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Computer Methods and Programs in Biomedicine: Reza Boostani, Foroozan Karimzadeh, Mohammad Nami
Computer Methods and Programs in Biomedicine: Reza Boostani, Foroozan Karimzadeh, Mohammad Nami
a r t i c l e i n f o a b s t r a c t
Article history: Background and objective: Proper scoring of sleep stages can give clinical information on diagnosing pa-
Received 7 August 2016 tients with sleep disorders. Since traditional visual scoring of the entire sleep is highly time-consuming
Revised 17 November 2016
and dependent to experts’ experience, automatic schemes based on electroencephalogram (EEG) analysis
Accepted 5 December 2016
are broadly developed to solve these problems. This review presents an overview on the most suitable
methods in terms of preprocessing, feature extraction, feature selection and classifier adopted to precisely
Keywords: discriminate the sleep stages.
Sleep stage classification Methods: This study round up a wide range of research findings concerning the application of the sleep
Wavelet transform stage classification. The fundamental qualitative methods along with the state-of-the-art quantitative
Random forest classifier
techniques for sleep stage scoring are comprehensively introduced. Moreover, according to the results
Entropy
of the investigated studies, five research papers are chosen and practically implemented on a well-known
public available sleep EEG dataset. They are applied to single-channel EEG of 40 subjects containing equal
number of healthy and patient individuals. Feature extraction and classification schemes are assessed
in terms of accuracy and robustness against noise. Furthermore, an additional implementation phase is
added to this research in which all combinations of the implemented features and classifiers are consid-
ered to find the best combination for sleep analysis.
Results: According to our achieved results on both groups, entropy of wavelet coefficients along with
random forest classifier are chosen as the best feature and classifier, respectively. The mentioned feature
and classifier provide 87.06% accuracy on healthy subjects and 69.05% on patient group.
Conclusions: In this paper, the road map of EEG-base sleep stage scoring methods is clearly sketched. Im-
plementing the state-of-the-art methods and even their combination on both healthy and patient datasets
indicates that although the accuracy on healthy subjects are remarkable, the results for the main commu-
nity (patient group) by the quantitative methods are not promising yet. The reasons rise from adopting
non-matched sleep EEG features from other signal processing fields such as communication. As a con-
clusion, developing sleep pattern-related features deem necessary to enhance the performance of this
process.
© 2016 Elsevier Ireland Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.cmpb.2016.12.004
0169-2607/© 2016 Elsevier Ireland Ltd. All rights reserved.
78 R. Boostani et al. / Computer Methods and Programs in Biomedicine 140 (2017) 77–91
Fig. 1. This figure illustrates Wake, N1, N2, N3, REM stages, from top to bottom
panels, respectively.
Fig. 2. Distribution of research papers by year of publication from 20 0 0 to 2015. Fig. 3. Automatic sleep stage classification process.
sleep time (TST), sleep efficiency (SE) and REM stage measures achieve an accurate automated (expert-independent) method for
while it affected the quantification of sleep latency, wakes after sleep stage scoring.
sleep onset (WASO) and the distribution of NREM sleep stages. Based on the available literature, the quantitative sleep stage
These result in implications both in the clinical and research fields. scoring schemes comprises 3 common steps include preprocessing,
According to the AASM manual, each of the five stages is feature extraction and classification. Furthermore, in some papers,
defined below and also illustrated in Fig. 1: feature selection step is added following feature extraction in
order to find suitable subset of features [35]. What follows is
• W: Awake state (stage W) is characterized by alpha or faster introducing more frequent techniques in each step. The process for
frequency bands occupying more than 50% of the epoch, automatic sleep stage scoring is schematically illustrated in Fig. 3.
frequent eye movements and high EMG tone.
• N1: Stage N1 is scored when alpha occupies more than 50% 2.2.1. Preprocessing
of epoch while theta activity, slow rolling eye movements and The presence of artifacts might lead to the misinterpreta-
vertex waves are evident. tion, inaccuracy and distorted quantitative results; therefore, a
• N2: Stage N2 is scored when sleep spindles or K-complexes preprocessing step is necessary to remove artifacts and magnify
(less than 3 min apart) are noted. informative components of raw EEG signals prior to any further
• N3: Stage N3 is characterized by delta activity detected in over analysis [36]. There are biasing factors which potentially affect the
20% of the epoch length. accuracy of sleep EEG scoring [26]. These factors can be measure-
• REM: Upon sleep scoring an epoch is marked as REM when ment noise, physiological factors (including psycho-physiological
saw-tooth waves along with rapid eye movements as well as variants and aging) and pathological conditions (such as disordered
lowest EMG signals are observed through each epoch. sleep breathing and REM behavioral disorder) [30,37].
Despite hardware filtering during the recording, EEG signals
2.2. Quantitative assessment are still contaminated by other noise sources [38]. Diffuse artifacts
may mask cerebral activity and simulate sleep phasic events
Several automatic sleep stage classification methods are pre- (sharp vertex waves, K-complexes). Moreover, some noises and
sented in the literature [33,34]. To demonstrate the growing artifacts are created by the measurement apparatus. The power
interest on sleep stage classification, the number of papers pub- line interference (the 50/60 Hz components) or movements of the
lished in 28 relevant journals from the year 20 0 0 to 2015 are wires and electrodes can impose changes in the baseline charac-
shown in Table 2. Among such publications, “Computer Methods teristics of signals. Moreover, some artifacts are originated from
and Program in Biomedicine” and “Neuroscience Methods” are of non-cerebral sources such as eye movement, muscle and cardiac
the greatest interest. sources. Rolling eye movements happen upon the consciousness
As demonstrated in Fig. 2, the rate of publications has remained while in REM sleep the eye movements acquire saccadic patterns.
steady between 20 0 0 and 20 09, while it has quickly increased In addition, given the comparatively high amplitude level of ECG
from 2010 to 2015. This may indicate the recent growing attention signals, the QRS complex regularly interfere in the EEG signals
and joint cooperation of biomedical engineers and practitioners to causing spiky pattern [39]. Muscle activities generate EMG signals
80 R. Boostani et al. / Computer Methods and Programs in Biomedicine 140 (2017) 77–91
Table 2
Distribution of research papers by journal.
which can corrupt and distort EEG signals, especially during the isting papers, we can observe that Symmlet and Daubechies
arousal periods [26,40]. Further to the instrumental and biological mother wavelets are the most common used wavelets for EEG
artifacts, inter-individual variability of background activity and processing [46].
phasic events as well as age-related changes may influence the • Blind Source Separation (BSS): An alternative artifact removal
sleep stage scoring. On the other hand, focal cerebral lesions might approach is BSS algorithms. Independent Component Analysis
decrease phasic event’s amplitude, density and therefore mimic (ICA) [39,40]is one of the well-known BSS methods to produce
the REM pattern. In patients with wake or nocturnal epilepsy, the de-correlated brain source signals after fading the artifacts. By
interictal EEG epileptic activity may similarly mask sleep activity calculating the energy of source signals and using a threshold,
or bias sleep EEG phasic events [6]. Consequently, the above the independent signals with lower energy level will be elim-
biasing factors may hinder accurate scoring and emphasize the inated. Finally, with an inverse transform, the denoised signals
role of preprocessing in order to avoid deceiving clinical results will project back into the spatio-temporal domain.
both in visual and automatic scoring.
After the preprocessing step, based on the mentioned criteria,
Several methods are proposed in order to attenuate or elim-
EEG records are segmented into the successive 30 sec epochs
inate the effects of artifacts in EEG signals. These methods are
with no overlap, after which, further analysis are carried out at
described below:
each epoch.
• Digital Filtering: It covers a vast class of different filters
which can be linear or non-linear. To pre-process raw EEGs, 2.2.2. Feature extraction
it is common to apply a band-pass filter (e.g. Butterworth) to Features are descriptive values that project the content of a
eliminate the undesired parts. In order to eliminate the power signal from a special aspect. Usually, different types of features are
line noise from the signals, a digital Notch filter is utilized extracted from a windowed signal; therefore, to avoid collecting
[38]. Band-pass filters [41] such as Butterworth [38] are used redundant information, the elicited features should be as inde-
to reduce the muscle artifacts and eliminate linear trends pendent as possible. Extracting informative, discriminative and
[42]. Further to the linear filtering, adaptive filters are used to independent features is a crucial step to prepare a suitable set
remove the effects of the EOG and ECG artifacts in which the of values for a classifier [47]. A wide variety of signal processing
frequency contents overlaps with EEG spectrum [43]. techniques are utilized to extract discriminative information from
• Regression: Regression methods are able to learn a signal be- the EEG signals in order to automatically classify the sleep stages
havior. If an additive color noise distorts the EEGs, a regression [10,36]. Features can be totally divided into four categories (Time
method is used to learn this trend and therefore by modeling domain, Frequency domain, Time-Frequency domain, Nonlinear)
the color noise, it can be subtracted from the recorded signal which are briefly discussed below:
[44].
Time Domain Features. Time domain features can represent
• Wavelet Transform (WT): WT decomposes a signal into its
the morphological characteristics of a signal. They are simply
sub-bands. By calculating the energy in each sub-band and
interpretable and suitable for real-time applications. Some of the
applying a threshold, the noisy and undesired bands are elim-
widespread time-base features are described below:
inated [45]. Since there are many mother wavelet functions,
the one with highest similarity to the nature of EEG (in terms • Statistical Parameters: 1st to 4th-order moments of time series
of frequency bands) should be selected. Reviewing the ex- i.e., mean, standard deviation, skewness and kurtosis, respec-
R. Boostani et al. / Computer Methods and Programs in Biomedicine 140 (2017) 77–91 81
Table 3
Time domainfeatures.
tively [25,41], median and 25th, 75th percentile of the signal to model the two others. To solve this problem, some criteria
distribution [35] are known as the most effective time domain such as Akaike’s information criterion (AIC) [54] are introduced
features for EEG signals. Their mathematic formulas are pre- in the literature [55].
sented in Table 3. They are not only applied to EEG signals but • Non-parametric methods: In non-parametric approaches, PSD
also used to extract features from the other biological signals values are calculated directly from the signal samples in a
including EOG and EMG [13,38]. given windowed signal. They are based on Fourier transform
• Hjorth Parameters: Hjorth parameters are introduced by Bo [56]. Among non-parametric methods, Periodogram and Welch
Hjorth in 1970 [48]. These parameters include Activity (Ha ), [57] schemes are general for calculating PSD and extracting
Mobility (Hm ) and Complexity (Hc ) as the measure of variance features from EEGs. Easy implementation based on Fast Fourier
of a time series (x), proportion of standard deviation of the Transform (FFT) algorithm is the merit of non-parametric
power spectrum and change in the frequency, respectively. methods; however, they gain low frequency resolution when
They are widely applied features for EEG analysis [41,49] and the signal interval becomes short.
described below.
Higher Order Spectra (HOS). HOS is another method used to
Ha = var (x(t )) (1) extract frequency domain features. HOS techniques are employed
in several biomedical applications [58]. HOS represents the fre-
quency content of higher order statics of signals (cumulants)
var (x(t ) dx
dt
) [59,60]. Power spectrum equals to second-order spectra which
Hm = (2)
var (x(t )) lose the phase information. Also, the 3rd order spectrum is known
as bi-spectrum which is showed in Eq. (5).
Hm (x(t ) dx
dt
)
Hc = (3) B( f1 , f2 ) = E[X ( f1 )X ( f2 )X ∗ ( f1 + f2 )] (5)
Hm (x(t ))
where E[.] is expectation operator, X(f) is the Fourier transform of
• Zero Crossing Rate (ZCR): ZCR represents number of times that
the signal and f is the frequency.
a signal crosses the baseline (Eq. (4). The baseline can be
The advantage of using HOS is its ability to reveal non-Gaussian
obtained by taking a mean value from a windowed signal [41].
and nonlinearity characteristics of the data [58,60]. Since EEG is
It measures the number of sign-changes through a windowed
a complex signal subject to some non-linear interaction in its
signal. Given the differences in quality and the appearance of
frequency components, HOS methods are useful approaches in
the each sleep stage in the time domain, ZCR may vary from
analyzing sleep EEG signals [59].
one stage to another; as such, it can be used as a suitable
feature for sleep stage classification [25,35,50]. Nevertheless
ZCR is highly sensitive to additive noises. Time-Frequency Domain Features. Due to the non-stationary
nature of EEG signal, i.e. variation in its properties during the
ZCR = count {n|(xn xn−1 ) < 0} (4) time, a wide range of time-frequency methods are utilized as an
efficient tool in this field. There are three ways to transfer a signal
Frequency Domain Features. Frequency domain features are ver- into the time-frequency plane including signal decomposition,
satile features which are repeatedly utilized for describing changes energy distribution and modeling. The first two ways are utilized
in EEG signals [7,14,38,51,52]. There are several approaches to in the sleep applications [33,61] (explained below).
extract frequency features, herewith summarized.
Spectral Estimation. To obtain spectral characteristics of EEG
• Signal Decomposition: These methods decompose signals to a
signals, first, time series should be transferred to the frequency series of basis functions. Short Time Fourier transform (STFT)
domain. Due to the stochastic nature of EEG signals, signal au- is a very simple time-frequency analysis. In this method, first,
tocorrelation needs to be estimated first. Then, by taking Fourier signal is uniformly windowed and then FT is applied to each
transform (FT) from the autocorrelation function, Power Spectral window as described in Eq. (6).
+∞
Density (PSD) is achieved. The two approaches to estimate PSD of a
windowed signal include parametric and non-parametric methods. ST F Tx (t, f ) = x(τ )h∗ (τ − t ) exp(− j2π f τ ) dτ (6)
−∞
• Parametric methods: parametric methods are model-based where h(.) is a window function.
approaches in which the spectrum is estimated by the signal To use this method as a means of feature extraction, the
model. Autoregressive (AR), Moving average (MA) and Autore- issue of time and frequency resolution need to be well noted.
gressive moving average (ARMA) are amongst popular methods There is an inverse relationship between the length of the
in EEG processing [53]. When signals have low SNR and long window and the time resolution. In addition, the time and
length, parametric approaches present a smoother and better frequency resolutions have an trade-off together. For instance,
estimation of power spectra. However, model order determina- the shorter the data segment, the higher the time resolution
tion of AR is a main concern in such methods, since AR is able will be achieved and therefore frequency resolution decreased.
82 R. Boostani et al. / Computer Methods and Programs in Biomedicine 140 (2017) 77–91
However, a fixed specific length of the window is considered Several entropy and complexity measures such as Renyi’s
to determine STFT leading to a limited frequency resolution. Entropy [33], Sample Entropy [7], Tsallis Entropy [64], Permuta-
Wavelet Transform (WT) is a popular time-frequency trans- tion Entropy [34], Lempel–Ziv [41], Multi Scale Entropy (MSE)
formation that applies different filters to decompose a signal [20] and Approximate Entropy (ApEn) [67] are introduced in the
into dyadic frequency scales. These filters are generated from literature. They have enough potential to serve as informative
a function which called mother wavelet. Both discrete and features in sleep stage classification [10].
continuous forms of WT are utilized for sleep classification • Fractal-based: Constructing a noisy-like shape can be done
[33,62]. Continuous Wavelet Transform formula of a given by repeatedly applying an operator on a geometric element.
signal of x(t) is shown in Eq. (7). Several phenomena exist which have a noisy behavior while
they are rule-base in nature. For instance, the behavior of EEG
Wa,s = x(t )φa,s (t )dt (7) signals or shape of leaves in a tree look random while one
can hardly claim that creating EEG signals or leaves in a tree
where a and s are scale and time shifting parameters, respec- are random. For the first time a novel method is proposed by
tively. φ a,s is mother wavelet transformation which is defined Mandelbrot [69] to measure the fractal dimension of irregular
as: shapes. The concept of fractal dimension can describe the
1
t − s behavior of random-like shape by determining the amount of
φa,s (t ) = φ (8) self-similarity on that given shape or signal. There are many
|a| a
fractal-based methods like Correlation Dimension [59], Lyapanov
WT is a powerful method since it describes the signal into exponent [41] and Hurst exponent [38] which first map a signal
different frequency resolutions where the decomposed signals into the phase space and then measures the self-similarity of its
are orthogonal in most mother wavelets. In addition, a colored trajectory shape. In other words, instead of analyzing a signal in
noise cannot invade all of the wavelet features in different the time domain, these methods analyze its trajectory behavior
scales [46]. in the phase space, in terms of self-similarity. There are some
• Energy Distribution (ED): ED represents the distribution of en- other methods determining the roughness or irregularity of the
ergy simultaneously through both time and frequency domains. signal in the time domain such as Katz [70], Petrosian [35] and
Several methods are placed in this category. Choi–Williams dis- Higuchi fractal dimension (HFD) [41]. Experimental results from
tribution (CWD), is energy conservative which maintains time different studies have suggested that measuring the behavior
shifts as well as the frequency shifts. These characteristics make in the phase space is more accurate than the same in the time
it a favorable method for the time-frequency analysis [33,63]. domain, though it imposes a higher computational burden [70].
Wigner-Ville distribution (WVD) is another non-linear time-
frequency method which is widely used to analyze non- 2.2.3. Feature selection
stationary signals. However, the presence of cross-terms in the In some sleep stage classification methods especially in multi-
time-frequency domain for multi-component non-stationary channel approaches, feature selection techniques are applied
signals hinder its efficiency. Therefore, the smoothed pseudo after the feature extraction stage to find discriminative subset of
Wigner–Ville distribution (SPWVD) (the modified version of features. The purpose of adding feature selection part is to obtain
WVD) is proposed to avoid the effects of cross-terms [61], as minimum number of features without redundancy while produc-
described in Eq. (9). ing higher accuracy. Furthermore, it avoids the issue of over-fitting
τ ∗ τ
and reduce the computational time. Since an overnight PSG record
S(t, f ) = h (τ ) f ( u − t )x u + x u− du is large, feature selection is useful especially once different types
2 2 of features are extracted.
×exp(− jwτ )dτ (9) To this end, some statistical techniques are proposed in the
literature. These techniques try to find appropriate and discrim-
where f(.) and h(.) are the time and frequency smoothing
inative subset of features to distinguish different sleep stages.
functions, respectively.
Sequential forward selection (SFS) [15] and sequential backward
In addition, Hilbert–Huang Transform (HHT) is a new method
selection (SBS) [15,71] are two simple strategies to explore through
in analyzing nonlinear and non-stationary signals such as EEGs.
the features and find a proper subset. Nevertheless, SFS and SBS
It is recently employed in many applications in biomedical
highly suffers from the lack of backtracking. In addition, feature
fields including sleep stage scoring [33].
extraction algorithms such as Principal Component Analysis (PCA)
and Linear Discriminant Analysis (LDA) [72] are used for feature
Non-linear features. Since EEG signals exhibit non-linear charac- reduction. On the other hand, meta-heuristic algorithms like
teristics and complex dynamics [64], non-linear measures are used Genetic Algorithm (GA) [66] and Particle Swarm Optimization
as effective techniques for EEG processing [65,66]. They are also [73] are repeatedly used for feature selection.
widespread in sleep stage scoring to extract efficient features from
sleep EEG [15,18,65,67,68]. Non-linear methods are mainly divided 2.2.4. Classification
into two categories described as follows: Various classifiers are utilized to classify the elicited features
and assign a sleep stage into each epoch. These classifiers are
• Entropy and complexity-based: Entropy-based methods calculate learned to construct linear/non-linear boundaries to separate
the irregularity and impurity of a signal in the time domain feature vectors of different classes. Some of the popular classifiers
[66]. In other words, the more the changing patterns inside used in sleep stage scoring are herewith explained.
a windowed signal get regular, the less would be the entropy
value of that windowed signal and vice versa. The most famous • K-Nearest Neighbor (KNN): This is a local classifier which is
entropy measure is introduced by Shannon as described below: suitable for multi-modal distribution data. In other words,
when the samples of a certain class are modularly scattered
Entropy(X ) = −iN=1 Pi Ln(Pi ) (10) in different locations of the feature space, even flexible and
strong classifiers cannot accurately put a boundary around this
where N is the number of samples and Pi is the probability of localities. KNN assigns a label to an input patterns based on
ith sample. the majority vote of its k-nearest samples [57].
R. Boostani et al. / Computer Methods and Programs in Biomedicine 140 (2017) 77–91 83
1
1
for patients with sleep abnormalities, these methods should have
g ( x | μi , i ) = exp − (x − μi )T i−1 (x − μi ) (19) high performance in patients’ recorded signals. To the best of our
(2π )D/2 |i | 2 knowledge, evidence on various methods on a specific dataset
where T is the sign of vector transform. acquired from patients with sleep disorders are thin. The present
In fact, the independent Gaussian functions with different review is an attempt to discuss the most recent automatic sleep
weights can model every arbitrary distribution functions. In stage classification methods using single-channel EEG data.
order to use GMM as a classifier, the distribution of input
features of each class is learned by a GMM where each GMM 3.1. Polysomnographic datasets
acquires a specific label, as illustrated in Fig 6. Consequently,
when a sample is entered to the parallel GMMs, its label Two EEG datasets which are available on-line in the data repos-
is assigned according to the label of the given GMM which itory physionet [91] have been employed in this study. The first
produces the highest probability. dataset contains EEG signals belong to healthy subjects whereas
R. Boostani et al. / Computer Methods and Programs in Biomedicine 140 (2017) 77–91 85
|B ( f 1 , f 2 )| sample.
pn = (22) 3: Identify the Entropy of these successive samples as a sample
|B ( f 1 , f 2 )|
entropy feature.
is the non-redundant region in Fig. 8
• Sum of logarithmic amplitude of bi-spectrum:
Afterwards, these weighted features are applied to KNN
H1 = log(|B( f1 , f2 )| ) (23) classifier, where K is set to 30 through the cross validation phase.
86 R. Boostani et al. / Computer Methods and Programs in Biomedicine 140 (2017) 77–91
1
REnt = log2 (in=1 Piα ) (27)
1−α the classification accuracy of sleep stages on both groups. The
where Pi is the histogram distribution belonged to the coefficients results in Fig. 9 are presented as an average for all sleep stages,
of each mentioned time-frequency algorithms in each band with while Table 4, illustrates the classification accuracy of those meth-
n bins. α is the order of Renyi’s entropy. When α equals to 1, the ods on just normal subjects upon the entire sleep. Moreover, a
Renyi’s Entropy converge to Shannon Entropy. short description of each method is presented in Table 4.
These entropy values are extracted from the sub-bands of The best performance in terms of accuracy belongs to the
each time-frequency transforms, separately. In their proposed 5th approach in which entropy of CWT and RF are chosen as
method an assessment is carried out by applying the entropy the features and classifier, respectively. Apparently, this approach
values, belong to each transform, to a random forest (contains 10 provide over 80% classification accuracy in average over the whole
trees) classifier. According to the obtained results, the CWT feature sleep stages. Moreover, to better understand the misclassification
provides the highest accuracy, compared to the others. among stages and reveal the affection of classes on each other, the
mean percentage of accuracy for 2 by 2 stages for the approach
4. Results with higher total accuracy (i.e. 5th approach) is demonstrated
in Table 5. This table is similar to what confusion matrix (CM)
After investigating the results from five elegant studies, their present, but it is not exactly CM since CM is defined for 2 classes,
methods are applied to the present datasets (containing healthy but here we have 5 classes. According to the obtained results,
subjects and patients) as described in Section 3. The employed Among all sleep stages, the classification accuracies of the W stage
datasets are annotated by experts according to R&K rules [92,93]. and N2 have shown the best performance, while the classification
Since AASM is an improved and more recent standard for sleep of stage N1 and REM have the lowest performance, respectively.
stage scoring, to match the results with this standard, S3 and S4 stage N1 mostly misclassified with stage W, N2 and REM, while
are merged into one stage (N3). These five methods are evaluated more than 20% of stage REM was classified as stage N2.
in terms of classification accuracy and their robustness against Moreover, as demonstrated in Fig. 9, the accuracy of five
additive noise (with different SNRs). To find the best combination methods on the RBD dataset is reduced more than 25% in av-
of features and classifier for achieving accurate and reliable re- erage. Although the accuracy of all methods has decreased for
sults, here, additional implementations are suggested and executed the patients’ dataset, the 5th method again presented the best
by applying the deployed features by the mentioned papers to classification performance.
different classifiers including: RF, KNN, LDA+NC and GMM. On the other hand, when comparing these five approaches from
To proceed to the preprocessing phase, the raw signals are fairly the robustness point of view, white Gaussian noise is added to the
cleaned by applying a bandpass Butterworth filter (order 5 with raw signals with different levels of SNR and then the whole pro-
frequency cutoff between 0.5 − 35 Hz) to remove the base-line cess is executed. The SNR levels are 1, 10, 20 dB. Since the results
drift and linear trends. Next, EEGs are segmented into successive of patients are not comparable to normals, additive noises are just
30 s epochs and then the features and classifier of each paper are added to the raw normal signals. According to the results which
separately executed to those epochs in order to produce the results are shown in Fig. 10, The 5th method shows of the lowest sensi-
on both groups. The accuracies of each sleep stage classification tivity to noise compared to others, even at different SNR levels.
method are demonstrated in Table 4. Results have emerged from As mentioned earlier, the present study add an additional
a cross validation phase in which features vector of one subject is phase to find the best combination among features and classifiers.
considered as the test set and the rest of subjects are considered As such, the feature sets of each approach is applied to the four
as the train sets. This substitution for constructing new train and classifiers (RF, KNN, LDA+NC, GMM). According to the results
test sets is continued in parallel up to the number of subjects. This (Fig 11), random forest classifier produce the best classifier for all
cross validation is called leave-one(subject)-out in which the train different sets of features. Moreover, the highest accuracy is belong
and test sets of subjects are selected totally blinded to each other. to the time-frequency domain features (i.e. CWT using different
Since the main concern of automatic methods is the accurate mother wavelets) along with random forest classifier (87.49%).
detection of the sleep stages for abnormalities in patients records,
to make a real evaluation among these papers on real patients, 5. Discussion and conclusion
here the methodologies of the papers are applied to both normal
and patient groups. Not surprisingly, lower performance on pa- The aim of this study is to carry out a comprehensive review
tients is expected compared to the normal groups. Fig. 9 illustrates on automatic sleep stage classification methods. This investigation
R. Boostani et al. / Computer Methods and Programs in Biomedicine 140 (2017) 77–91 87
Table 4
Brief description of each method along with their obtained total accuracy (mean± standard deviation (std)).
1 Acharya et al. 2010 4 features; HOS based features - GMM Classifier 77.25 ± 0.43
[59]
2 Fraiwan et al. 2010 21 features; Continuous Wavelet Transform (CWT) - LDA+NC Classifier 80.76 ± 0.06
[46] using 3 mother wavelets: reverse bioorthogonal
(rbio3.3), Daubechies (db20), and Gauss of order 1
(gauss1), Shannon Entropy.
3 Gunes et al. 2010 129 features; Welch spectral analysis; k-means 4 features: Max, Min, KNN Classifier 71.81 ± 0.18
[57] clustering based feature weighting (KMCFW). Mean, Std of
previous features
4 Liang et al. 2012 21 features; Multiscale Entropy (MSE) and - LDA+NC Classifier 75.15 ± 0.09
[20] Autoregressive (AR) coefficients.
5 Fraiwan et al. 2012 7 feature; Continuous wavelet transform (CWT), - Random Forest 87.06 ± 0.09
[33] Choi-Williams distribution (CWD), Hilbert-Huang Classifier
Transform (HHT) and Renyi’s Entropy measures.
the state-of-the-art studies, five papers are selected and discussed through the time domain while other related features may fail to
with regard to their performance. The pros and cons of their detect such information. Nevertheless, the main flaw of AR model
methods are discussed below. is its high sensitivity to additive noises since these coefficients are
determined by auto-correlation functions.
5.1. Evaluation of features
5.1.3. Time-frequency features
The suggested EEG features in those papers (illustrated in Since Fourier transform fails to reveal the frequency and time
Table 4) can be totally divided into four categories: spectrum-base resolution simultaneously, time-frequency domain transforms are
features, time-frequency features, time features, fractal & entropy developed. These transforms can be divided in two categories, i.e.
features. linear and nonlinear. Famous linear transforms are the continuous
and discrete Wavelet transform and STFT. Nonlinear transforms
such as spectrogram and Choi–Williams can demonstrate the en-
5.1.1. Spectrum-base features ergy distribution of a signal, while similar to HOS, they suffer from
Spectrum estimation methods are repeatedly used in sleep the effect of cross-terms in a very low frequency band signals like
stage classification studies based on which sleep stages are marked EEGs. Wavelet transform decomposes frequency content of a signal
with specific frequency ranges and are classified accordingly. To in a dyadic manner matched to the standard EEG frequency bands.
estimate the frequency content of each epoch, parametric (e.g. AR, In other words, Wavelet acts as a bank of filters to decompose
ARMA), non-parametric (e.g. periodogram, Welch) and HOS meth- signals into their sub-bands. Since sleep stage transition depends
ods are vastly utilized. Based on the existing evidences, the elicited on both the EEG frequency band changes and amplitude variations
features by Welch method could better distinguish the sleep stages wavelet features may efficiently detect the stage transition (similar
than other parametric methods. This supremacy roots in the lower to frequency features). The main advantage of Wavelet features
sensitivity of non-parametric methods to the still remaining compare to the spectrum-base features is that such features do
motion artifacts and noises as compared to the parametric and not involve in calculating inaccurate auto-correlation functions.
cumulant-base methods. This is because non-parametric methods Moreover, Wavelet transform can be applied to a whole epoch
(e.g. Welch method) need to estimate just one auto-correlation since it is not sensitive to the non-stationary property of EEG
function while parametric ones have to construct a matrix of auto- signals. In addition, unlike Welch method, no averaging is taken
correlation functions. Each auto-correlation function has a bias to determine the wavelet coefficients throughout an epoch. In
and variance; therefore, the calculation of auto-correlation matrix conclusion, Wavelet transform retain comparative advantages to
while taking an inverse from it, subject to great bias and variance the other time-frequency domain transforms in EEG analysis. It
to this estimation. In addition, impact of bias and variance of a should be noted that for this specific application, CWT provides
cumulant function is much worse than that of an auto-correlation more separable features than that of DWT in terms of frequency
function leading to the deterioration of HOS results. resolution within the same time frame. In addition, wavelet co-
On the other hand, HOS is capable of revealing the phase- efficients calculated by CWT are more redundant than DWT. This
coupling inside of a signal as well as frequency behavior of their redundancy provides more stable elicited features for sleep stage
corresponding cumulant. Since HOS of a signal presents in the classification problem leading to a higher accuracy [11].
form of a surface in bi-frequency space, it contains unique in-
formation and several features can be elicited from this space as 5.1.4. Fractal and entropy features
compare to other spectrum-base methods. Furthermore, bispectral Since EEG signals behave irregularly, fractal and entropy meth-
analysis of EEG signals during the surgical operation can finely ods are suitable to measure the amount of the roughness captured
estimate the depth of anesthesia [58]. Given the similarity of inside the signal. As the entropy of a signal is increased, its infor-
anesthesia to sleep in some extent, HOS features are expected to mation contents is inclined, accordingly. In other words, as a signal
provide discriminant values for different stages of sleep. Moreover, behaves more irregular, fractal dimension and entropy of the signal
higher-order cumulants easily remove the additive Gaussian noise. are increased. When a sleep stage is changed, the efficient fre-
In the case of sleep signals, if the movement artifact and other quency bandwidth along with the signal amplitude varies accord-
additive noises have Gaussian distribution, HOS can eliminate ingly. Therefore, it is expected that fractal and entropy measures
them perfectly. However, cumulant estimation impose a high can finely describe each sleep stage. Although these measures are
computational burden, due to several multiplication of the signal somehow correlated to each other, the way of determination of
with its shifted versions. The main flaw of HOS application raise entropy is less sensitive to noise rather than that of the fractal
from the narrow band content of EEGs and also creating a lot of dimension. Accurate computation of fractal dimension and entropy
cross-terms in this thin frequency band. needs a large number of samples making their application limited
for analyzing short time signals (e.g. an EEG epoch). Nevertheless,
5.1.2. Time features ApEn is a fast entropy measure at the cost of loosening the accu-
Based on the discussed publications, time domain features are racy. Standard EEG bands are defined by their frequency bandwidth
frequently used for sleep EEG analysis. The main reason of using and amplitude variations, while entropy and fractal measures are
such features is that the amplitude of EEG signals significantly not designed to capture the signal bandwidth. Therefore, these fea-
varies from one sleep stage to another one. So far, AR coefficients, tures might appear effective in detecting just the stage transitions.
Hjorth parameters, statistical parameters of the time domain
signals (e.g. variance, skewness, kurtosis and MSE), are suggested 5.2. Classifiers
as discriminative features for sleep analysis. Among the methods
discussed, AR model is frequently used for EEG analysis, and also The final phase of automatic sleep stage scoring is classifica-
provides good results for discriminating depth of hypnosis [94], tion. Some of the most used classifiers in this field are compared
identifying the depth of anesthesia [95] as well as sleep stage anal- in this study (outlined in Fig. 11). Among the compared classifiers,
ysis [20]. As such, AR coefficients can be considered as a versatile RF produces the highest sleep stage classification for different
feature for different EEG applications. The main advantage of AR types of feature sets introduced in the five selected publications
model is to encode the time behavior of EEG into few coefficients. (Fig. 11). Random forest is fast for large scale samples, it does
In other word, AR coefficients elicit under-layer dynamics of EEGs not over-fit, has shown a great performance in several real world
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