Islam 2016
Islam 2016
ScienceDirect
www.sciencedirect.com
a
Department of Electrical and Computer Engineering, National University of Singapore, Singapore
b
Department of Electrical Engineering, University of Malayer, Malayer, Iran
KEYWORDS Summary Electroencephalography (EEG) is the most popular brain activity recording tech-
Ambulatory EEG; nique used in wide range of applications. One of the commonly faced problems in EEG recordings
Artifact removal; is the presence of artifacts that come from sources other than brain and contaminate the
Brain-computer acquired signals significantly. Therefore, much research over the past 15 years has focused on
interface (BCI); identifying ways for handling such artifacts in the preprocessing stage. However, this is still an
Empirical mode active area of research as no single existing artifact detection/removal method is complete
decomposition (EMD); or universal. This article presents an extensive review of the existing state-of-the-art artifact
Independent detection and removal methods from scalp EEG for all potential EEG-based applications and
component analysis analyses the pros and cons of each method. First, a general overview of the different artifact
(ICA); types that are found in scalp EEG and their effect on particular applications are presented.
Scalp EEG; In addition, the methods are compared based on their ability to remove certain types of arti-
Wavelet transform facts and their suitability in relevant applications (only functional comparison is provided not
performance evaluation of methods). Finally, the future direction and expected challenges of
current research is discussed. Therefore, this review is expected to be helpful for interested
researchers who will develop and/or apply artifact handling algorithm/technique in future for
their applications as well as for those willing to improve the existing algorithms or propose a
new solution in this particular area of research.
© 2016 Elsevier Masson SAS. All rights reserved.
∗ Corresponding author.
E-mail address: [email protected] (A. Rastegarnia).
http://dx.doi.org/10.1016/j.neucli.2016.07.002
0987-7053/© 2016 Elsevier Masson SAS. All rights reserved.
288 M.K. Islam et al.
Figure 1 Left: a scalp EEG segment where all channels are more or less contaminated with muscle activity during the 10 seconds.
Right: the 10-second scalp EEG recordings with 21 channels from a long-term Epilepsy Monitoring Unit (OSG EEG recorders, Rumst,
Belgium). The seizure EEG was contaminated with muscle artifacts and eye blinks. Muscle artifacts can be observed between 0 sec
and 3.9 sec on channels F7, T3, T5, C3, and T1 and between 5 sec and 10 sec on channels F8, T4, F4, C4, and P4 [16].
Physiological/internal Extra-physiological/external
Eye blink ECG pulse Chewing Gloss kinetic Electrode Electrical Head
Eye movement Swallowing Skin Displacement Magnetic movement
Eye flatter Clenching Respiration and pop-up Sound Body
REM sleep Sniffing Cable Optical movement
Talking movement EM waves Limbs
Scalp Poor ground movement
contraction Tremor
Other
movements
Scalp EEG artifacts 291
Artifact detection
Artifact removal
• availability of a reference artifact source;
• the number of available recording channels;
Artifact removal involves canceling or correcting the arti-
• the need for removing the artifacts after detection stage.
facts without distorting the signal of interest. This is
primarily done in two ways: either by filtering and regres-
A few existing methods adopted the idea of machine sion or by separating/decomposing the EEG data into other
learning for artifact separation from useful EEG signal by domains.
training a classifier with (supervised) or without (unsuper-
vised) labeled training datasets. Once artifactual epochs
are identified by applying a machine learning algorithm, Regression
such epochs are either highlighted as artifact annotator to Regression analysis [43,101], using a multi-modal linear
the clinicians for helping in decision making (e.g. epileptic model between observed and a reference signal, is a
seizure detection) or can be rejected before examina- traditional way of identifying artifactual samples and con-
tion from clinician or before sending to automated signal sequently removing such sample that do not belong to the
processing system [70]. model. Observed artifact-contaminated EEG signal and an
Machine learning techniques are mainly two types: super- artifact reference signal are common methods for remov-
vised and unsupervised learning. Among supervised learning ing some physiological artifacts such as ocular and cardiac
algorithms, two most popular methods used for classifica- artifacts.
tion between artifact and brain signals are artificial neural However, such regression analysis often fails when there
network (ANN) [11,38,40,57,83] and support vector machine is no reference channel available. In addition, EEG signal
(SVM) [6,44,70,71,85,87]. Among unsupervised learning, k- being non-linear and non-stationary process, linear regres-
means clustering and outlier detection are most common sion is not the best choice for analysis in such applications.
in this particular area of research [70]. A basic approach Moreover, it can only be used to treat few particular types
to classify artifact from EEG by using the machine learning of artifact, not all types.
classifier is shown in Fig. 2.
xa,L [n] = xa−1,L [2n − k]g[k] (6) is shown in Table 4. EEMD: it is an enhanced version of
k=1
EMD (enhanced empirical mode decomposition) and inspired
from the fact that EMD algorithm is very sensitive to noise,
N
which often leads to mode mixing complication. Therefore,
xa,H [n] = xa−1,L [2n − k]h[k] (7) EEMD is proposed which uses an average number of ensem-
k=1 bles (IMFs) from EMD as the optimal IMFs thus it provides a
where g[n] is a low pass filter just like scaling function and noise-assisted data analysis method [94].
h[n] is a high pass filter just like mother wavelet function.
Briefly, discrete wavelet transform is entering of a signal into Adaptive filtering
a low pass filter to get the low frequency component and An adaptive filter is a system with a linear filter that has
into a high pass filter to get the high frequency component. a transfer function controlled by variable parameters and
An example structure of 2-level decomposition by discrete a means to adjust those parameters according to an opti-
wavelet transform is shown in Fig. 4 [51]. mization algorithm [89]. The filter weights can adapt based
Once the signal is decomposed into detail and approxi- on the feedback from output of the system and it requires
mate coefficients, thresholding is applied on the coefficients a reference input to compare the desired output with the
to denoise the signal from artifacts. Then the new sets of observed output. An improved adaptive filtering by opti-
coefficients (all detail with final level approx. coefficients) mal projection which is based on common spatial pattern
are added up to reconstruct back the artifact-reduced sig- for artifact removal is mentioned in [9,10], especially for
nal. epilepsy patient’s EEG [74]. Let s[n] denote the observed
signal which is combination of the original EEG, x[n] and
Empirical mode decomposition additive artifact r[n]. Then, if the artifact source v[n] is
EMD is an empirical and data-driven method developed to available from a dedicated channel (e.g. EOG or ECG); an
perform on non-stationary, non-linear, stochastic processes adaptive algorithm (e.g. LMS, RLS, etc.) can be used to
and therefore it is ideally suitable for EEG signal analysis and derive an artifact-free EEG, x [n] given that the desired EEG
processing. However, the computational complexity of EMD and artifact signal are independent (or at least uncorrelated
is quite heavy, so may not be suitable for online applications. [91]). An illustration of the use of adaptive filter for EOG
Moreover, the theory behind EMD is still not complete and artifact removal is shown in Fig. 5.
so far used in empirical studies, therefore it is difficult to
predict its robustness in all EEG recordings. Principal component analysis (PCA)
EMD algorithm decomposes a signal, s[n] into a sum PCA is a type of spatial filter that transforms the time
of the band-limited components/functions, c[n] called domain datasets into a different space by rotating axes in
294 M.K. Islam et al.
EMD-ICA or EMD-CCA
Removal performance
Table 5 Comparative analysis of artifact removal methods found in literature published in recognized journals.
Table 5 (Continued)
Table 5 (Continued)
Nicolaou EOG, EMG and ECG TDSEP + LAMIC N/A Y EOG Multi Discovery and
et al. [64] analysis of ERP
Rashed-Al- Ocular EMD N/A Y Simulated Multi BCI
Mahfuz
et al. [77]
Guerrero- Ocular Adaptive N/A Y Fpl, Fp2, F7 Multi General
Mosquera filtering + ICA and F8
et al. [31] Electrodes
Mammone Ocular + muscle + EAWICA N Y N Multi General
et al. [52] electrical shift (wICA)
Winkler EOG + EMG TDSEP (based Y Y N Multi BCI
et al. on ICA) + LPM
[104]
Chen et al. Muscle EEMD-JBSS N/A Y N Single General + ictal
[16] EEG
Zeng et al. EOG SSA N N N Multi Diagnosis
[108] (BSS) + EMD
knowledge, no real-time hardware implementation has been ocular artifacts for portable EEG applications which is
performed. found to achieve lower MSE and higher correlation between
cleaned and original EEG in comparison with existing
methods such as wavelet packet transform (WPT) and
Single or multi-channel independent component analysis (ICA), discrete wavelet
transform (DWT) and adaptive noise cancellation (ANC).
BSS-based methods require multi-channels to function, the Another article [43] reported an automated ocular artifact
more number of channels the better for separating indi- removal method using adaptive filtering and ICA with the
vidual sources. Therefore, such methods cannot be used help of vertical (vEOG) and horizontal (hEOG) EOG channel
in low-channel (e.g. 4—6) or single-channel based appli- as reference. On the other hand, Flexer et al. [27] pro-
cations (e.g. in ambulatory monitoring of epilepsy patient posed an ICA-based ocular artifact removal method from
or ambulatory BCI-prosthesis). On the other hand, Wavelet blind subjects’ EEG utilizing both vertical and horizontal
transform and EMD-based techniques can work with single- EOG references.
channel analysis by decomposing a single data sequence into
multiple components (approx./detail coefficient for wavelet
decomposition and IMF for EMD). ECG
Authors in [21] proposed removal/reduction of ECG/cardiac
artifacts from EEG using a separate ECG reference channel.
Reference channel In [31], an automatic method based on a modified ICA algo-
rithm has been proposed that works for a single-channel EEG
Most of the available methods require a dedicated arti- and the ECG (as reference) which gives promising results
fact channel to be functional. In order to remove ocular or when compared with two popular methods that use a refer-
cardiac artifacts, the reference channel often provides sat- ence channel namely ensemble average subtraction (EAS)
isfactory complementary information to identify ECG/EOG and adaptive filtering. The other two articles proposed
artifacts. Besides, real-time contact impedance measure- their methods for application in neonatal EEG monitoring.
ment can provide the complementary information about Another paper [60] proposed a combination of EMD and
artifacts due to electrode pop, movement or loose con- adaptive filtering based method for ECG artifact removal
nection. Some movement tracking devices such as motion in preterm EEG and reported up to 17% improvement in cor-
captured camera, accelerometer and/or gyroscope can help relation coefficient between original and cleaned datasets
to detect motion artifacts. compared with removal by only adaptive filtering.
not only captures ocular events but also some frontal EEG from a high-density EEG recordings (248-channel) with the
events. Besides, in practical daily applications, the use of help of kinematics and kinetics information acquired from a
eye tracker removes the requirement of EOG electrodes 8-camera, 120 frames/s, motion capture system. The sub-
attached to the face. Results in [42] show significantly ject was asked to walk and run on a custom built, dual-belt,
improved performance in removing of only eye movement force measuring treadmill with two 24-inwide belts mounted
artifacts by combining Kalman filter with the eye tracker flush with the floor while simultaneously both brain and
information compared with three other popular methods body dynamics were recorded. The findings conclude that
namely Regression, PCA, and SOBI. On the other hand, high-density EEG is possible to use in order to study brain
Noureddin et al. [68] introduced an online algorithm for ocu- dynamics during whole body movements; and the artifact
lar artifacts (both movements and blink) removal from EEG from rhythmic gait events can be reduced by template
by utilizing a high-speed eye tracker (> 400 Hz) along with regression procedure.
the frontal EEG as reference instead of EOG channel. The
article used two adaptive filters (RLS and H) to prove the
Robustness
efficacy of their proposed technique, which was shown to
outperform the techniques using only EOG as reference.
Robustness is an important issue in developing any arti-
fact removal algorithm as artifacts are of diverse types and
Accelerometer contaminate the EEG differently in different recording envi-
There are few articles reported to have used accelerometer ronments. Some of the factors that should be considered for
recordings in conjunction with EEG recordings for detecting robustness include artifact-SNR, type of artifact, duration
motion artifacts [82,93]. In [82], it has been shown that of artifacts, subject-variability, environmental variability,
movement artifacts can be detected automatically using application-specificity.
an accelerometer with a developed algorithm based on AR
modeling and thus can increase the speed efficiency for
automatic computation of EEG model parameters compared Discussion
with manual detection of movement artifacts. Sweeney
reported in [93] that the use of accelerometer as refer- Current status
ence channel not only can detect motion artifacts but also
can remove them with the use of different filtering tech- Although significant amount of efforts has been made to
niques such as adaptive filters, Kalman filtering and Wiener develop methods for artifact detection and removal in EEG
filtering. applications, it is still an active area of research. Most of
them handle single type of artifact, many of them cannot
Gyroscope work for single-channel EEG, some of them require training
Authors in [71] proposed to detect different head movement data, some require a dedicated reference channel, some are
artifacts automatically by using a gyroscope as complemen- designed for general purpose applications that often leads
tary features in fusion with EEG features and finally with to overcorrection of data and some of them are not fully
the help of SVM, to classify artifacts from neural informa- automated. Some of the currently available major software
tion. The method is inspired by the realization of an artifact plug-in GUIs are discussed in Appendix B.
detection system for implementing with the point-of-care
REACT (Real-time EEG Analysis for event detection) tech- Future direction
nology that has potential application in the detection of
neurological events (e.g. seizure events) in adults. The arti- Here we present the future direction for handling artifacts
facts were generated for 10 different types of head-related by raising realistic issues, proposing some ideas and provid-
movements using 14-channel Emotiv EEG headset and the ing recommendation based on review of existing solutions.
movement time was recorded for validation during arti-
fact detection. The reported accuracy in terms of Avg. ROC
Probability mapping
areas was 0.802 and 0.907 for participant independent and
From the above literature review of existing solutions for
dependent systems respectively.
artifact handling, it is obvious that artifacts are of dif-
ferent types and not all types will play major role in all
Contact impedance measurement EEG-based applications. Sometimes, clinicians prefer man-
Bertrand et al. and Mihajlovic et al. [5,55,56] reported that ual event detection than automated algorithm for certain
by measuring the change in contact impedance due to head disease diagnosis (e.g. seizure detection). However, such
movements can help to estimate the motion artifacts and by manual analysis is also time-consuming. In such cases, if we
utilizing this information with an adaptive filter in combina- can give the users an option to choose which particular arti-
tion with band-pass filtering, the artifacts can be reduced facts they want to be detected and/or removed with what
significantly in real-time. The article also studies the effect amount (%) for each epoch or data-segment of duration 1-
of head movement artifacts on EEG recordings results in sec (depends on application), then the process would still
contaminating the spectral domain in < 20 Hz frequency. be automated with tuning facilities for the users either to
turn-ON or remain OFF if not required. In order to imple-
Motion captured camera ment such facility, a probability mapping of artifacts can
Authors in [32] proposed a channel and IC-based method be proposed (something similar to the idea of [105]) for
to remove movement artifacts during walking and running each epoch of data based on some statistical features to
300 M.K. Islam et al.
quantify the probability of an epoch to be artifactual. Then movement in an ambulatory environment [15]. Thus, it will
the user can opt for some threshold of probability above be easier to label both ground truth EEG and artifacts.
which he/she may want to remove artifacts while below
the threshold, to preserve the epoch as it is. Thus it is pos- Recommendation
sible to design automated artifact detection and removal In order to choose the right artifact handling method, we
algorithm, which is application-specific with tuning facil- need to consider the particular application, required spec-
ity for user. This would greatly enhance the signal analysis ification to be satisfied given the computational resources
process by avoiding the chance of removing important sig- and recording environment available. There are EEG appli-
nal information. In addition, it will reduce the unnecessary cations where only one or two types of artifacts affect the
computational resources and time by focusing on the desired later stage information decoding or processing, thus it is not
artifacts for detection/removal (i.e. only those types to be wise to attempt to identify and remove all the artifacts as
expected to affect the signal quality) and ignoring the rest other artifacts may not (or minimally) harm a particular sig-
of them. nal processing purpose. If any reference channel is available
in the targeted application, then regression or adaptive fil-
tering technique may be a preferred solution. In the case
Standard performance evaluation of ambulatory EEG monitoring, when number of channels
One of the important issues in evaluating the perfor- are fewer, no reference channel is available and wireless
mance of any artifact detection or removal method is EEG transfer preferred, in such case it is recommended to
that there is no universal standard quantitative metric use computationally cheaper method that can work without
for the researchers to use. Most of the methods men- reference and on single or few channels, e.g. wavelet-based
tioned in the literature use some qualitative time/frequency methods since BSS-based methods may not perform satisfac-
domain plot to evaluate the artifact removal performance tory with less number of channels. In some applications, if
or evaluated by the clinical expert. Sweeney et al. [92] it is possible to have some a priori knowledge about arti-
proposed a recording methodology for accurate evalua- facts and some training data available, and the application
tion and comparison between different artifact removal only require to identify artifacts not to remove them, then
techniques/algorithms which presented the EEG recordings machine learning based classifiers can be good choice. If the
of two separate but highly-correlated channels that allow EEG recording involves high-density channels, then PCA may
recording both artifact-contaminated and artifact-free sig- be preferred to reduce the dimensionality before applying
nal simultaneously. It also presented a tagging algorithm any artifact removal methods, such as BSS-based methods.
employing two accelerometers for generating a quality-of- If the application is based on offline analysis, then we can
signal (QOS) metric, which can be used to for multiple afford some computational expensive techniques such as ICA
purposes such as classification of motion artifacts, activation or EMD.
of artifact removal technique only when required and iden-
tification of the artifact-contaminated epochs. Thus, this
approach can provide accurate measurements of quantita- Conclusions
tive metrics for fair performance evaluation.
However, such methodology still requires intervention to An extensive analysis of the existing methods for arti-
the recording technique and also extra reference channel fact detection and removal has been presented with their
for accelerometer data, which may not be feasible in every comparison, advantages and limitations. The research on
application (e.g. portable EEG recordings). Although it is handling artifacts present in the typical EEG recordings is
highly encouraged for the removal performance to be evalu- still an active area of research and none of the existing
ated by the domain experts, however, such evaluation varies methods can be considered as the perfect solution. Most
from one expert to another and still is manual and/or qual- of the solutions do not consider the particular application,
itative evaluation. Therefore, it is an urge to have a single therefore, not optimized for that application. Although,
standard evaluation method consists of both qualitative and most of the removal algorithms provide good performance,
more importantly quantitative metrics or ways for evaluat- however, they are only suitable for offline analysis because
ing the performance in a more realistic and fair manner. of their high computational complexity and unsupervised
nature. Some of them even require a dedicated reference
channel, which is not feasible for some applications. Fur-
Ground truth data ther studies are required to characterize the properties of
Another reason of not being able to evaluate artifact commonly encountered artifacts and to observe the effects
removal performance fairly is that the lack of availability of their contamination to the desired later stage signal
of ground truth data. It’s now equally important to have processing/analysis. Some applications may only require to
a public database with sufficiently long-term EEG recor- identify artifacts and not to remove them, e.g. in appli-
dings without or minimal artifacts to be used as a ground cations where classification/identification of two classes
truth data. Besides such, an acceptable mathematical model are required. In such cases, a more realistic mathematical
to generate basic EEG rhythms and finally integrate them model of the desired event(s) to be identified is essential in
to simulate an EEG sequence with standard 10—20 system order to easily ignore other non-brain signals (i.e. artifacts
EEG channels is required for quantitative evaluation of any or interferences). Finally, the future direction will be to
existing/future artifact removal methods. In addition, more provide application-specific solutions with reasonable com-
study is necessary to characterize as much as possible of all plexity, optimized performance and most importantly with
artifact types, specially the motion artifacts for different feasible solutions.
Scalp EEG artifacts 301
Disclosure of interest in 0.5—29 Hz [26]. These bands and their FFT or spectral
power are useful features for separating artifacts from EEG.
The authors declare that they have no competing interest. FFT, F: Fast Fourier Transform or FFT is the frequency
representation of time domain signal values. For feature
extraction, we have used the mean of the absolute of FFT
Acknowledgments values for each epoch computed over the entire frequency
range of EEG signal (i.e. 0—128 Hz).
This work was supported by A*STAR PSF Grant R-263-000-
699-305 and NUS YIA Grant R-263-000-A29-133. F = mean(abs[FFT (k)]) (12)
Maximum FFT, Fmax : This feature is the maximum or peak
Appendix A. Statistical features value of the absolute of FFT values.
Fmax = max(abs[FFT (k)]) (13)
Time Domain Features
Spatial Features
Entropy, H: is a measure of uncertainty of information
content [78], of a discrete random variable x with possible
values x1 , ..., xn , can be calculated as: Spatial distribution or topographic mapping helps to iden-
tify the origin of many artifacts (e.g. ocular artifacts are
H(x) = E[− ln(P(x))] (8) dominant in frontal EEG channels) [93]. In addition, some
artifacts may appear in several nearby channels (global arti-
Here E is the expected value operator and P(x) is the facts such as eye blink) where some appear only in one
probability mass function of x. channel (i.e. local artifacts). Therefore, spatial features
Kurtosis, Kr: Kurtosis is the measure of ‘‘peakedness’’ of along with their spectral content are important to identify
probability distribution function [50] and is calculated for a artifacts from EEG signals [57,88].
real-valued random variable x as follows
4 Appendix B. Software plug-ins
Kr[x] = (9)
4
where and are the mean and standard deviation of ran- FORCe
dom variable x.
Line Length, L[n]: Line length, a signal feature for Fully Online and automated artifact Removal for brain-
seizure onset detection as reported by [24,59], for a discrete Computer interfacing or FORCe is the most recent method
time signal x[k] can be represented by, reported in [18] that is based on a unique combination of
WT, ICA and thresholding. Compared with two other state-
n
of-the-art methods namely LAMIC and FASTER, FORCe has
L[n] = abs[x[k − 1] − x[k]] (10)
been shown to outperform them significantly and is capa-
k=n−N
ble of removing different types of artifacts including eye
where N is the time window length. Here N = 1 sec. blink, EOG and EMG. One of salient features of FORCe is
Maximum, M: It is the maximum or peak value of an that it doesn’t require any reference channel and can oper-
epoch and noted down as a feature. ate on fewer numbers of channels which makes it suitable
NEO, : The ability of Non-linear Energy Operator (NEO) for ambulatory EEG applications.
to enhance signal’s transition or large amplitude event
[53,57,75] is sometimes considered as feature for seizure FASTER
classification. The NEO operator applied to a discrete time
variable x[n] is calculated as follows
FASTER stands for Fully Automated Statistical Thresholding
2
[x[n]] = x[n] − x[n + 1]x[n − 1] (11) for EEG artifact Rejection which is an unsupervised algo-
rithm for parameter estimation in both EEG time series and
Usually the mean and/or variance of [x[n]] for each in the ICs of EEG [66]. The achieved sensitivity and speci-
epoch are used as feature(s). ficity is > 90% for detection of EOG and EMG artifacts, linear
trends and white noise in the contaminated channels.
Frequency Domain Features
LAMIC
Spectral features along with temporal or spatial features are
often used for EEG classification. As mentioned before, EEG Lagged auto-mutual information clustering (LAMIC) is a clus-
rhythms have different spectral bands, therefore sometimes tering algorithm developed for automatic artifact removal
the relative power in those bands are used as features for from EEG [64]. The method involves data decomposition
classifier training. It is important to note that apart from the by a BSS algorithm called TDSEP (Temporal De-correlation
rhythms, there are recently reported High Frequency Oscil- source SEParation), which is a temporal extension of ICA.
lations (HFO having band of 80—200 Hz), Ripple (200—600 Hz) Then the components are clustered using the similarity of
bands present in EEG. In addition, the frequency band of typ- their lagged Auto-Mutual Information (AMI). This is inspired
ical Scalp EEG is 0.05—128 Hz while epileptic seizure appears from the fact that EEG and artifacts are different from their
302 M.K. Islam et al.
temporal dynamics point of view. The clustering procedure artifact-specific spatial and temporal features to automat-
follows the usual steps of hierarchical clustering. ically identify the artifactual ICs after ICA is performed.
Four different artifact types (i.e. eye blink, vertical eye
PureEEG movement, horizontal eye movement and generic disconti-
nuities) are chosen for extracting features such as temporal
kurtosis, spatial average and variance difference, maximum
This is an automatic EEG artifact removal algorithm for
epoch variance, spatial eye difference. The key feature of
epilepsy monitoring that based on a neurophysiological
ADJUST is that it is entirely automated and unsupervised
model by utilizing an iterative Bayesian estimation scheme
with reported accuracy of 95.2% in classifying all of the four
[35]. The method targets to remove most of the artifact
artifacts. It can also successfully reconstruct the clean ERP
types and does not require any manual intervention. The
topographies from heavy artifact-contamination.
authors reported the performance of PureEEG from two
independent clinical experts perspective and its found to
be significantly improving the readability of EEG recordings
after artifact removal. PREP Pipeline
pulse artifact and a method for its subtraction. Neuroimage preprocessing refines neonatal seizure detection. Clin Neu-
1998;8:229—39. rophysiol 2011;122:2345—54.
[3] Allen PJ, Josephs O, Turner R. A method for removing imaging [22] Delorme A, Makeig S. EEGLAB: an open source toolbox for
artifact from continuous EEG recorded during functional MRI. analysis of single-trial EEG dynamics including independent
Neuroimage 2000;12:230—9. component analysis. J Neurosci Methods 2004;134:9—21.
[4] Anderson CW, Knight JN, O’Connor T, Kirby MJ, Sokolov A. [23] Devuyst S, Dutoit T, Stenuit P, Kerkhofs M, Stanus E. Cancelling
Geometric subspace methods and time-delay embedding for ECG artifacts in EEG using a modified independent compo-
EEG artifact removal and classification. IEEE Trans Neural Syst nent analysis approach. EURASIP J Advances Signal Process
Rehabil Eng 2006;14:142—6. 2008;2008:180.
[5] Bertrand A, Mihajlovic V, Grundlehner B, Hoof CV, Moonen M. [24] Esteller R, Echauz J, Tcheng T, Litt B, Pless B. Line length: an
Motion artifact reduction in EEG recordings using multichan- efficient feature for seizure onset detection. In: Proceedings
nel contact impedance measurements. In: Proceedings of IEEE of the 23rd Annual International Conference of the IEEE Engi-
Biomedical Circuits and Systems Conference (BioCAS). 2013. neering in Medicine and Biology Society. 2001. p. 1707—10.
p. 258—61. [25] Ferdowsi S, Sanei S, Abolghasemi V, Nottage J, O’Daly
[6] Bhattacharyya S, Biswas A, Mukherjee J, Majumdar AK, O. Removing ballistocardiogram artifact from EEG using
Majumdar B, Mukherjee S, et al. Detection of artifacts short and long-term linear predictor. IEEE Trans Biomed Eng
from high energy bursts in neonatal EEG. Comput Biol Med 2013;60:1900—11.
2013;43:1804—14. [26] Fisher RS, Vickrey BG, Gibson P, Hermann B, Penovich
[7] Bigdely-Shamlo N, Mullen T, Kothe C, Su KM, Robbins KA. The P, Scherer A, et al. The impact of epilepsy from the
prep pipeline: standardized preprocessing for large-scale EEG patient’s perspective I. Descriptions and subjective percep-
analysis. Front Neuroinformatics 2015;9:1—20. tions. Epilepsy Res 2000;41:39—51.
[8] Bono V, Jamal W, Das S, Maharatna K. Artifact reduction in [27] Flexer A, Bauer H, Pripfl J, Dorffner G, Using ICA. for removal
multichannel pervasive EEG using hybrid WPT-ICA and WPT- of ocular artifacts in EEG recorded from blind subjects. Neural
EMD signal decomposition techniques. In: Proceedings of IEEE Netw 2005;18:998—1005.
Acoustics, Speech and Signal Processing (ICASSP). 2014. p. [28] Ge S, Han M, Hong X. A fully automatic ocular artifact removal
5864—8. from EEG based on fourth-order tensor method. Biomed Eng
[9] Boudet S, Peyrodie L, Gallois P, Vasseur C. Filtering by optimal Lett 2014;4:55—63.
projection and application to automatic artifact removal from [29] Gomez-Herrero G. Automatic artifact removal (AAR) toolbox
EEG. Signal Process 2007;87:1978—92. v1. 3 (release 09. 12. 2007) for MATLAB. Tampere University
[10] Boudet S, Peyrodie L, Forzy G, Pinti A, Toumi H, Gallois P. of Technology; 2007.
Improvements of adaptive filtering by optimal projection to [30] Groppe DM, Makeig S, Kutas M. Identifying reliable inde-
filter different artifact types on long duration EEG recordings. pendent components via split-half comparisons. Neuroimage
Comput Methods Programs Biomed 2012;108:234—49. 2009;45:1199—211.
[11] Burger C, Heever DJVD. Removal of EOG artefacts by com- [31] Guerrero-Mosquera C, Navia-Vazquez A. Automatic removal
bining wavelet neural network and independent component of ocular artifacts using adaptive filtering and independent
analysis. Biomed Signal Process Control 2015;15:67—79. component analysis for electroencephalogram data. IET Sig-
[12] Calcagno S, Foresta FL, Versaci M. Independent component nal Process 2012;6:99—106.
analysis and discrete wavelet transform for artifact removal [32] Gwin JT, Gramann K, Makeig S, Ferris DP. Removal of move-
in biomedical signal processing. Am J Appl Sci 2014;11:57—68. ment artifact from high-density EEG recorded during walking
[13] Cassani R, Falk TH, Fraga FJ, Kanda PA, Anghinah R. and running. J Neurophysiol 2010;103:3526—34.
The effects of automated artifact removal algorithms on [33] Hallez H, De Vos M, Vanrumste B, Van Hese P, Assecondi S, Van
electroencephalography-based Alzheimer’s disease diagnosis. Laere KP, et al. Removing muscle and eye artifacts using blind
Front Aging Neurosci 2014;6:55. source separation techniques in ictal EEG source imaging. Clin
[14] Castellanos NP, Makarov VA. Recovering EEG brain signals: Neurophysiol 2009;120:1262—72.
artifact suppression with wavelet enhanced independent [34] Hamaneh MB, Chitravas N, Kaiboriboon K, Lhatoo SD,
component analysis. J Neurosci Methods 2006;158:300—12. Loparo K, et al. Automated removal of EKG artifact from
[15] Chang BS, Schachter SC, Schomer DL. Atlas of ambulatory EEG data using independent component analysis and con-
EEG. Academic Press; 2005. p. 56—74. tinuous wavelet transformation. IEEE Trans Biomed Eng
[16] Chen X, He C, Peng H. Removal of muscle artifacts from 2014;61:1634—41.
single-channel EEG based on ensemble empirical mode [35] Hartmann M, Schindler K, Gebbink T, Gritsch G, Kluge T. Pure
decomposition and multiset canonical correlation analysis. J EEG: Automatic EEG artifact removal for epilepsy monitoring.
Appl Math 2014. Neurophysiol Clin 2014;44:479—90.
[17] Cohen MX. Analyzing neural time series data: theory and [36] Hirsch L, Brenner R. Atlas of EEG in critical care. John Wiley
practice. MIT Press; 2014. p. 51—4. and Sons Ltd; 2010. p. 187—216.
[18] Daly I, Scherer R, Billinger M, Muller-Putz G. Force: [37] Hsu WY, Lin CH, Hsu HJ, Chen PH, Chen IR. Wavelet-based
fully online and automated artifact removal for brain- envelope features with automatic EOG artifact removal:
computer interfacing. IEEE Trans Neural Syst Rehabil Eng application to single-trial EEG data. Expert Syst Appl
2015;23:725—36. 2012;39:2743—9.
[19] De Clercq W, Vanrumste B, Papy JM, Van Paesschen W, Van [38] Hu J, Wang CS, Wu M, Du YX, He Y, She H. Removal of EOG and
Huffel S. Modeling common dynamics in multichannel signals EMG artifacts from EEG using combination of functional link
with applications to artifact and background removal in EEG neural network and adaptive neural fuzzy inference system.
recordings. IEEE Trans Biomed Eng 2005;52:2006—15. Neurocomputing 2015;151:278—87.
[20] De Clercq W, Vergult A, Vanrumste B, Van Paesschen W, Van [39] Islam MK, Rastegarnia A, Yang Z. A wavelet-based artifact
Huffel S. Canonical correlation analysis applied to remove reduction from scalp EEG for epileptic seizure detection. IEEE
muscle artifacts from the electroencephalogram. IEEE Trans J Biomed Health Inform 2016;20:1321—32.
Biomed Eng 2006;53:2583—7. [40] Jafarifarmand A, Badamchizadeh MA. Artifacts removal in
[21] De Vos M, Deburchgraeve W, Cherian P, Matic V, Swarte EEG signal using a new neural network enhanced adaptive
R, Govaert P, et al. Automated artifact removal as filter. Neurocomputing 2013;103:222—31.
304 M.K. Islam et al.
[41] James CJ, Gibson OJ. Temporally constrained ICA: an appli- filtering. In: Acoustics, Speech and Signal Processing (ICASSP),
cation to artifact rejection in electromagnetic brain signal 2012 IEEE International Conference. 2012. p. 661—4.
analysis. IEEE Trans Biomed Eng 2003;50:1108—16. [61] Nazarpour K, Wongsawat Y, Sanei S, Chambers JA, Oraintara
[42] Kierkels JJ, Riani J, Bergmans JW, Van Boxtel GJ. Using an S. Removal of the eye-blink artifacts from EEGs via STF-TS
eye tracker for accurate eye movement artifact correction. modeling and robust minimum variance beamforming. IEEE
IEEE Trans Biomed Eng 2007;54:1256—67. Trans Biomed Eng 2008;55:2221—31.
[43] Klados MA, Papadelis C, Braun C, Bamidis PD. Reg-ica: a hybrid [62] Ng SC, Raveendran P. Enhanced rhythm extraction using blind
methodology combining blind source separation and regres- source separation and wavelet transform. IEEE Trans Biomed
sion techniques for the rejection of ocular artifacts. Biomed Eng 2009;56:2024—34.
Signal Process Control 2011;6:291—300. [63] Nguyen HAT, Musson J, Li F, Wang W, Zhang G, Xu R, et al. EOG
[44] Lawhern V, Hairston WD, McDowell K, Westerfield M, Robbins artifact removal using a wavelet neural network. Neurocom-
K. Detection and classification of subject-generated artifacts puting 2012;97:374—89.
in EEG signals using autoregressive models. J Neurosci Meth- [64] Nicolaou N, Nasuto SJ. Automatic artefact removal from
ods 2012;208:181—9. event-related potentials via clustering. J VLSI Signal Process
[45] LeVan P, Urrestarazu E, Gotman J. A system for automatic Syst Signal Image Video Technol 2007;48:173—83.
artifact removal in ictal scalp EEG based on independent com- [65] Niedermeyer E, Da Silva FL. Electroencephalography: basic
ponent analysis and Bayesian classification. Clin Neurophysiol principles, clinical applications, and related fields. 5th edi-
2006;117:912—27. tion Lippincott Williams & Wilkins; 2004.
[46] Li Y, Ma Z, Lu W, Li Y. Automatic removal of the eye blink [66] Nolan H, Whelan R, Reilly R. Faster: fully automated sta-
artifact from EEG using an ICA-based template matching tistical thresholding for EEG artifact rejection. J Neurosci
approach. Physiol Meas 2006;27:425. Methods 2010;192:152—62.
[47] Lopez-Calderon J, Luck SJ. EEPLAB: an open-source toolbox [67] Noureddin B, Lawrence PD, Birch GE. Time-frequency anal-
for the analysis of event-related potentials. Front Hum Neu- ysis of eye blinks and saccades in EOG for EEG artifact
rosci 2014;8:1—14. removal. In: Neural Engineering, 2007. CNE’07. 3rd Interna-
[48] Ma J, Bayram S, Tao P, Svetnik V. High-throughput ocular arti- tional IEEE/EMBS Conference on neural Engineering. 2007. p.
fact reduction in multichannel electroencephalography (EEG) 564—7.
using component subspace projection. J Neurosci Methods [68] Noureddin B, Lawrence PD, Birch GE. Online removal of eye
2011;196:131—40. movement and blink EEG artifacts using a high-speed eye
[49] Ma J, Bayram S, Tao P, Svetnik V. Muscle artifacts in multi- tracker. IEEE Trans Biomed Eng 2012;59:2103—10.
channel EEG: characteristics and reduction. Clin Neurophysiol [69] Oostenveld R, Fries P, Maris E, Schoffelen JM. Fieldtrip: open
2012;123:1676—86. source software for advanced analysis of MEG, EEG, and
[50] Mahajan R, Morshed BI. Unsupervised eye blink artifact invasive electrophysiological data. Comput Intell Neurosci
denoising of EEG data with modified multiscale sample 2010;2011:1—9, http://dx.doi.org/10.1155/2011/156869
entropy, kurtosis, and wavelet-ICA. IEEE J Biomed Health [Article ID 156869].
Inform 2015;19:158—65. [70] O’Regan S. Artefact detection and removal algorithms for EEG
[51] Mallat S. A wavelet tour of signal processing: the sparse way. diagnostic systems. PhD thesis. University College Cork; 2013.
3rd edition Academic press; 2008. p. 535—90. [71] O’Regan S, Faul S, Marnane W. Automatic detection of EEG
[52] Mammone N, Morabito FC. Enhanced automatic wavelet artefacts arising from head movements using EEG and gyro-
independent component analysis for electroencephalographic scope signals. Med Eng Phys 2013;35:867—74.
artifact removal. Entropy 2014;16:6553—72. [72] Park HJ, Jeong DU, Park KS. Automated detection and elim-
[53] Maragos P, Kaiser J, Quatieri T. On amplitude and frequency ination of periodic ECG artifacts in EEG using the energy
demodulation using energy operators. IEEE Trans Signal Pro- interval histogram method. IEEE Trans Biomed Eng 2002;49:
cess 1993;41:1532—50. 1526—33.
[54] Mateo J, Torres AM, Garcia MA. Eye interference reduction [73] Peng H, Hu B, Shi Q, Ratcliffe M, Zhao Q, Qi Y, et al. Removal
in electroencephalogram recordings using a radial basic func- of ocular artifacts in EEG-an improved approach combining
tion. IET Signal Process 2013;7:565—76. DWT and ANC for portable applications. IEEE J Biomed Health
[55] Mihajlovic V, Li H, Grundlehner B, Penders J, Schouten Inform 2013;17:600—7.
A. Investigating the impact of force and movements on [74] Peyrodie L, Gallois P, Boudet S, Cao H, Barbaste P, Szurhaj
impedance magnitude and EEG. In: Engineering in Medicine W. Evaluation of the AFOP/DAFOP method for automatic fil-
and Biology Society (EMBC), 2013 35th Annual International tering of EEGs of patients with epilepsy. J Clin Neurophysiol
Conference of the IEEE. 2013. p. 1466—9. 2014;31:152—61.
[56] Mihajlovic V, Patki S, Grundlehner B. The impact of head [75] Potamianos A, Maragos P. A comparison of the energy opera-
movements on EEG and contact impedance: an adaptive tor and the Hilbert transform approach to signal and speech
filtering solution for motion artifact reduction. In: Engi- demodulation. Signal Process 1994;37:95—120.
neering in Medicine and Biology Society (EMBC), 2014 [76] Rankine L, Stevenson N, Mesbah M, Boashash B. A non-
36th Annual International Conference of the IEEE. 2014. stationary model of newborn EEG. IEEE Trans Biomed Eng
p. 5064—7. 2007;54:19—28.
[57] Mognon A, Jovicich J, Bruzzone L, Buiatti M. Adjust: an auto- [77] Rashed-Al-Mahfuz M, Islam MR, Hirose K, Molla MKI. Artifact
matic EEG artifact detector based on the joint use of spatial suppression and analysis of brain activities with electroen-
and temporal features. Psychophysiology 2011;48:229—40. cephalography signals. Neural Regen Res 2013;8:1500.
[58] Molla MKI, Islam MR, Tanaka T, Rutkowski TM. Artifact sup- [78] Richman JS, Moorman JR. Physiological time-series analysis
pression from EEG signals using data adaptive time domain using approximate entropy and sample entropy. Am J Physiol
filtering. Neurocomputing 2012;97:297—308. Heart Circ Physiol 2000;278:2039—49.
[59] Mukhopadhyay S, Ray G. A new interpretation of nonlinear [79] Roy V, Shukla S. Automatic removal of artifacts from EEG
energy operator and its efficacy in spike detection. IEEE Trans signal based on spatially constrained ICA using Daubechies
Biomed Eng 1998;45:180—7. wavelet. Int J Modern Educ Comput Sci (IJMECS) 2014;6:31.
[60] Navarro X, Poree F, Carrault G. ECG removal in preterm [80] Sameni R. The Open Source Electrophysiological Toolbox
EEG combining empirical mode decomposition and adaptive (OSET). http://www.oset.ir/ [Online].
Scalp EEG artifacts 305
[81] Sameni R, Gouy-Pailler C. An iterative subspace denoising [97] Ting K, Fung P, Chang C, Chan F. Automatic correction of arti-
algorithm for removing electroencephalogram ocular arti- fact from single-trial event-related potentials by blind source
facts. J Neurosci Methods 2014;225:97—105. separation using second order statistics only. Med Eng Phys
[82] Savelainen A. Movement artifact detection from electroen- 2006;28:780—94.
cephalogram utilizing accelerometer. Master’s thesis. Aalto [98] Turnip A. Automatic artifacts removal of EEG signals
University School of Science and Technology; 2011. using robust principal component analysis. In: Technol-
[83] Schetinin V, Schult J. The combined technique for detection ogy, Informatics, Management, Engineering, and Environment
of artifacts in clinical electroencephalograms of sleep- (TIME-E), 2014 2nd International Conference. 2014. p. 331—4.
ing newborns. IEEE Trans Inf Technol Biomed 2004;8: [99] Turnip A, Junaidi E. Removal artifacts from EEG signal using
28—35. independent component analysis and principal component
[84] Seneviratne U, Mohamed A, Cook M, D’Souza W. The analysis. In: Technology, Informatics, Management, Engi-
utility of ambulatory electroencephalography in routine clin- neering, and Environment (TIME-E), 2014 2nd International
ical practice: a critical review. Epilepsy Res 2013;105: Conference. 2014. p. 296—302.
1—12. [100] Vaughan TM, Heetderks W, Trejo L, Rymer W, Weinrich M,
[85] Shao SY, Shen KQ, Ong CJ, Wilder-Smith EP, Li XP. Auto- Moore M, et al. Brain-computer interface technology: a
matic EEG artifact removal: a weighted support vector review of the second international meeting. IEEE Trans Neural
machine approach with error correction. IEEE Trans Biomed Syst Rehabil 2003;11:94—109.
Eng 2009;56:336—44. [101] Wallstrom GL, Kass RE, Miller A, Cohn JF, Fox NA. Automatic
[86] Shoker L, Sanei S, Latif M. Removal of eye blinking artifacts correction of ocular artifacts in the EEG: a comparison of
from EEG incorporating a new constrained BSS algorithm. In: regression-based and component-based methods. Int J Psy-
Engineering in Medicine and Biology Society, 2004. IEMBS’04. chophysiol 2004;53:105—19.
26th Annual International Conference of the IEEE, volume 1. [102] Wang Z, Xu P, Liu T, Tian Y, Lei X, Yao D. Robust removal of
2004. p. 909—12. ocular artifacts by combining independent component anal-
[87] Shoker L, Sanei S, Chambers JA. Artifact removal from elec- ysis and system identification. Biomed Signal Process Control
troencephalograms using a hybrid BSS-SVM algorithm. IEEE 2014;10:250—9.
Signal Process Lett 2005;12:721—4. [103] Winkler I, Haufe S, Tangermann M. Automatic classification
[88] Skupch AM, Dollfuss P, Furbass F, Gritsch G, Hartmann MM, of artifactual ICA-components for artifact removal in EEG
Perko H, et al. Spatial correlation based artifact detection signals. Behav Brain Funct 2011;7:30.
for automatic seizure detection in EEG. In: Engineering in [104] Winkler I, Brandl S, Horn F, Waldburger E, Allefeld C,
Medicine and Biology Society (EMBC). 2013. p. 1972—5. Tangermann M. Robust artifactual independent compo-
[89] Stearns SD. Adaptive signal processing. Prentice Hall; 1985. nent classification for BCI practitioners. J Neural Eng
[90] Stevenson N, Rankine L, Mesbah M, Boashash B. Newborn EEG 2014;11:035013.
seizure simulation using time—frequency signal synthesis. In: [105] Yang Z, Liu W, Keshtkaran MR, Zhou Y, Xu J, Pikov V, et al.
Proc. APRS Workshop on Digital Image Computing. 2005. p. A EC-PC threshold estimation method for in vivo neural spike
145—51. detection. J Neural Eng 2012;9:046017.
[91] Sweeney K, Ward T, McLoone S. Artifact removal in physiolog- [106] Yong X, Ward RK, Birch GE. Artifact removal in EEG using
ical signals—practices and possibilities. IEEE Trans Inf Technol morphological component analysis. In: Acoustics, Speech and
Biomed 2012;16:488—500. Signal Processing, 2009. ICASSP 2009. IEEE International Con-
[92] Sweeney K, Ayaz H, Ward TE, Izzetoglu M, McLoone SF, ference. 2009. p. 345—8.
Onaral B. A methodology for validating artifact removal tech- [107] Yong X, Ward RK, Birch GE. Generalized morphological
niques for physiological signals. IEEE Trans Inf Technol Biomed component analysis for EEG source separation and artifact
2012;16:918—26. removal. In: Neural Engineering, 2009. NER’09. 4th Interna-
[93] Sweeney K. Motion artifact processing techniques for phys- tional IEEE/EMBS Conference. 2009. p. 343—6.
iological signals. PhD thesis. National University of Ireland [108] Zeng H, Song A, Yan R, Qin H. EOG artifact correction from
Maynooth; 2013. EEG recording using stationary subspace analysis and empiri-
[94] Sweeney K, McLoone SF, Ward TE. The use of ensemble empir- cal mode decomposition. Sensors 2013;13:14839—59.
ical mode decomposition with canonical correlation analysis [109] Zhao C, Qiu T. An automatic ocular artifacts removal method
as a novel artifact removal technique. IEEE Trans Biomed Eng based on wavelet-enhanced canonical correlation analysis.
2013;60:97—105. In: Engineering in Medicine and Biology Society, EMBC, 2011
[95] Takahashi T, Cho RY, Mizuno T, Kikuchi M, Murata T, Takahashi Annual International Conference of the IEEE. 2011. p. 4191—4.
K, et al. Antipsychotics reverse abnormal EEG complexity in [110] Zhao Q, Hu B, Shi Y, Li Y, Moore P, Sun M, et al. Automatic iden-
drug-naive schizophrenia: a multiscale entropy analysis. Neu- tification and removal of ocular artifacts in EEG — improved
roimage 2010;51:173—82. adaptive predictor filtering for portable applications. IEEE
[96] Teixeira AR, Tome AM, Lang EW, Gruber P, Da Silva AM. Trans Nanobioscience 2014;13:109—17.
Automatic removal of high-amplitude artefacts from single- [111] Zou Y, Nathan V, Jafari R. Automatic identification of artifact-
channel electroencephalograms. Comput Methods Programs related independent components for artifact removal in EEG
Biomed 2006;83:125—38. recordings. IEEE J Biomed Health Inform 2016;20:73—81.