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Computer Methods and Programs in Biomedicine (2005) 80, 37—45

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 Summary Application of non-linear dynamics methods to the physiological sci-


Correlation dimension; ences demonstrated that non-linear models are useful for understanding complex
Sleep stages; physiological phenomena such as abrupt transitions and chaotic behavior. Sleep
Approximate entropy; stages and sustained fluctuations of autonomic functions such as temperature, blood
Hurst exponent; pressure, electroencephalogram (EEG), etc., can be described as a chaotic pro-
Fractal dimension; cess. 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,
Lyapunov Exponent
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 on the non-invasive nature of EEG. The approach


is based on the principles of non-linear dynamics
Non-linear dynamical analysis has emerged as a and deterministic chaos that involves the charac-
novel method for the study of complex systems terization of the system attractors with its invariant
in the past few decades. The non-linear analysis parameters. This method is far more superior to the
method is effectively applied to electroencephalo- traditional linear methods such as the Fourier trans-
gram (EEG) to study the dynamics of the complex forms and power spectral analysis [2]. Yet, since the
underlying behavior [1]. The growth of this method EEG signal is non-stationary and noisy, all such stud-
as a tool for mental health evaluation mainly rests ies 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 appli-
∗ Corresponding author.
cations (such as diagnosis of schizophrenia) and in
E-mail address: aru@np.edu.sg (R. Acharya U.). brain dynamics research.

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

Sleep is not a uniform state, but is character- measures such as correlation dimension, Lyapunov
ized by a cyclic alternating pattern of non-rapid exponent and entropy are used in recent literature
eye movement (REM) and REM sleep [4—9]. Non- [12—17].
REM sleep encompasses the deeper stages of sleep Baumgaurt-Schmitt et al. have used neural net-
(sleep stages 1 and 2, and slow wave sleep with work to classify the various sleep stages by extract-
sleep stages 3 and 4), whereas REM sleep is a highly ing the features from the genetic algorithms [18].
activated state of the brain accompanied by dream- Recently, the polysomnography of a healthy male
ing. Sleep patterns in humans undergo a marked subject was analyzed by evaluating the correlation
change from birth to old age. dimensions. The correlation dimensions decreased
In sleep 0 (awake) stage, the patient’s eyes are from the ‘awake’ stage to sleep stages 1—3 and
open and the EEG is rapidly varying. The voltage increased during rapid eye movement sleep. In each
is low and the ‘‘beta waves’’ are prominent. Eyes sleep cycle, the correlation dimensions decrease
move very slowly, the EEG frequency will be 6—8 Hz for slow wave sleep, and increase for REM sleep
and alpha waves are more predominant in the sleep [19,20]. Fell et al. have calculated the first Lya-
1 (drowsiness) stage. Sleep 2 stage is the light sleep punov exponents (L1 ) for different sleep EEG signal
state, where the eye movements stop and our brain in 15 healthy subjects corresponding to the sleep
waves become slower. Special waves ‘K-complexes’ stages 1—4 and REM. And they found statistically
and sleep spindles begin to appear. In this state, significant differences between the values of L1 for
EEG amplitude is medium and EEG frequency is different sleep stages [21]. Fell et al. have studied
4—7 Hz. In stage 3 (deep sleep), extremely slow the sleep stages using the spectral analysis and non-
brain waves called delta waves begin to appear, linear techniques [22,23]. They concluded that non-
interspersed with smaller, faster waves. EEG sig- linear measures yield additional information, which
nal will have the frequency 1—3 Hz and amplitude improves the ability to discriminate sleep stages.
will be high. By stage 4 (deep sleep, slow wave Recently, Dingli et al. have shown the spectral anal-
sleep), the brain produces delta waves. It is very ysis technique for the detection of cortical activity
difficult to wake someone during stages 3 and 4, changes in sleep apnoea subjects. The most con-
which together are called deep sleep. In stage 4, sistent significant change is the decrease in theta
the amplitude of EEG will be high, but the fre- power, during NREM sleep is either associated with
quency will be less than 2 Hz. The subject’s eyes an increase in high frequencies (alpha and sigma)
move rapidly along with the occasional muscular or delta increase [24]. In this work, we study the six
twitches in sleep 5 (REM) stage. Theta wave is more different types of sleep signals using the non-linear
predominant in this sleep stage. parameters, namely correlation dimension (CD),
The importance of the biological time-series Hurst exponent (H), approximate entropy (ApEn),
analysis, which exhibits typically complex dynam- largest Lyapunov entropy (LLE), fractal dimension
ics, has long been recognized in the area of (FD), phase space plot and recurrence plots (RP).
non-linear analysis. Several features of these
approaches have been proposed to detect the
hidden important dynamical properties of the 2. Methodology
physiological phenomenon. The analysis of these
biological signals is complicated due to its highly 2.1. Subjects
irregular and non-stationary property. The non-
linear dynamical techniques are based on the The EEG data for analysis were obtained from the
concept of chaos and it has been applied to many Sleep-EDF Database available from the PhysioBank,
areas including the areas of medicine and biology. a data resource. The recordings were obtained from
The theory of chaos has been used to detect some Caucasian males and females (21—35 years old)
cardiac arrhythmia such as ventricular fibrillation without any medication. The recordings were taken
[10]. Efforts have been made in determining for 24 h from eight subjects. Sleep EEG for 80 h
non-linear parameters like correlation dimension is extracted from the recordings and sampled at
for pathological signals and it has been shown 100 Hz. The sleep stages are coded according to
that they are useful indicators of pathologies. Rechtschaffen and Kales based on Fpz-Cz/Pz-Oz
Non-linear dynamics theory opens new window EEG [25]. In this work, the maximum available sam-
for understanding behavior of EEG. EEG models ples for different sleep states were taken from the
were proposed by Freeman [11] for neocortical PhysioBank, except for sleep state 0, where 1500
dynamics. The technique has been extended samples were selected. This sample size is suffi-
here to identify the abnormalities of different cient for accurate analysis and gives better sample
types. In analysis of EEG data, different chaotic sizes distribution across the various sleep states.
Non-linear analysis of EEG signals at various sleep stages 39

In sleep 1 state, 800 samples (maximum available), 2.4. Approximate entropy


1000 samples in sleep 2—4 state and in sleep 5 state
900 samples (maximum available) were extracted Approximate entropy is defined as the logarithmic
from PhysioBank for our study. likelihood that the patterns of the data that are
close to each other will remain close for the next
2.2. Phase space plot comparison with a longer pattern. Thus, ApEn
provides a generalized measure of regularity. A
In this approach, a phase space plot is obtained deterministic signal with high regularity has a
with the X-axis representing the EEG sample x(k), higher probability of remaining close for longer
and the Y-axis representing the EEG sample after vectors of the series and hence has a very small
a delay x(k + T). The delay interval T is calculated ApEn value. On the other hand, a random signal
using the minimal mutual information technique has a very low regularity and produces a high ApEn
[26,27]. It has been observed that the patterns value.
emerging on the screen can be correlated to the Approximate entropy is a measure of complex-
various sleep states. ity and is applied to relatively short and noisy
A method of estimating the embedding dimen- data [32,33]. In EEG analysis, there are very few
sion from the phase space patterns was proposed by reported results [34] of the application of ApEn.
Grassberger and Procaccia [28]. Other authors have Two parameters m and r must be chosen prior to
verified that the embedding theorem restriction is the computation of ApEn, where m specifies the
only a sufficient, but not a necessary condition for pattern length and r is the effective filter. Here,
dynamical reconstruction [29]. Nevertheless, the one has to compute the correlation integral Cm (r)
dimensionality of the attractor is usually unknown (with embedding dimension m and time lag 1). This
for experimental data and therefore, the corre- measure is finally obtained as follows:
sponding embedding dimension is unknown. In the L−m
present work, an embedding dimension of 10 was 1  1
ApEn(m, r, L) = log Cim+1 (r) −
chosen [30,31]. The software used for analysis is L−m L−m+1
i=1
CDA Pro Data analyzer [31].
L−m

× log Cim (r) (3)
2.3. Correlation dimension
i=1

Correlation dimension describes the dimensionality Thus, ApEn quantifies the (log) likelihood that sets
of the underlying process in relation to its geomet- of patterns that are close on next incremental
rical reconstruction in phase space. We estimated comparison. Smaller values of ApEn imply a greater
CD using an approach based Grassberger—Procaccia likelihood that certain patterns of measurements
algorithm [28]. It estimates the average number of will be followed by similar measurements. If the
data points within a radius r of the data point Xy . time-series is highly irregular, the occurrence of
Correlation dimension was calculated using the similar patterns in the future is less likely. For
fundamental definition this study, m is set to 2 and r is set to 15% of the
log C(r) standard deviation of each time-series.
CD = lim (1)
r→0 log(r)
2.5. Largest Lyapunov exponent ( max )
where the correlation integral C(r) is given by
N Largest Lyapunov exponent reflects the sensitiv-
1 
C(r) = ity of the system to the initial conditions. The
(N − min )(N − min − 1) time-domain signal is embedded in the phase
x=1
space, and examined there in. If the attractor,
N
 during its orbit, passes closely to a state it was
× (r − |Xx − Xy |) (2)
previously in and diverges, max provides a measure
y=x+min
of the rate of this (typically exponent) divergence
where Xx and Xy are the points of the trajectory [35].
in the phase space, N the number of data points It defines the averaged rate of divergence (or
in phase space, r the radial distance around each convergence) of two neighboring trajectories. For
reference point Xi ,  the Heaviside function and two points in a space X0 and X0 + x0 , that are func-
min is the average correlation time, the time taken tion of time and each of which will generate an
for the autocorrelation function to first decay to orbit in that space using some equation or system
1/e. of equations, then the separation between the two
40 A.U. Rajendra et al.

orbits x will also be a function of time. This sepa- looked at smaller scales, resembles the whole set.
ration is also a function of the location of the initial The concept of fractal dimension that refers to
value and has the form x(X0 , t). For chaotic data a non-integer or fractional dimension originates
set, the function x(X0 , t) will behave erratically. from fractal geometry. In traditional geometry, the
The mean exponential rate of divergence of two topological or Euclidean dimension of an object is
initially close orbits is characterized by known as the number of directions each differen-
  tial of the object occupies in space. This definition
1 x(X0 , t)
= lim ln (4) of dimension works well for geometrical objects
t→˛ t |X0 | whose level of detail, complexity or ‘‘space-filling’’
This number, called the Lyapunov exponent ‘‘ ’’, is is the same. However, when considering two frac-
useful for distinguishing among the various types of tals of the same topological dimension, their level
orbits. of ‘‘space-filling’’ is different, and that information
is not given by the topological dimension. The FD
emerges to provide a measure of how much space
2.6. Hurst exponent an object occupies between Euclidean dimensions.
The FD of a waveform represents a powerful tool
The Hurst exponent is a measure that has been
for transient detection. This feature has been used
widely used to evaluate the self-similarity and cor-
in the analysis of ECG and EEG to identify and dis-
relation properties of fractional Brownian noise,
tinguish specific states of physiological function.
the time-series produced by a fractional (fractal)
Many algorithms are available to determine the
Gaussian process. Hurst exponent is used to evalu-
FD of the waveform. In this work, algorithm pro-
ate the presence or absence of long-range depen-
posed by Katz is implemented for analysis of EEG
dence and its degree in a time-series. However,
signals.
local trends (non-stationarities) are often present
in physiological data and may compromise the abil-
ity of some methods to measure self-similarity. The 2.8. Katz algorithm
Hurst exponent is a measure of the smoothness of a
fractal time-series based on the asymptotic behav- Using Katz’s method [37], the FD of a curve can be
ior of the rescaled range of the process. The Hurst defined as,
exponent, H, is defined as:
log10 (L)
DKatz = (6)
log(R/S) log10 (d)
H= (5)
log(T )
where L is the total length of the curve or sum of
where T is the duration of the sample of data distances between successive points and d is the
and R/S is the corresponding value of rescaled diameter estimated as the distance between the
range. The above expression is obtained from the first point of the sequence and the point of the
Hurst’s generalized equation of time-series that sequence that provides the farthest distance. Math-
is also valid for Brownian motion. It is given by ematically, d can be expressed as d = max(x(1),
R/S = k × TH , where k is a constant. If H = 0.5, the x(i)).
behavior of the time-series is similar to a ran- Considering the distance between each point
dom walk; if H < 0.5, the time-series covers less of the sequence and the first, point i is the one
‘‘distance’’ than a random walk (i.e. if the time- that maximizes the distance with respect to the
series increases, it is more probable that then it first point. The FD compares the actual number
will decrease, and vice-versa); if H > 0.5, the time- of units that compose a curve with the minimum
series covers more ‘‘distance’’ than a random walk number of units required to reproduce a pattern
(if the time-series increases, it is more probable of the same spatial extent. FDs computed in this
that it will continue to increase). Given a time- fashion depend upon the measurement units used.
series x(n), n = 1, . . ., N, H can be estimated by If the units are different, then so are the FDs.
taking the slope of (R/S) plotted versus n in a Katz’s approach solves this problem by creating
log—log scale. H is related to the fractal dimension a general unit or yardstick: the average step
D: H = E + 1 − D, where E is the Euclidean dimension. or average distance between successive points,
a. Normalizing the distances DKatz is then given
2.7. Fractal dimension by,

The term ‘‘fractal’’ was first introduced by Man- log10 (L/a)


DKatz = (7)
delbrot [36]. A fractal is a set of points that when log10 (d/a)
Non-linear analysis of EEG signals at various sleep stages 41

2.9. Recurrence plot 2.11. ANOVA test

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

Table 1 Result of various non-linear parameters for various sleep stages


Parameters Sleep 0 Sleep 1 Sleep 2 Sleep 3 Sleep 4 Sleep 5 ‘p’-Value
FD −1.45 ± 0.19 −1.60 ± 0.21 −1.39 ± 0.20 −1.74 ± 0.11 −1.81 ± 0.05 −1.55 ± 0.20 0.000
ApEn 0.97 ± 0.40 0.68 ± 0.57 0.91 ± 0.47 0.45 ± 0.53 0.28 ± 0.41 0.83 ± 0.51 0.000
CD 6.03 ± 0.86 6.34 ± 0.60 5.96 ± 0.67 6.29 ± 0.67 6.42 ± 0.54 6.30 ± 0.59 0.000
LLE 0.91 ± 0.34 0.95 ± 0.21 0.84 ± 0.31 1.10 ± 0.30 0.98 ± 0.28 1.02 ± 0.41 0.063
H 0.51 ± 0.20 0.39 ± 0.19 0.58 ± 0.24 0.25 ± 0.07 0.23 ± 0.07 0.43 ± 0.23 0.000

the presence of high frequencies (Fig. 1(a)). In In sleep 2 state, the theta activity is indicated by
sleep 1 stage, the high frequency component blue patches. In state 3, the EEG signal frequency
decreases and is indicated by blue, red and green decreases further, the delta waves begin to appear
patches (Fig. 2(a)). The presence of blue and green (is indicated by small green patches). And in sleep
patches indicates the theta activity in this state. state 4, these blue and green patches decreases
The sleep 2—4 states show patches of blue, red indicating the decrease in the frequency and also
and green colors indicating less variation in the the presence of delta wave. Finally, in sleep state
EEG signal (Figs. 3(a), 4(a) and 5(a), respectively). 5, there are still patches of blue and yellow colors

Fig. 1 (a) Result of recurrence plot at sleep 0 stage. (b) Phase space plot at sleep 0 stage.

Fig. 2 (a) Result of recurrence plot at sleep 1 stage. (b) Phase space plot at sleep 1 stage.
Non-linear analysis of EEG signals at various sleep stages 43

Fig. 3 (a) Result of recurrence plot at sleep 2 stage. (b) Phase space plot at sleep 2 stage.

Fig. 4 (a) Result of recurrence plot at sleep 3 stage. (b) Phase space plot at sleep 3 stage.

Fig. 5 (a) Result of recurrence plot at sleep 4 stage. (b) Phase space plot at sleep 4 stage.
44 A.U. Rajendra et al.

Fig. 6 (a) Result of recurrence plot at sleep 5 stage. (b) Phase space plot at sleep 5 stage.

indicating the low and high frequencies (Fig. 6(a)). more neurons will be available for processing the
These figures are unique for the different sleep information.
states. Fig. 1(b) shows the phase space plot for Kobayashi et al. have used the polysomnogra-
the sleep 0 (awake) state. It shows a wide spread, phy of a healthy male subject to analyze the sleep
indicating more variation in the EEG in this state. stages by calculating the correlation dimensions
Figs. 2(b), 3(b), 4(b) and 5(b) indicate the phase [19]. The correlation dimensions decreased from
space plots of the sleep 1—4 states. The phase the ‘awake’ stage to sleep stages 1—3 and increased
space plot area decreases from states 1 to 4, due during rapid eye movement sleep. These results
to the decrease in the variation and at state 5, were seen during each sleep cycle. In each sleep
the spread is wide due to the increase in the EEG cycle, the correlation dimensions decrease for slow
variation (Fig. 6(b)). wave sleep, and increase for REM sleep. Fell et al.
To test for the non-linearity of the sleep EEG have studied the sleep stages using the spectral
signal, 20 sets of surrogate data are generated for analysis and non-linear techniques [22,23]. They
each of the five stages of sleep. ApEn is obtained evaluated the spectral measures like relative delta
for both the original and surrogate data sets. We power, spectral edge, spectral entropy and first
found that the surrogate data ApEn and original spectral moments, and non-linear measures like
data ApEn are different from each other by more correlation dimension, largest Lyapunov exponent
than 50%. The similar procedure is repeated for cor- and approximated Kolmogorov entropy (K2). And
relation dimension. The surrogate data correlation they showed that the non-linear parameters (CD
dimension and original data correlation dimension and LLE) performed better in discriminating sleep
are different from each other by more than 58%. stages 1 and 2, whereas the values of spectral mea-
This rejects the null hypothesis and hence the orig- sures were distinct for stages 2 and 3. Combinations
inal data contain non-linear features. of spectral and non-linear measures yielded a bet-
ter overall discrimination of sleep stages than spec-
tral measures alone.
4. Discussion
The cortex becomes more inactive as the person 5. Conclusion
goes through from one sleep stage to the next
stage, until sleep 4 state. Hence, less number of In this work, we have analyzed the cortical func-
neurons will be available for processing the infor- tioning at different sleep stages using the non-
mation and as a result the entropy, CD, LLE and H linear parameters: FD, CD, max , ApEn and Hurst
fall. But in sleep 5 (REM) state, the brain is very exponent. These values decrease indicating the
active in this state, almost to the level at which reduction in the disorder from sleep states 0 to 4,
it is when a person is awake. Blood flow to the due to the lesser number of available neurons in
brain is also increased during this stage of sleep. each state for processing. But in sleep 5 state, these
As a result, the cortex becomes more active and values increase due to the highly active cortex. The
Non-linear analysis of EEG signals at various sleep stages 45

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