sleep 4 Sleep 5 ‘p’-Value 0.31 1. In sleep 2 state.41 0.45 ± 0.000 0.28 ± 0. the EEG signal frequency decreases further.91 0.02 ± 0. there are still patches of blue and yellow colors Fig.97 6. (b) Phase space plot at sleep 1 stage.000 0. 1 (a) Result of recurrence plot at sleep 0 stage. the high frequency component decreases and is indicated by blue.51 0.84 ± 0.42 A. The presence of blue and green patches indicates the theta activity in this state. in sleep state 5.U.43 ± 0.59 0.96 ± 0.30 0.60 ± 0.83 ± 0. Fig. 3(a).20 0.23 Parameters the presence of high frequencies (Fig.45 0. Rajendra et al.98 ± 0.25 ± 0.000 0.29 ± 0. respectively). the theta activity is indicated by blue patches.55 ± 0.86 6.000 0. And in sleep state 4.24 0.23 ± 0.30 ± 0.11 −1.67 6.40 0. (b) Phase space plot at sleep 0 stage. 4(a) and 5(a).68 ± 0. 1(a)). 2 (a) Result of recurrence plot at sleep 1 stage.57 0. Table 1 FD ApEn CD LLE H Result of various non-linear parameters for various sleep stages Sleep 0 −1. The sleep 2—4 states show patches of blue.07 0.60 5. In state 3.10 ± 0.21 −1.39 ± 0.54 6. In sleep 1 stage. 2(a)).20 0.21 0.47 0.20 −1.28 1.19 −1.53 0.34 ± 0.42 ± 0. Finally.91 ± 0. the delta waves begin to appear (is indicated by small green patches). red and green patches (Fig. red and green colors indicating less variation in the EEG signal (Figs.58 ± 0.41 0.19 0.95 ± 0.05 −1.39 ± 0.07 0. .

4 (a) Result of recurrence plot at sleep 3 stage. 3 (a) Result of recurrence plot at sleep 2 stage.Non-linear analysis of EEG signals at various sleep stages 43 Fig. (b) Phase space plot at sleep 4 stage. . 5 (a) Result of recurrence plot at sleep 4 stage. Fig. (b) Phase space plot at sleep 3 stage. Fig. (b) Phase space plot at sleep 2 stage.

20 sets of surrogate data are generated for each of the ﬁve stages of sleep. (b) Phase space plot at sleep 5 stage. spectral edge. almost to the level at which it is when a person is awake. whereas the values of spectral measures were distinct for stages 2 and 3. And they showed that the non-linear parameters (CD and LLE) performed better in discriminating sleep stages 1 and 2.44 A. But in sleep 5 (REM) state. the spread is wide due to the increase in the EEG variation (Fig. due to the decrease in the variation and at state 5. have used the polysomnography of a healthy male subject to analyze the sleep stages by calculating the correlation dimensions [19]. spectral entropy and ﬁrst spectral moments. As a result. It shows a wide spread. and non-linear measures like correlation dimension. indicating the low and high frequencies (Fig. These ﬁgures are unique for the different sleep states. less number of neurons will be available for processing the information and as a result the entropy. In each sleep cycle. To test for the non-linearity of the sleep EEG signal. 6 (a) Result of recurrence plot at sleep 5 stage. 6(a)). ApEn and Hurst exponent. This rejects the null hypothesis and hence the original data contain non-linear features. Figs. Fig. and increase for REM sleep. They evaluated the spectral measures like relative delta power. Rajendra et al. Hence. The . LLE and H fall. 4(b) and 5(b) indicate the phase space plots of the sleep 1—4 states. Fell et al. 5. 2(b). until sleep 4 state. 3(b). Fig. Conclusion In this work. CD. Kobayashi et al. 4. largest Lyapunov exponent and approximated Kolmogorov entropy (K2). the cortex becomes more active and more neurons will be available for processing the information. ApEn is obtained for both the original and surrogate data sets. the brain is very active in this state. we have analyzed the cortical functioning at different sleep stages using the nonlinear parameters: FD. Blood ﬂow to the brain is also increased during this stage of sleep. The phase space plot area decreases from states 1 to 4. But in sleep 5 state. These results were seen during each sleep cycle. We found that the surrogate data ApEn and original data ApEn are different from each other by more than 50%. These values decrease indicating the reduction in the disorder from sleep states 0 to 4. due to the lesser number of available neurons in each state for processing. max . have studied the sleep stages using the spectral analysis and non-linear techniques [22. 1(b) shows the phase space plot for the sleep 0 (awake) state.U. Discussion The cortex becomes more inactive as the person goes through from one sleep stage to the next stage. The similar procedure is repeated for correlation dimension. indicating more variation in the EEG in this state. these values increase due to the highly active cortex. The correlation dimensions decreased from the ‘awake’ stage to sleep stages 1—3 and increased during rapid eye movement sleep.23]. Combinations of spectral and non-linear measures yielded a better overall discrimination of sleep stages than spectral measures alone. The surrogate data correlation dimension and original data correlation dimension are different from each other by more than 58%. CD. the correlation dimensions decrease for slow wave sleep. 6(b)).

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