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March 28, 2012 17:8 1250001

International Journal of Neural Systems, Vol. 22, No. 2 (2012) 1250001 (16 pages)
c World Scientific Publishing Company
DOI: 10.1142/S0129065712500013

A NEW PARAMETRIC FEATURE DESCRIPTOR


FOR THE CLASSIFICATION OF EPILEPTIC AND
CONTROL EEG RECORDS IN PEDIATRIC POPULATION

MERCEDES CABRERIZO∗ , MELVIN AYALA


and MOHAMMED GORYAWALA
by UNIVERSIDADE FEDERAL DO RIO GRANDE DO SUL on 01/13/14. For personal use only.

Center for Advanced Technology and Education


College of Engineering and Computing
Florida International University
10555 West Flagler Street, Miami FL 33174, USA
Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com


cabreriz@fiu.edu
PRASANNA JAYAKAR
Brain Institute, Miami Children’s Hospital
3100 SW 62nd Ave, Miami, FL 33155, USA
MALEK ADJOUADI
Center for Advanced Technology and Education
College of Engineering and Computing
Florida International University
10555 West Flagler Street, Miami FL 33174, USA

This study evaluates the sensitivity, specificity and accuracy in associating scalp EEG to either control or
epileptic patients by means of artificial neural networks (ANNs) and support vector machines (SVMs). A
confluence of frequency and temporal parameters are extracted from the EEG to serve as input features
to well-configured ANN and SVM networks. Through these classification results, we thus can infer the
occurrence of high-risk (epileptic) as well as low risk (control) patients for potential follow up procedures.

Keywords: EEG data; temporal and frequency parameters; artificial neural networks; support vector
machines; EEG classification; epileptic versus control EEG.

1. Introduction did not.2 Similarly, another study proposes an imple-


In epilepsy research, the development of algorithms mentation of nonlinear decision functions and iden-
to automate the detection of epileptiform activity tification of multidimensional classification domains
from EEG has become a common line of investigation to detect seizures.3
for many scientists due to its potential for improv- Furthermore, recent advances in artificial intelli-
ing disease diagnosis and treatment. Examples of gence have benefited from the problem solving capa-
such efforts are reflected in our earlier work, where bilities of ANNs as exemplified by the classification of
interictal spikes from EEG recordings are detected sleep apnea syndrome based on wavelet transforms
using the Walsh transform,1 and where different back and ANN4 ; classification of seizures by determin-
propagation-based artificial neural networks (ANNs) ing the features of temporal epilepsy and the func-
are compared for extracting and assessing features tional anatomy of involved brain networks5 ; epileptic
that are best for delineating electrodes whose sig- seizure detection using time-frequency analysis and
nals contained a seizure from those with signals that ANNs6 ; classification of primary generalized epilepsy

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M. Cabrerizo et al.

by EEG signals using multilayer perceptron neural a scaled conjugate gradient (SCG) back-propagation
networks7 ; and also analysis of EEG signals by imple- algorithm in order to delineate epileptic from control
menting eigenvector methods for the classification of EEG. Such an approach could complement interest-
EEG signals.8 ing studies that have used in a unique way gamma
Support vector machine (SVM) is also a powerful activity,19,20 alpha waves by means of a coherence
method that has been investigated to classify back- measure,21 and nonlinear classification methods22,23
ground and epileptic EEG,9 where the extrema of the to address the critical neurophysiological issues that
power density spectrum served as inputs to the clas- could discriminate epileptic EEG from control EEG
sifier in order to classify different mental tasks from signals, whether a seizure is eminent or not and
EEG signals10 ; and to analyze continuous EEG sig- whether the states are interictal or pre-seizure.
nals for an asynchronous BCI application, or where However, abnormalities in the EEG in some
the inputs to the classifier are the fractal feature vec- patients are at times too subtle to be detected using
by UNIVERSIDADE FEDERAL DO RIO GRANDE DO SUL on 01/13/14. For personal use only.

tors extracted from the input EEG signals.11 conventional techniques. It is this dilemma that the
Feature extraction has been applied to EEG sig- proposed classification method is trying to address,
nals in order to obtain meaningful patterns related to by initially confining the search space to only those
Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com

a specific task or a particular biomarker (like spikes). EEG data that have a very high likelihood of being
Some studies such as the classification of EEG from recorded from epileptic patients. The objective then
healthy and Alzheimer’s subjects have used the was to establish a system for the classification of key
phase and nonlinear measurements to distinguish characteristics of EEG signals to differentiate control
the two populations12 ; classification of EEG signals EEG from epileptic EEG. Hidden signs (biomarkers)
using an extensive parametric analysis from healthy were considered as key indicators of the epileptic ten-
and epileptic subjects that employed the capabil- dency in the EEG. Consequently, this study lays out
ities of the resilient backpropagation algorithm,13 the framework in the use of key EEG features that
which is a variation of the standard back propaga- serve as input to a scaled conjugate gradient back-
tion method with a faster convergence, has yielded propagation neural network algorithm for an opti-
a 92.5% accuracy and using a new neural net- mized solution.
work model (Multi-Spiking)14 with a 90.7% accu- The proposed framework for classifying EEG
racy; detection of nonlinear interactions of the alpha data relies on a new methodology to analyze fea-
waves by applying the coherence to EEG obtained ture trends in EEG files and compares control sub-
from epileptic patients that have been treated with jects and epileptic patients as an attempt to delin-
anti-epileptic drugs15 ; identification of sleep stages eate differences between them. The method was
with an accuracy of 88.7% using a Gaussian mix- based on establishing a descriptor matrix for each
ture model (GMM) using higher order spectra of the EEG parameters used as means to character-
parameters16 ; reflection of the pathological interac- ize the unique behavior of these parameters, keeping
tion of the epileptic focus (source) with other brain the process generalized in its application and while
areas through the application of directionality mea- seeking simplicity and robustness in terms of compu-
sures based on the phase and the space topography.17 tational requirement and classification accuracy. The
By means of visual inspection, EEG experts are algorithm for computing the matrix involves sim-
often able to qualitatively distinguish specific EEG ple statistical operations on parameters across elec-
activity contained within long EEG records with trodes and across time including signal to noise ratio
the intent to diagnose a patient with epilepsy. One (SNR). The advantage of this matrix is that it can
such interesting study is in the use of the so-called be used to represent and compare EEG files regard-
recurrence quantification analysis (RQA) parame- less of the different recording durations and number
ters in order to classify the EEG signals into con- of electrodes.
trol, ictal, and interictal classes.18 The expressed The parameters investigated in this study com-
need in differentiating the three types of EEG seg- bine the Hjorth’s parameters which are activity,
ments is indeed extremely important. It is this exact mobility and complexity24,25 with spectral power in
need that is being explored here by introducing the all frequency bands. The matrices were computed
so-called GDT of parameters that serve as input to for all EEG files and were then used as inputs of a

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A New Parametric Feature Descriptor for the Classification of Epileptic and Control EEG Records

specific ANN that was trained to differentiate EEG EEG is recorded over a short period of time, usu-
recordings from epileptic patients and nonepileptic ally 20–40 min. Children with parent’s consent were
controls. encouraged to go to bed late or get up early prior
The significance of this study relates directly to to the test. Therefore, the study could include short
the unique classification process of off-line scalp EEG periods of sleep. Electrodes are applied according to
recordings to facilitate screening of potential epilep- the 10–20 system. The activation procedure or action
tic patients. The classification of EEG signals related steps such as: Hyperventilation (over-breathing for 3
to epilepsy is difficult to ascertain in the absence of to 5 min.) and Photic Stimulation (flashing lights)
seizures because one can only rely on the existence are performed during the recording. Hyperventi-
of abnormal behaviors in the EEG, such as interictal lation is performed on patients who are 4 years
spikes, which represent an area of cortical irritabil- or older, while photic stimulation is performed on
ity that may or may not be predisposed to produce patients older than 4 weeks. This is the basic EEG
by UNIVERSIDADE FEDERAL DO RIO GRANDE DO SUL on 01/13/14. For personal use only.

epileptic seizures at some point. The dilemma is that test that is used to diagnose epilepsy and other neu-
interictal spikes could be seen in control subjects who rological conditions. Such a test can confirm suspi-
never develop epilepsy, and could be related to other cion of epilepsy, but other types of tests might be
Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com

neurological disorders that may or may not be associ- needed to obtain a more accurate diagnosis. In this
ated with epilepsy at all. In addition, around 10% of study, all the patients were not taking medications
epileptic patients never show any evidence for epilep- prior to the test. The same number of electrodes (19)
tiform discharges. Other behaviors, such as abnor- following the standard 10–20 system was used for all
malities of background activity and slow activity in patients. The EEG segments selected were extracted
some regions, are much less evident than epileptiform from the portions of the EEG where the patient was
activity and cannot be easily appreciated just by relaxed and with the eyes closed (may or may not be
looking at the EEG. That is why long EEG record- asleep).
ings require the use of reliable and accurate com- Two EEG expert reviewers at Miami Children’s
puter programs that are able to extract the hidden Hospital visually selected the EEG segments that
information, so that a better diagnosis can be pro- were processed. Only EEG segments that were free
vided. Robust signal processing algorithms become of artifacts were chosen for the analysis, thus the dif-
indispensable, especially when long recordings have ferent sizes of the EEG segments where selected.
to be evaluated. Visual screening only relies on the Scalp EEG recordings from eight control subjects
EEG experts that can draw subjective conclusions and nine epileptic patients were used. The data was
at times. In this context, it is useful to automatically collected from routine EEG recordings from patients
differentiate between the two main categories of EEG and controls, without the imposition of long record-
signals: epileptic EEG versus control EEG. This can ing sessions. For an unbiased comparison of files, the
be achieved by using short segments of scalp interic- segments from the epileptic patients were extracted
tal EEG without having to record the patient for a from sections that do not include the seizure event,
long time until an event associated with epilepsy hap- which may or may not contain abnormal discharges.
pens. This last assertion is the premise of this study. Recordings were performed at Miami Children’s Hos-
pital, using XLTEK Neuroworks Ver. 3.0.5 equip-
2. Materials and Methods ment and sampled at 512 Hz and 500 Hz for both
control subjects and epileptic patients, indistinctly.
2.1. Data acquisition A total of 19 electrodes were used for the analysis
When a patient has any suspicious signs related to following the 10–20 system using a referential mon-
epilepsy, an EEG test is administered to make an tage. In total, 5 to 30 random segments per patient
appropriate diagnosis. An EEG is able to detect were extracted from all EEG recordings; to prevent
unusual activity in the brain. The test performed biasing, all segments were free of artifacts. The DC
at Miami Children’s Hospital on all the patients offset was removed from all segments. The file seg-
considered in this study was a Routine Electroen- ments from epileptic patients were only interictal (i.e.
cephalogram following established guidelines. The without seizure activity). All files were 4 to 45 s long.
patient is placed in a dark and quiet room and scalp The patients’ information is given in Table 1.

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M. Cabrerizo et al.

Table 1. Patients’ information and number of files used in the study (E: epileptic, C: control).

Patient # Epileptic (E) Age Gender Diagnosis Number of files


control (C)

1 C 15 F Control EEG 10
2 C 10 M Control EEG 15
3 C 17 M Control EEG 20
4 C 18 F Control EEG 5
5 C 8 M Control EEG 5
6 C 12 M Control EEG 12
7 C 15 F Control EEG 14
8 C 12 M Control EEG 14
9 E 7 M Focal area of epileptogenesis within left frontal 20
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region involving frontal pole and posterior frontal


lobe near the midline region primarily
10 E 4 F Intractable seizures over the right 30
frontocentro-temporal epileptogenicity
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11 E 15 F Medically intractable seizures with epileptogenicity 10


involving both frontal regions
12 E 2 M Diffuse cerebral dysfunction and a region of epileptic 5
activity over the left posterior temporal area. An
area of potential epileptogenicity in the left
frontocentral region as well
13 E 10 F Syndrome: Symptomatic partial epilepsy; Etiology: 5
Left temporal lobe dysplasia
14 E 8 M Occasional right parietal temporal discharges. An 11
indication of potential epileptogenic focus in the
right parietal temporal region
15 E 14 M Generalized 3–3.5 Hz spike wave discharges not 6
associated with altered responsiveness. Generalized
potential epileptic dysfunction
16 E 1 M Discharges in the left frontal temporal region. These 17
results indicate a potential epileptogenic focal
dysfunction
17 E 15 M Generalized epileptiform activity suggestive of 14
primary generalized epilepsy; however a few
fragmented discharges were predominant over the
left frontocentral region

Two hundred and thirteen scalp EEG files from Frequency parameters were added to the inves-
17 patients were evaluated by calculating tempo- tigation because frequency analysis in scalp and
ral and frequency parameters using nonoverlapping intracranial EEG has proven to be quite useful for
1-second windows. pre-surgical evaluation.26–30 The span in the fre-
quency domain stopped at the 44 Hz because dur-
ing the preliminary evaluation, spectral power in the
2.2. Research method EEG file segments was found to be very low for
The research method focused on investigating the frequencies above 44 Hz.
merits of nine EEG parameters, namely activity,
mobility, complexity, and spectral power in the
frequency bands delta (< 4 Hz), theta (4 to less 2.3. Organizational structure of the
classification process
than 8 Hz), alpha (8 to less than 13 Hz), beta I
(13 to less than 20 Hz), beta II (20 to less than Figure 1 illustrates the flowchart describing the oper-
36 Hz), and low gamma (36 to less than 44 Hz). ational structure of the algorithm, which consists of

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A New Parametric Feature Descriptor for the Classification of Epileptic and Control EEG Records

then split into training and testing data using


the 50/25/25 partitioning rule;
(3) Running the Classification Analysis: In the train-
ing phase, an ANN with distinct weights is estab-
lished, and in the testing phase, the classifier is
tested on the dataset previously selected, and the
results are contrasted with those obtained using
the SVM methods.

Once these steps are accomplished, the classi-


fier performance is then evaluated. The classifier is
defined as the one that yielded the highest accuracy
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as well as the highest sensitivity (i.e. smallest number


of false negatives).
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2.4. Mathematical model for generating


the global parametric features
The extraction of parameters from EEG has been a
common practice in epilepsy research with applica-
tions ranging from interictal spike detection, seizure
detection, and up to prediction. What this study pro-
poses is to consolidate the contribution of each of
these parameters in a unique way not found previ-
ously in the literature.
An appendix is provided to show the formulas
with brief descriptions of the nine parameters that
were used in this study. Figures 2 and 3 illustrate
in detail the computational steps that were taken in
order to extract the different features that quantify
these parameters, in terms of what we refer to as the
global parametric features (GPF). These features are
structured into a 3 × 3 matrix, and are sought for
each of the nine parameters considered, thus the 81
features that are used as input to the ANN/SVM
networks, which along with the N segments of the
EEG make up the N × 81 GDT.
The 3 × 3 structure as shown in Table 2 is the
Fig. 1. Flowchart of the working steps of the proposed result of determining for each EEG segment through
classification strategy.
1-second windows, the average, standard deviation
and SNR across time along each EEG record (time
the following steps: series or temporal features) in one dimension and
across all electrodes (inter-electrode features) in the
(1) Collection of Data: A descriptor for each param- other dimension. The temporal features are denoted
eter is extracted from all EEG segments for each through small case acronyms (avg, std, snr) and
subject; inter-electrode features are denoted through upper
(2) Organization of Data: Descriptors from all EEG case acronyms (AVG, STD and SNR). Consequently
segments and for all nine parameters are stored notation avg (AVG) denotes the temporal average
in a parametric table referred to as the global (avg) of the inter-electrode average (AVG), and
descriptor table (GDT) — this GDT table is likewise std (SNR) is the temporal standard (std)

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M. Cabrerizo et al.
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Fig. 2. (a) Extraction of a parameter Xn from 1-second


windows; (b) Extraction of inter-electrode average and
(c) Extraction of grand average over time of the inter-
electrode average.

deviation of the inter-electrode signal to noise ratio Fig. 3. Feature extraction from EEG data segments
(SNR), and so on. After such a process, the origi- using common statistical parameters AVG, STD and
nal input EEG data is transformed into this feature SNR.
space (81 features in total), which is used as input
to the ANN and SVM systems. A unique attribute Table 2. Segment descriptor matrix for a
of this GPF configuration is that the computed ele- particular parameter.
ments that constitute it do not depend on duration
avg std snr
of the EEG recordings or on location or number of
electrodes that were used, an attribute that could AVG avg(AVG) std(AVG) snr(AVG)
extend its use to other applications. STD avg(STD) std(STD) snr(STD)
The detailed parametric extraction process is SNR avg(SNR) std(SNR) snr(SNR)
illustrated in Fig. 2 for one given parameter, denoted
as Xn (n = 1, 2, . . . , 9). This process is performed for
all nine parameters. In this illustrated example of window, as depicted in Fig. 2(b), where the grand
Fig. 2, parameter Xn is computed for each electrode average across all electrodes is then used as a repre-
using windows for 1 s. As can be seen from Fig. 2(a), sentative feature. However, since the purpose was to
extracting electrode parameters has the disadvan- analyze and compare EEG recordings regardless of
tage of generating a set of values which depend on their duration, further statistical feature extraction
the number of electrodes. To cope with this issue, was performed along the time axis to provide a single
this study used statistical features such as average, feature descriptor for the whole EEG file. Figure 2(c)
standard deviation, and signal-to-noise ratio, which illustrates this last step using the grand average of
were computed across all electrodes for each time the so-called inter-electrode average.

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A New Parametric Feature Descriptor for the Classification of Epileptic and Control EEG Records

The statistical features chosen for extracting the corresponding to the nine parameters mentioned ear-
global features from the EEG segments were the lier. The number of processing elements in the hid-
average (AVG), standard deviation (STD) and signal den layers was 100. The choice of 100 hidden units is
to noise ratio (SNR). All steps of the global parame- arbitrary, with the intention that enough number of
ter extraction procedure for the AVG, STD and SNR hidden units (more than the input units) is chosen
features of any particular parameter are illustrated in to achieve accurate results. The output layer, con-
Fig. 3, where it can be observed how an entire EEG sisting of one neuron with a sigmoid transfer func-
segment can be described by a single global value for tion, provided the network’s output: epileptic (1) or
a particular parameter. Following this feature extrac- control (−1).
tion process whose steps are described in Figs. 2 The scaled conjugate gradient (SCG) back-
and 3, a 3×3 GPF matrix for each of the nine param- propagation algorithm was first introduced by
eters were computed to serve as 81 inputs for the Moller.31 This algorithm is an improvement over
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ANN and SVM networks in the classification process. the back propagation algorithm. The added value in
using the SCG is based on the fact that this algo-
2.5. Neural network configuration and rithm is based upon a class of optimization tech-
Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com

generation of the training and niques known as conjugate gradient methods, which
testing tables rely on the use of second-order information to train
the neural network. SCG algorithms are not depen-
The network used for this classification study, as
dent on user inputs such as the learning rate and
depicted in Fig. 4, was a feed-forward multilayer
the momentum constant which make them more
perceptron (3-layers) built using commercial soft-
robust. Another important feature of the SCG algo-
ware (Neural Network Toolbox of The MathWorks
rithm is in the ability to avoid the time consuming
Inc.). This network architecture consisted of an
line search which is used by standard back propa-
input layer one hidden layer and the output layer.
gation algorithms. The standard back propagation
There were 81 units in the input layer, each unit
algorithm adjusts the weights depending on the neg-
corresponding to one of the statistical features
ativity of the gradient and this does not necessar-
ily produce the fastest convergence all the times; on
the other hand, in the SCG algorithm, a search is
performed along the conjugate directions, which in
turns produces faster convergence than the direc-
tion used for the back propagation algorithm. This
circumvention makes the SCG algorithms orders of
magnitude faster that the standard back propagation
algorithms.
In order to generate the training and testing
tables, 50% of the files were used for training, 25%
for cross-validation and 25% for testing. A cross-
validation strategy was implemented in the training
so as to create early stopping conditions to avoid
network memorization and to prevent over-fitting of
data. In this setup, distribution was done such that
each patient had approximately the same balance of
files for training, cross-validation and testing. From
all 214 files that were extracted from the 17 patients,
a total of 106 files were used for training, 54 were
reserved for cross-validation and 54 were used for
testing.
Fig. 4. ANN configuration showing the 81-100-1 topol- The network is trained 15 times starting with
ogy used in the classification process. random initial weight assignments and a random

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M. Cabrerizo et al.

distribution of the 214 files into the three sets 1

namely training, validation and testing according to 0.9

the ratios listed above. Training and testing tables 0.8

True Positive Rate


0.7
for each parameter were structured into a matrix.
0.6
The rows corresponding to each subject reflect the
0.5
number of files for that particular subject and the
0.4
columns are formed by the nine statistical features
0.3
extracted from each parameter. The last column of Lower Bound Trial
0.2
the table corresponds to the target (1 or −1). All the 0.1
Average Trial
Upper Bound Trial
subjects were concatenated into a big matrix that
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1
corresponds either to the training or testing tables.
False Positive Rate
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Fig. 5. ROC curve for the 15 classifiers.


2.6. Training and testing of the ANNs
Since the network creates its initial set of weights requirements especially when using large datasets,
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randomly, and therefore, each new set can be bet- which is the case of this study. Conjugate gradient
ter or worse for the training than the previous one, methods considerably reduce the learning time since
regardless of the number of hidden units, 15 training they avoid the consuming line search where the net-
trials were performed on the ANN in order to pre- work response in the training phase must be com-
vent training from trapping the network into a local puted several times for each search. Figure 5 shows
minima or leading it to overflow. The intention of the ROC curves for the 15 trials. It is seen that for
repeating the training was to rule out the possibil- all the trials the curves hug the left top corner of the
ity that any differences in the results were obtained chart and hence shows a very high accuracy for the
just by chance. All training repetitions were stopped classification algorithm. The overlap of all the curves
by different stop criteria conditions such as: (1) the on top of one another is clearly an indication of the
network is trained for a maximum of 1000 epochs low standard deviation seen in the clustering, which
after which the process is terminated; (2) the net- proves consistency in the results.
work is trained until the performance function (mean The validation error curves plotted as a func-
squared error) reduces below 0.000001; (3) the train- tion of the training epochs are shown in Fig. 6.
ing is terminated when the training gradient falls The validation error curves show the trend in the
below 0.000001 and (4) the validation error increases
over six iterations.
The performance function is calculated during 100
Trial 1
training only. In this case, the mean square error Trial 2
Trial 3
was used, and the square difference of the desired 10-1 Trial 4
Mean Squared Error (MSE)

network output to the actual value is calculated in Trial 5


Trial 6
each iteration. As a consequence, the training gradi- Trial 7

ent will also reach its minimum value. The error on 10-2 Trial 8
Trial 9
the validation set is also monitored during training. Trial 10
Trial 11
The training will be terminated when the validation 10-3 Trial 12
Trial 13
error increases over six iterations in order to assure Trial 14
that a true incremental trend is been followed and Trial 15
AVG Trial
10-4
the network needs to be terminated at that point.
This procedure was applied consistently across
all the 15 training trials. The scaled conjugate 10-5
10 20 30 40 50 60 70 80 90 100
gradient back-propagation algorithm is a combina-
tion of model-trust region approach and the con- Epochs

jugate gradient method. The conjugate gradient Fig. 6. Trend of MSE as a function of epochs for train-
method is used since it is less expensive on memory ing the ANN.

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A New Parametric Feature Descriptor for the Classification of Epileptic and Control EEG Records

reduction of the mean square error (MSE) for the val- or −1 is the value associated to either epileptic or
idation data set. It is observed that the MSE reduces control, respectively.
rapidly at the beginning of the training process and It is noted that the choice of the kernel for this
reaches a minimum value as demonstrated by the study was selected by trial and error, and the best
results depicted in Fig. 6. The training process is results were obtained using a polynomial kernel of
terminated when the validation error rises for a con- degree 1. During this process, we do not know the
secutive 6 epochs. Such a termination condition does suitability of the kernel until the testing with real
not allow the training to end abruptly in case the data has been tried. This polynomial kernel as simple
network deviates from the correct training direction. as it is proved to be superior to other kernels.
An average of 42 epochs were required to train the
neural network with some trials needing as many as
73 epochs to train and some needing as few as 19 3. Results
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epochs. It should be noted that the average of these The proposed ANN algorithm on the basis of the
error curves shown in bolded black could not extend newly developed global descriptor table has shown
beyond the shortest error curve. a fast convergence rate along with a smaller vari-
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ance among runs when compared with the sole use


2.7. Training and testing of the SVM of the back-propagation algorithm. The suitability of
algorithm the EEG descriptors is assessed based on the results
obtained in the testing phase. After training the net-
The SVM method can best be described as a method
work 15 times, the final results correspond to the
that makes use of generalized linear classifiers which
mean of all the 15 results. The accuracy, specificity
map input vectors to a higher dimensional space (fea-
and sensitivity values are displayed in Table 3. Dur-
ture space), where a maximal separating hyperplane
ing the testing phase, the neural network yielded
is sought to separate any two different classes. The
an accuracy of 96.28% with a sensitivity and speci-
main idea is to minimize the classification risk by
ficity of 96.42% and 95.50%, respectively. The total
maximizing the inter-class margins. Optimal hyper-
amount of false detections (FN and FP) is small
planes are known to maximize the Euclidean distance
and the TP value is rather high. Based on the inter-
between each point and the hyperplane. The margins
patient nature of this procedure, the results can be
of the classifiers refer only to the support vectors.
considered highly significant.
SVM rely on a set of prescribed kernels as means to
The accuracy results as a function of the number
resolve data with complex mapping.
of trials are displayed in Fig. 7 for both the train-
For the EEG data at hand, we used a polynomial
ing and testing phases. The training phase during
of first order together with the so-called Soft Margin
the 15 trials showed a more steady behavior than
algorithm, which is a modification of the maximum
the testing phase. The fluctuations of the accuracy
margin idea that accounts for overlapping. If there
values during the training of 50% of the data using
is a sufficient amount of overlap, the Soft Margin
25% cross-validation as the stopping condition are
method will still select an optimum hyperplane that
minimal.
separates the EEG data, while still maximizing to
A high accuracy value is maintained during 15
the greatest extent the margin distances within that
trials of the network. In retrospect, the input data
context. As shown in Eq. (1), the method incorpo-
successfully adjusted to the network’s weights and
rates the slack variables (ξi ) that measure the degree
thresholds and the error was minimized on the train-
of misclassification of the input data.
ing set. At this stage, the classifier is deemed reliable
C = Yi (αi K(xi , x) + b) ≥ 1 − ξi , ξi ≥ 0 and ready to be tested on new data.
  During the 15 trials of the neural network in the
Where K(x, x ) = (x • x + 1) d
(1)
testing phase, the accuracy, sensitivity and speci-
Polynomial Kernel order d = 1,
ficity fluctuate between 90% and 100%. The min-
where b is the bias, αi (i = 1, 2, . . . , k) are the weights imum value reached by two of these measures is
corresponding to the support vectors (SV) since only 90%, which is an acceptable outcome given the com-
the SV have an influence on the equation, and C = 1 plexity of EEG data. The accuracy is the measure

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M. Cabrerizo et al.

Table 3. Testing results for the accuracy, sensitivity and specificity comparing SVM and ANN.

Trial # NN Accuracy SVM Accuracy NN Sensitivity SVM Sensitivity NN Specificity SVM Specificity

1 92.60 98.15 94.12 96.55 90.00 100.00


2 98.10 96.30 100.00 97.06 95.65 95.00
3 92.6 94.44 92.59 93.33 92.59 95.83
4 92.60 94.44 90.00 94.12 95.83 95.00
5 96.30 96.30 100.00 100.00 92.00 92.59
6 96.30 98.15 93.33 100.00 100.00 94.12
7 92.60 96.30 90.00 100.00 95.83 92.00
8 94.40 98.15 92.59 97.14 96.30 100.00
9 98.10 98.15 100.00 96.97 95.65 100.00
10 98.10 100.00 100.00 100.00 95.00 100.00
by UNIVERSIDADE FEDERAL DO RIO GRANDE DO SUL on 01/13/14. For personal use only.

11 96.30 96.30 100.00 94.12 91.67 100.00


12 98.10 96.30 97.22 96.88 100.00 95.45
13 98.10 96.30 96.43 100.00 100.00 93.33
14 100.00 96.30 100.00 96.43 100.00 96.15
Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com

15 96.30 96.30 100.00 93.33 92.00 100.00


AVG 96.03 96.79 96.42 97.06 95.50 96.63
STD 2.49 1.48 3.94 2.52 3.38 3.05

100 kernel that was used for this classification was a


90 polynomial with degree 1, other degrees were also
80 implemented and the results as shown in Fig. 8
70
indicate that degree 1 polynomial is most effective
in this case.
Accuraccy

60
The testing results show the superiority of SVM
50
over ANN for the classification of EEG signals.
40
Figure 9 shows the accuracy and sensitivity over
30
15 trials. The SVM yielded AVG/STD values of
20 97.1/2.52 and the ANN with 96.4/3.94 for the accu-
Training
10 Testing racy plots. The behavior of the performance of the
0 two different classifiers shows less fluctuation; indeed
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
Trial Number
it is more stable when using SVM over ANN.
Overall, within the 15 runs, it is observed that
Fig. 7. Accuracy during training (solid line) and testing some of the EEG files belonging to controls 1 and 7
(dotted line) of the ANN. were misclassified as epileptic. For example, for con-
trol subject 1, depending on the run, 2–4 files out of
that has shown fewer variations with a calculated 10 were classified incorrectly, and for control subject
standard deviation of 2.39, and the sensitivity is 7, 4 to 7 out of the 14 files were misclassified. Clini-
the measure with more variations with a standard cal reports indicate that control subject 1 was having
deviation of 3.94. Thus, a scaled conjugate gradi- some episodes of dizziness, fatigue and shortness of
ent back-propagation neural network designed on the breath, and control subject 7 was having some abnor-
basis of the descriptor matrices was able to accu- mal movements including some shivering. In terms of
rately classify scalp EEG data into epileptic and false negatives, for patient 9, as an overall, 3–5 EEG
control. segments out of 20 were misclassified as nonepileptic.
The SVM outperformed the ANN, but the differ- This patient had a very focal area of epileptogenesis
ence according to the t-test (p = 0.50 for accuracy and in some segments, abnormal behavior was not so
and p = 0.60 for sensitivity) suggests that this dif- evident. Patient 14 had some occasional right pari-
ference is not statistically significant. Although the etal temporal discharges that were not present in all

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A New Parametric Feature Descriptor for the Classification of Epileptic and Control EEG Records
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Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com

Fig. 8. Performance of the SVM using different degree polynomials.

11 EEG segments, and 2–5 segments, depending on the entire EEG record, which is tedious and is often
the run, were misclassified. limited to the subjective nature of visual inspection.
Instead, we are proposing an automated and quan-
4. Discussion tifiable method that can classify short segments of
EEG into control EEG behavior or epileptic EEG
This study reveals that using the combination of 81
without including the seizure itself in the case of
features is a more reliable approach as it consoli-
epileptic EEG. Based on standard frequency and
dates key behaviors of all these features as input to
time domain features, one can extract hidden infor-
a scaled conjugate gradient back-propagation ANN
mation in the form of time series statistics that
or SVM. More importantly, SVM is shown to yield
are most suitable for an ANN, but extremely sub-
the highest accuracy while keeping both the number
tle for visual inspection. The results of this study
of false positives and false negatives to a minimum.
The uniqueness of the proposed method is that it demonstrate that short EEG segments are suffi-
brought together different features in both time and cient for the parameters that were used to extract
frequency domains as global descriptors that are best the needed information to delineate the two types
suited for both ANN and SVM implementations. The of EEGs (epileptic and control) as considered in
resulting classifiers were able to delineate successfully this study. Ultimately, it is all about the means
EEG data as either belonging to a control subject or by which the information was extracted and in the
to an epileptic patient, even in the absence of inter- way it is structured before it is fed as input into a
ictal spikes and the seizure event itself. well-configured ANN or SVM network. The results
In order to make an assessment of any EEG obtained serve to reinforce the merit of the proposed
record collected, neurophysiologists have to monitor approach.

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M. Cabrerizo et al.

100 features all at once to an ANN or SVM network


90 to sift through all these dimensions together and to
80 combine the 81 statistical features through different
70 weights in seeking an optimal classification process.
Accuraccy

60 The principal component analysis (PCA) was also


50 investigated in order to use in the classification pro-
40 cess for only those dimensions associated with the
30 highest eigenvalues. Then the reduced GPF matrix
20 ANN was used as an input to both the ANN and SVM
10 SVM networks with two discrete outputs: epileptic or con-
0 trol EEG. The accuracy of the various classifiers
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
was assessed and cross-compared. The results showed
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Trial Number
that SVM and ANN with the reduced GPFs using
100 PCA did not perform better. As the processing time
90 was not an issue to begin with, the various empirical
Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com

80 evaluations showed that the best performance was


70 still achieved when using all the features.
Sensitivity

60 Furthermore, in order to determine if the dif-


50 ference in the metrics obtained between the nine
40 parameters is not just by chance, ANOVA (analy-
30
sis of variance) test was applied.
20
In this case, the test showed that the descriptors
ANN
10
are different with a certainty degree of almost 100%
SVM
(1−1.42 ∗ 10−19 ) as depicted in Table 4. These results
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 of the ANOVA test are not surprising considering the
Trial Number clear variation in the mean of the nine descriptors.
The ANOVA test results prove that the variance of
Fig. 9. Accuracy and sensitivity of SVM versus ANN.
nine parameters between the descriptors is not dif-
ferent by chance.
It should be noted that our first attempt at deal- It is reassuring that the means of the nine param-
ing with the data for this study was to question eters used are different by looking at the box plots
whether all nine features extracted for any one given in Fig. 10. The nine notches display the variability
parameter were all-at-once necessary, with the poten-
tial to reduce data dimensionality, and still resolve Table 4. ANOVA (analysis of variance) test on the nine
the problem at hand. As an example we consid- parameters: F-Statistic is used for testing the equality of the
ered the gamma frequency range parameter. The parameter means, and F-crit. is the tabular critical value of
reason why the gamma parameter was considered the F distribution, based on the 0.05 level of confidence.
here is because of the suitability of this frequency Groups Sum Average Variance
range for seizure detection purposes.19,20 When we
investigated all 36 possible 2D plot combinations Activity 7.3999 0.924988 0.002333
Mobility 6.2847 0.785588 0.002442
for the nine features that were considered (C29 ), we
Complexity 5.5151 0.689388 0.00327
observed that some of the plots showed in general Delta 6.7181 0.839763 0.001604
a wider spread of clusters, with the potential of Theta 5.3 0.6625 0.001726
using nonlinear decision functions to separate the Alpha 5.7001 0.712513 0.000448
two classes (control EEG and epileptic EEG), but Beta I 6.3879 0.798488 0.001046
Beta II 6.5666 0.820825 0.000932
overlap existed in all of these 2D plots. Consequently, Gamma 6.2485 0.781063 0.000918
as most of these data clusters are somewhat orga-
F -Statistic P -value F -crit.
nized and separated from each other in different
32.53271 1.42E-19 2.089185
ways, our research premise led us at inputting such

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A New Parametric Feature Descriptor for the Classification of Epileptic and Control EEG Records

the so-called GPF matrices which capture statistics


of EEG along each record (time series) and across all
electrodes (inter-electrode). The uniqueness of this
approach is in the way 81 features are configured
using statistical analysis across electrodes and across
time into an optimal input to a scaled conjugate
gradient back-propagation ANN. Another important
point to make is that such input features are inde-
pendent of the EEG segment length as well of the
number of electrodes used, which could lead to their
use on other applications that rely on statistical anal-
ysis of signals. An SVM implementation is also pro-
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vided for comparative purposes, and to comfort the


generalized concept of this classification approach.
These statistical features, which include SNR, proved
Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com

through the excellent classification results that were


obtained, that they must embed within them key
Fig. 10. Means of the nine parameters.
characteristics that are most suitable for delineat-
ing control EEG data from epileptogenic data, and
of the median between the different parameters. The more forcefully so when all the standard param-
width of a notch is computed so that box plots whose eters are used in a consortium. Our earlier work
notches do not overlap (as in this case) have differ- on using any one particular parameter may have
ent medians at the 5% significance level. Compar- its unique benefits in the classification process, but
ing box-plot medians is like a visual hypothesis test, through empirical evaluations it was determined that
analogous to the t test used for means. The box plot informed decisions can be better made when these
parameters are brought together.
suggests the size of the F -statistic and the p-value.
These GPF matrices can be regarded as the sim-
Large differences in the center lines of the boxes cor-
plest way of comparing EEG recordings. While one
respond to large values of F and correspondingly
can assume that the grand AVG of the activity across
to small values of p. In other words, the F statis-
all electrodes and time windows can be compared
tic (32.53271) and the low p-value (1.42E-19) calcu-
between EEG files, this method expanded this rea-
lated, corroborate the statistical significance of the
soning to include the standard deviation and signal
observed differences among the means of the nine
to noise ratio across time and across electrodes. The
parameters.
results obtained lead us to conclude that the unique
way in which important parameters and related mea-
5. Conclusion sures were brought together could make up for a gen-
eralized mathematical framework that could extend
This study proposed a new EEG classification
to other classification problems.
method based on the aggregation of key frequency
Both classifiers yielded promising results, mini-
and temporal parameters commonly used in the lit-
mizing to a great extent the number of false neg-
erature, but seeking what we believe is an optimal
ative instances. Empirical evaluations of these two
input to the ANN/SVM classifiers. Different types
classifiers using the ANOVA test yielded accuracy
of machine learning classifiers would yield different
and sensitivity measures higher than 96%. Through
results depending uniquely on the choice of inputs these classification results, we observe that given the
that are fed into them. A mathematical model for 15 trials that were used to ensure consistency in the
generating the GPF was designed specifically to show results, in the worst case scenario 5% of the EEG
how a combination of 81 features (9 parameters × segments from controls were misclassified as epilep-
(3 × 3) features/per parameter) using both the fre- tic EEG segments, and 4% of the EEG segments
quency and temporal domains are consolidated into from patients were misclassified as nonepileptic. We

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M. Cabrerizo et al.

thus can infer the occurrence of high-risk (epilep- signal to the activity of the (original) signal:
tic) as well as low-risk (control) patients which 
Ax
can be planned accordingly for potential follow up Mx = (A.2)
Ax
procedures.
where x represents the first derivative of the signal x.
An extension of this research endeavor could
Mobility gives a measure of deviation of the voltage
include other interesting parameters, such as
changes with respect to deviation of the EEG voltage
coherence32,33 even if it is to assess or classify other
amplitude.
types of dysfunctions such as Alzheimer and may
Complexity, C, is defined as the ratio of the
use different models of ANNs. Window sizes greater
mobility of the first derivative of the signal to the
than 1 s could also be explored to see how they could
mobility of the signal itself:
affect the results in terms of balancing processing 
requirements with the resulting accuracy obtained in Mx Ax /Ax
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c= = , (A.3)
the classification process. It would be also extremely Mx Ax /Ax
interesting to look into the third generation of neural
where x stands for the second derivative of the
network models, named spiking neural networks,34
Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com

signal.
in terms of developing new ways at looking at the
Once the spectral analysis is estimated for all
dynamics of the human brain by including the con-
EEG channels, the power on the five recognized fre-
cept of time as input to the operational mode of the
quency bands of EEG activity (delta, theta, alpha,
ANN, where the 1 s windows which are averaged in
beta, and gamma) is analyzed. The power spectrum
this study could now be fed into the ANN as a func-
is a measure of the signal variation in a specific fre-
tion of time. Another issue of clinical importance is
quency range. The power on each band is computed
the integration of key recording modalities where an
by squaring all Fourier coefficients that fall in a spe-
immediate challenge will be to integrate this EEG-
cific frequency range (f1 , f2 ), and adding them. Since
based approach with fMRI studies which attempt at
the Fourier coefficients are complex numbers, squar-
determining typical and atypical activation patterns
ing is substituted by the norm as follows:
in epilepsy patients and control subjects in a pedi-
atric population.35,36 
f2
P (f1 , f2 ) = |S(f )|2 , (A.4)
From a clinical point of view, it is also important
f =f1
to look into sampling frequencies higher than 512 Hz
to see if the spectrum reveals high frequency powers where f1 and f2 are the lower and upper bounds of
which could be of value to the classification process. the desired frequency range and S(f ) is the power
In retrospect, the complex interactions of the differ- spectrum at frequency bin f .
ent parameters considered and modeled through the In this EEG study analysis, the following estab-
proposed ANN configuration, proved that the right lished frequency ranges have been investigated:
confluence of key EEG parameters may eventually be Delta (<4 Hz): These waves are normal in adults
applied for individualized diagnosis of epilepsy and during sleep, although are the dominant rhythms in
could serve as an effective tool for EEG monitoring. infants up to 1 year of age.
Theta (4–8 Hz): Theta waves are strong during alert-
Appendix ness and meditation and reflect the transition from
Activity, Ax , is simply the variance of the signal seg- sleep to wakefulness. They are normal in children up
ment x and is defined as: to 13 years old.
N
(xi − µ)2 Alpha (8–13 Hz): These waves are observed by clos-
Ax = i=1 . (A.1) ing the eyes and by relaxation.
N
The activity corresponds with the total power of the Beta (13–36 Hz): Beta waves reflect active concen-
signal and is thus a measure of the extent of the tration and are dominant in adults who are alert
amplitude of the EEG measurement. and have their eyes open. This band has a rela-
Mobility, Mx , is computed as the square root of tive large band and it has been subdivided in sev-
the ratio of the activity of the first derivative of the eral sub-bands: low beta (13–15 Hz), midrange beta

1250001-14
March 28, 2012 17:8 1250001

A New Parametric Feature Descriptor for the Classification of Epileptic and Control EEG Records

(15–18 Hz) and high beta (>18 Hz). A subdivision 3. M. Tito, M. Cabrerizo, M. Ayala, A. Barreto,
into beta I (13–20 Hz) and beta II (20–36 Hz) is also P. Jayakar and M. Adjouadi, Classification of elec-
troencephalographic seizure recordings into ictal and
found in the literature.
interictal files using correlation sum, Comp. Biol.
Gamma (36–44 Hz): These waves are present in Med. 39(7) (2009) 604–614.
4. N. Sezgin and M. E. Tagluk, Energy based feature
almost all areas of the brain and it is associated with extraction for classification of sleep apnea syndrome,
perception and consciousness. It is also sometimes Comp. Biol. Med. 39(11) (2009) 1043–1050.
defined as the frequencies above 36 Hz. 5. L. Vaugier, S. Aubert, A. McGonigal, A. Trebu-
chon, M. Guye, M. Gavaret, J. Regis, P. Chauvel,
The nine parameters will be extracted across elec- F. Wendling and F. Bartolomei, Neural networks
trodes as well as over time. To differentiate, upper- underlying hyperkinetic seizures of “temporal lobe”
case is used for the inter-electrode parameters, and origin, Epilepsy Res. 86(2–3) (2009) 200–208.
6. A. T. Tzallas, M. G. Tsipouras and D. I. Fotiadis,
by UNIVERSIDADE FEDERAL DO RIO GRANDE DO SUL on 01/13/14. For personal use only.

lower case is used for time series parameters. Since Epileptic Seizure detection in EEGs using time-
there are three features across electrodes and another frequency analysis, IEEE Trans. Inf. Technol. in
three for each resulting time series, there are in total Biomed. 13(5) (2009) 703–710.
7. S. N. Ogulata, C. Sahin and R. Erol, Neural
Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com

nine features per parameter, as shown in the table


network-based computer-aided diagnosis in classifi-
below, starting with the avg (AVG), i.e. the average
cation of primary generalized epilepsy by EEG sig-
over time (avg) of the inter-electrode average (AVG), nals, J. Med. Syst. 33(2) (2009) 107–112.
and ending with snr (SNR). 8. E. D. Ubeyli, Analysis of EEG signals by implement-
The signal to noise ratio (SNR) is the ratio of the ing eigenvector methods/recurrent neural networks,
mean to standard deviation of a given EEG channel Digit. Signal Process. 19(1) (2009) 134–143.
9. O. Faust, U. R. Acharya, L. C. Min et al., Automatic
segment x. identification of epileptic and background EEG sig-
µx nals using frequency domain parameters, Int. J.
SNR x = . (A.5) Neural Syst. 20(2) (2010) 159–176.
σx
10. N. Y. Liang, P. Saratchandran, G. B. Huang and
N. Sundararajan, Classification of mental tasks from
Acknowledgements EEG signals using extreme learning machine, Int. J.
Neural Syst. 16(1) (2006) 29–38.
The authors appreciate greatly the support provided 11. W. Y. Hsu, Continuous EEG signal analysis for asyn-
by the National Science Foundation under grants chronous BCI application, International Journal of
CNS-0959985, CNS-1042341, and HRD-0833093. We Neural Systems 21(4) (2011) 335–350.
also acknowledge the support provided by the Uni- 12. M. A. Kramer, F. L. Chang, M. E. Cohen, D. Hud-
son and A. J. Szeri, Synchronization measures of the
versity Graduate School through the Dissertation
scalp EEG can discriminate healthy from Alzheimers
Year Fellowship for Mr. Mohammed Goryawala. The subjects, Int. J. Neural Syst. 17(2) (2007)
authors give special thanks to Miami Children’s Hos- 61–69.
pital for their valuable clinical support and to the 13. S. Ghosh-Dastidar and H. Adeli, Improved spiking
Ware Foundation for the generous philanthropic sup- neural networks for EEG classification and epilepsy
and seizure detection, Integr. Comput.-Aided Eng.
port they continue to provide. 14(3) (2007) 187–212.
14. S. Ghosh-Dastidar and H. Adeli, A new super-
vised learning algorithm for multiple spiking neural
References
networks with application in Epilepsy and Seizure
1. M. Adjouadi, M. Cabrerizo, M. Ayala, P. Jayakar, detection, Neural Netw. 22(10) (2009) 1419–1431.
I. Yaylali and A. Barreto, Detection of interic- 15. D. Sherman, N. Zhang, M. Anderson, S. Garg, M. J.
tal spikes and artifactual data through orthogonal Hinich, N. V. Thakor and M. A. Mirski, Detection
transformations, J. Clin. Neurophysiol. 22(1) (2005) of nonlinear interactions of EEG alpha waves in the
53–64. brain by a new coherence measure and its application
2. M. Cabrerizo, M. Adjouadi, M. Ayala and to epilepsy and anti-epileptic drug therapy, Int. J.
P. Jayakar, Subdural interictal EEG analysis for Neural Syst. 21(2) (2011) 115–126.
extracting discriminating features towards elec- 16. U. R. Acharya, E. C. P. Chua, K. C. Chua, L. C.
trode classification using artificial neural networks, Min and T. Tamura, Analysis and automatic iden-
Brain Mapping Research Progress, Chapter 5 (2009), tification of sleep stages using higher order spectra,
pp. 87–108. Int. J. Neural Syst. 20(6) (2010) 509–521.

1250001-15
March 28, 2012 17:8 1250001

M. Cabrerizo et al.

17. H. Osterhage, F. Mormann, T. Wagner and K. Lehn- topographical functional based on an auditory-
ertz, Measuring the directionality of coupling: Phase comprehension paradigm using an eigensystem study
versus state space dynamics and application to EEG and spectrum analysis, Brain Topogr. 17(3) (2005)
time series, Int. J. Neural Syst. 17(3) (2007) 139– 151–163.
148. 28. R. S. Fisher, W. R. Webber, R. P. Lesser, S. Arroyo
18. U. R. Acharya, S. V. Sree, S. Chattopadhyay, W. and S. Uematso, High-frequency EEG activity at the
W. Yu and A. P. C. Alvin, Application of recurrence start of seizures, J. Clin. Neurophysiol. 9(3) (1992)
quantification analysis for the automated identifica- 441–448.
tion of Epileptic EEG signals, Int. J. Neural Syst. 29. E. Urrestarazu, R. Chander and F. Dubeau, Inter-
21(3) (2011) 199–211. ictal high-frequency oscillations (100–500 Hz) in
19. A. V. Medvedev, A. M. Murro and K. J. Meador, the intracerebral EEG of epileptic patients, Brain
Abnormal interictal gamma activity may manifest a 130(9) (2007) 2354–2366.
Seizure onset zone in temporal lobe Epilepsy, Int. J. 30. G. A. Worrell, T. D. Lagerlund and F. W. Shar-
Neural Syst. 21(2) (2011) 103–114. brough, Localization of the epileptic focus by low-
by UNIVERSIDADE FEDERAL DO RIO GRANDE DO SUL on 01/13/14. For personal use only.

20. M. Ayala, M. Cabrerizo, P. Jayakar and M. resolution electromagnetic tomography in patients


Adjouadi, Subdural EEG classification into Seizure with a lesion demonstrated by MRI, Brain Topogr.
and Non-seizure files using neural networks in the 12(4) (2000) 273–282.
gamma frequency band, J. Clin. Neurophysiol. 28(1) 31. M. F. Moller, A Scaled Conjugate-Gradient algo-
Int. J. Neur. Syst. 2012.22. Downloaded from www.worldscientific.com

(2011) 20–29. rithm for fast supervised learning, Neural Netw. 6(4)
21. D. Sherman, N. Zhang, S. Garg, N. V. Thakor, M. A. (1993) 525–533.
Mirski, M. A. White and M. J. Hinich, Detection of 32. Z. Sankari and H. Adeli, Intrahemispheric,
Nonlinear Interactions of EEG Alpha Waves in the interhemispheric and distal EEG coherence in
Brain by a New Coherence Measure and its Applica- Alzheimer’s disease, Clin. Neurophysiol. 122(5)
tion to Epilepsy and Anti-Epileptic Drug Therapy, (2011) 897–906.
Int. J. Neural Syst. 21(2) (2011) 115–126. 33. Z. Sankari, H. Adeli and A. Adeli, Probabilistic neu-
22. M. Tito, M. Cabrerizo, M. Ayala, P. Jayakar and M. ral networks for diagnosis of Alzheimer’s disease
Adjouadi, A comparative study of intracranial EEG using conventional and wavelet coherence, J. Neu-
files using nonlinear classification methods, Ann. rosci. Meth. 197(1) (2011) 165–170.
Biomed. Eng. 38(1) (2010) 187–199. 34. S. Ghosh-Dastidar and H. Adeli, Spiking neural net-
23. M. Tito, M. Cabrerizo, M. Ayala, P. Jayakar and works, Int. J. Neural Syst. 19(4) (2009) 295–308.
M. Adjouadi, Seizure detection: An assessment of 35. M. Adjouadi, X. You, M. Guillen, M. Ayala, M.
time- and frequency-based features in a unified 2-D Cabrerizo, P. Jayakar, A. Barreto, N. Rishe, J. Sul-
decisional space using nonlinear decision functions, livan, D. Dlugos, M. Berl, J. VanMeter, D. Mor-
J. Clin. Neurophysiol. 26(6) (2009) 381–391. ris, E. Donner, B. Bjornson, M. Smith, B. Bernal
24. B. Hjorth, The Physical significance of time domain and W. D. Gaillard, Integrating nonlinear decision
descriptors in EEG analysis, Electroenceph. Clin. functions with principal component analysis in fMRI
Neurophysiol. 34 (1973) 321–325. language activation patterns classification, Epilepsia
25. B. Hjorth, EEG Analysis based on time domain 50(11 Suppl.) (2009) 212–213.
properties, Electroenceph. Clin. Neurophysiol. 29 36. X. You, M. Adjouadi, M. Guillen, M. Ayala, A.
(1970) 306–310. Barreto, N. Rishe, J. Sullivan, D. Dlugos, J. Van-
26. M. Cabrerizo, M. Adjouadi and M. Ayala, An appli- Meter, D. Morris, E. Donner, B. Bjornson, M. L.
cation of eigensystem and frequency analysis in Smith, B. Bernal, M. Berl and W. D. Gaillard, Sub-
brain functional mapping, Progress in Brain Map- patterns of language network reorganization in pedi-
ping Research, Chapter 5 (2006), pp. 177–204. atric localization related Epilepsy a multisite study,
27. M. Cabrerizo, M. Adjouadi, M. Ayala, K. Nunez, Hum. Brain Mapp. 32(5) (2011) 784–799.
P. Jayakar and I. Yaylali, Integrated study of

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