2018 15th International Conference on Electrical Engineering, Computing Science and Automatic Control (CCE)

Mexico City, Mexico September 5-7, 2018

Pediatric Seizure Forecasting using Nonlinear

Features and Gaussian Mixture Hidden Markov
Models on Scalp EEG Signals
Carlos Emiliano Solórzano-Espı́ndola Blanca Tovar-Corona Álvaro Anzueto-Rı́os
Instituto Politécnico Nacional Instituto Politécnico Nacional Instituto Politécnico Nacional
UPIITA - Lab. Biomecánica UPIITA - Academia de Sistemas UPIITA - Lab. Biomecánica
Mexico City, Mexico Mexico City, Mexico Mexico City, Mexico
csolorzanoe1200@alumno.ipn.mx bltovar@ipn.mx aanzuetor@ipn.mx

Abstract—Seizure forecasting systems have been studied in
recent years for improving the quality of life for patients
with epilepsy and gain further understanding about seizures. A
common approach for this is the study of electroencephalography
(EEG) recordings, using signal processing techniques and, more
recently, machine learning algorithms. A four-stage system is
developed for patient-specific seizure prediction; consisting of
pre-processing, dimensionality reduction, feature extraction and
classification between interictal and preictal EEG signals. A
hybrid method using principal component analysis (PCA) and
independent component analysis (ICA) is applied for dimension-
ality reduction. Nonlinear features are selected for the analysis
and characterization of the signals. A Hidden Markov Model
(HMM) with Gaussian mixture emissions is trained for each type
of signal and evaluated as a classifier. A sensitivity of 0.95 and
a specificity of 0.86 were achieved.
Index Terms—seizure, forecasting, electroencephalography,
Markov, entropy
I. I NTRODUCTION
Epilepsy is a common neurological disorder, with an es-
timated incidence between 24 to 70 out of 100,000 people
according to different studies [1]–[3]. This proportion also
depends on risk factors as some groups have been shown to
have a higher incidence and prevalence of seizures. Some of
this factors include age, sex, family history, physical trauma,
environmental toxins, among others [4], [5].
Epilepsy is a disease of the brain characterized by the
predisposition to have epileptic seizures. Seizures are neuro-
logical events with abnormal and excessive electric discharges
originated from a synchronized activity of neurons [6]. The
onset can be either partial or generalized depending on how
the seizure begins and can be further classified according to
the symptoms that they manifest.
A. Treatment of Epilepsy
The treatment for epilepsy has evolved over the years giving
different types of solutions aiming to control of seizures.
Nowadays there is a broad range of anti-epileptic drugs
(AEDs) targeting different types of seizures and stages of the
disease, giving options for physicians to study their patient’s
conditions and prescribe the AED that they consider to be
optimal for the case. Some of these AEDs may have unde-
sirable side effects, that is one of the reasons that medical
doctors require to choose the one that minimizes the risk of
developing side effects [7], and approximately 20-30% of the
patients cannot find suitable AEDs that reduce or stop seizures
[8]. Therefore the medic must evaluate and present alternatives
to the patient and, when it is required, surgery.
A more recent alternative is the use of electrical stimulation
(neuromodulation) systems [7], [8]. Those systems use electric
pulses that target specific nerves in order to attenuate seizures.
The systems can administrate the pulse intermittently (open
loop) or activate the stimulus after some feedback reading
signals from the patient (closed loop).
II. E PILEPSY FORECASTING
Seizure detection systems provide a way to detect the
moment in which the seizure is occurring. The data for the
detection can come from many sources like electrocardiogra-
phy (ECG), accelerometry, chemical sensors and others [7].
The most common approach is the electroencephalography
signals (EEG) since previous research has been done by
neurologists to identify parameters that differentiate the base
state (interictal) to the state with an ongoing seizure (ictal).
Some methods have been optimized for real-time classifi-
cation and are used in the electric stimulation systems. An
example of this is the Neuropace, an implantable device able
to identify abnormal neurological activity and deliver pulses
to the vagus nerve.
A. Prediction systems
Although seizure detection has delivered improvement in
the treatment of seizure control and study, there are still
benefits on the prediction of seizures compared with simple
detection. Patients with epilepsy feel that the problem of the
uncertainty of seizures affects their life quality by inducing
fear to perform some activities along with psychological and
social problems [8].
Neuromodulation systems have shown a better performance
when the stimulus is applied moments before the seizure

978-1-5386-7033-0/18/31.00©2018IEEE
begins. The ability to predict seizures may also lead to alarm
systems that provide a way for patients to perform their daily
activities more secure by taking preventing actions prior to a
seizure. Predictions systems based on EEG signals hypothesize
the existence of a transition period called the preictal state, a
state where the patients present changes in physiological and
psychological activity.
The preictal state is still a research subject for neurologists,
the difference that it manifest with the interictal state appears
to be patient dependant. The time window that has to be used
for forecasting has yet to be determined and also changes from
patient to patient [9].
B. Proposed System
The stages considered for the system in this work are
based on the combination of many approaches for this task,
taking elements that have been used for seizure detection and
prediction. The stages are designed considering a Gaussian
Mixture Model-Hidden Markov Model (HMM) based classi-
fier, proposed as a final step. The steps are:
• Signal pre-processing: Filter the noise in the signals.
• Dimensionality reduction: Reduce the amount of data to
process in further steps.
• Feature extraction: Measurements from the signals.
• Classification: Train a GMM-HMM per each type of
signal and patient to identify them.
III. M ETHODOLOGY
A. Materials
The data chosen for this study were scalp EEG records,
they were acquired from the Children’s Hospital Boston-
Massachusetts Institute of Technology, dataset hosted in the
Physionet website [10]. The data consist of scalp EEG samples
of one hour each, sampled at 256 Hz with 16-bit resolution.
The recordings were acquired from 23 pediatric patients with
epilepsy as described in [11].
The recordings were segmented as in the work of Varathara-
jah et. al. [9] where 10-minutes clips are acquired from an
interval previous to the beginning of a seizure, and considering
a forecast horizon for possible ictal activity undetected by the
reviewers that made the annotations of the seizures. In this
case, a 30-minutes interval previous is proposed, acquiring
three preictal segments per recording with a seizure if possible.
The interictal segments were taken from recordings with no
ictal activity, taking care that in the following recording there
was no ictal activity when they correspond to the same session.
The algorithms for each stage are implemented for the
Python 2.7 programming language using the libraries of data
processing and machine learning from the SciKits [12]–[14].
The computer for the task is an HP (R) 14-k106la with an
Intel (R) i5-4200U 2.3 GHz processor and with Windows 10
(R) as the operating system.
B. Signal pre-processing
Traditional study of EEG signals proposes a frequency range
of 0.5 to 30 Hz, considering the delta, theta, alpha and beta
rhythms. Studies about epileptogenic activity have shown that
there is still relevant information above the typical range,
considering this, a broader range is used for the pre-processing
stage [15].
For the pre-processing stage, a band-pass filter is used to
attenuate components considered to be noise, coming from
other biological signals and movement artifacts. A 4th order
band-pass Butterworth filter is selected for this, the frequency
range is between 0.5 and 120 Hz.
To eliminate the noise coming from the power line a 2nd
order Butterworth notch filter is used with a rejection band of
57 to 63 Hz.
C. Dimensionality reduction
Real time computation of this methods is a key point to the
task of seizure prediction, this is why dimensionality reduction
techniques are commonly used [16]. Dimensionality reduction
techniques analyze high-dimensional data and transform it to
a new space where less variables are needed to represent
most of the information. The methods take into account what
is expected to be preserved in the new representation and
what form of information is needed. They are also useful for
exploration and visualization when the number of features is
too high to be represented on a graph.
1) PCA: Principal Component Analysis (PCA) is one of the
most popular techniques in Machine Learning tasks. It aims
to find a linear combination of the original variables using
the covariance matrix to obtain an orthogonal projection that
represents as much variance of the data as possible. The new
variables in this space are the principal components (PCs). The
projection of the data is defined by (1), where X is the original
data with dimension N by p, W is the matrix containing the
eigenvectors of the covariance matrix with dimension p by p
and Z are the PCs.
Z = WTX (1)
Each eigenvector is associated with an eigenvalue λi that
represents the amount of variance explained by that compo-
nent, that can be used to select how many eigenvectors from
the W matrix should be preserved in the final transformation,
preserving the ones that represent the highest variance. The
percentage of variance explained by the eigenvalues 1 to m,
considering being are ordered from highest to lowest, can be
computed using equation (2).
Pm
j=1 λj
var% = Pp (2)
j=1 λj
In this work, the number of remaining channels should
represent at least approximately 80% of the variance.
2) ICA: Another method commonly used to transform the
data is the independent component analysis (ICA). In this
algorithm, the data is supposed to be a linear mixture of
non-gaussian components from independent sources. The goal
for the algorithm is to find the transformation for the data
that either minimizes the mutual information (calculated using
measures like the Kullback-Leiber divergence and maximum
entropy) or maximizes the independence (calculated using
non-gaussianity approximate measures like kurtosis and ne-
gentropy) [17]. The new representation of the data is expressed
in (3), where X is the original data, A is the unmixing matrix
and Z the independent components.
Z = AX (3)
The goal of the algorithm is to find the elements of the
A matrix that give a representation of the data with the new
components as independent as possible.
3) PCA-ICA: The ICA algorithm performs better if some
pre-processing like whitening and detrending is applied, both
can be achieved by using PCA before ICA, with the additional
advantage of dimensionality reduction. If dimensionality re-
duction is used, the remaining matrix will be AW T where
W ∈ Rn×m and A ∈ Rm×m being n the number of original
channels and m the number of remaining channels.
D. Feature extraction
Applying a classification algorithm over the raw signals
can be both computationally expensive and difficult to find a
pattern to characterize the classes. The extraction of features
allows characterizing the behaviour of signals from hidden
information that can be obtained through calculations over the
data. The features proposed for the system are the following:
1) Entropy: Entropy is commonly described as a measure-
ment of the disorder of a system. In the information theory
field, entropy is a measurement of the uncertainty of the data.
The Shannon entropy is a nonlinear measurement used to
quantify the complexity level of a data series [18]. The formula
used to calculate the Shannon entropy is described at (4) with
p(i) being the probability of that value to appear.
k
X which states that for a sequence X = (x1 , x2 , .., xt−1 , xt )
H=− p(i) log p(i) (4)
i
2) Teager-Kaiser energy: The Teager-Kaiser energy is a
non-linear method for estimating the energy of a signal con-
sidering a second order or higher system, where both the
amplitude and the frequency influence the result [19]. The
calculation is carried out using the Teager-Kaiser operator
defined by equation (5), considering a discrete sequence
X = (x1 , x2 , ..., xn ).
Ψ(x[n]) = x2 [n] − x[n − 1] ∗ x[n + 1] (5)
3) Kurtosis: Statistical moments give information about
how the data is distributed. The most common moments are
the mean (1st moment) and variance (2nd moment) from the
normal distribution, Higher order moments, skewness and
kurtosis, describe the shape of the distribution; considering
a normal distribution, the typical values for both are zero and
are nondimensional. Kurtosis describes the relative peakdness
or flatness of a distribution [20]. The formula used to calculate
Fig. 1. Sequence of proposed features for a sine wave with three frequencies.
the Fisher’s coefficient of kurtosis is expressed in (6) with µ
as the mean and σ as the standard deviation.
N  4
1 X xi − µ
kurotsis(X) = −3 (6)
N i=1 σ
4) Feature sequence: The feature extraction is applied to
the signal by calculating the given formulas to a segment of the
signal with a fixed length or duration. Once all the features
are calculated, a vector is formed with each of the features
representing a dimension. This process is repeated for each
segment of the signal until the features for the whole signal
are obtained. This is represented in Fig. 1 where the features
for a sine wave with three different frequencies are obtained
for each segment of 20 samples.
E. Classification
For the classification part of the system the GMM-HMM
model is proposed. The classifier consists of a Hidden Markov
Model where the observable states are assumed to be a mixture
of Gaussians.
1) Hidden Markov Models: HMMs are used for modeling
a sequence of observable states with assumed hidden states
. HMMs used the Markov assumption, represented in (7),
the probability for the next state depends only on the actual
state [21].
P (xt |X) = P (xt |xt−1 ) (7)
In these models the sequences of observable states are
assumed to be caused by some hidden states. These hidden
states have a probability of emission for each of the finite set
of observable states, and also a probability for changing to
any other hidden state or to stay in the same one [22]. The
parameters to fit in these models for k hidden states and m
observable states are:
k
• An initial probability vector π ∈ R .
k×k
• A transition probability matrix A ∈ R .
k×m
• An emission probability matrix B ∈ R .
2) Gaussian Mixture Models: As the data from the features
is continuous, a clustering algorithm is needed to discretize the
data to a finite set of observable states [23]. GMM is a non-
supervised clustering algorithm that models a set of data as
the combination of Gaussian distributions [24]. The model is
 [b]
Fig. 2. Diagram for a HMM with three hidden states and four observable
states. The probabilities ai ∈ A are the transition probabilities among hidden
states, the bi ∈ B probabilities are the probabilities that the observable state
appears given the hidden state.
shown in (8) where φi represents the probability of belonging
to the cluster i, and each cluster has a normal distribution
N (µi , Σi ) with a vector of means µi and a covariance matrix
Σi .
k
X With the resulting data, the ICA algorithm was applied for
p(x) = φi N (µi , Σi ) (8)
i for this purpose, which is an efficient iterative algorithm
A parameter to measure if the number of clusters in the
resulting fitting is considered appropriate is the Bayesian In-
formation Criterion (BIC), that takes into account the number
of parameters and the likelihood of the model to evaluate the
model [25]. The BIC is expressed in (9) with L̂ being the
maximized likelihood, n the sample size and k the number of
parameters of the model.
BIC = −2 log (L̂) + k log (n) (9)
The models above are combined in a more complex model
called GMM-HMM. This models have been used for se-
quences of continous data where, for each each observation of
the sequence, first the GMM allows to identify the probability
of belonging to a cluster that will then be the observable
state for the HMM, the HMM then decodes the probability
of belonging to a hidden state given the observation and the
previous state (A matrix) or in the case of being the first
of the sequence, the probability of the sequence to start in
that state (π matrix). The overall likelihood of a sequence
X = (x1 , x2 , ..., xT ) for a given model is calculated by (10).
T
Y The HMM models were trained using a total of 169 clips
p(x1 , x2 , ..., xT ) = π(z1 )B(y1 |z1 ) A(zt |zt − 1)B(yt |zt )
t=2
(10)
Where yt denotes the observable state and zt the hidden
state at time t. The observable state yt can be obtained as
the most likely cluster for a GMM with θ parameters as
represented in (11).
yt = argmax(P (Y |xt , θ)) (11)
Fig. 3. Histogram distribution for both states using signals of 20 minutes of
recording for each state.
IV. R ESULTS
The recordings are first filtered using the proposed filters.
dimensionality reduction. The FastICA algorithm was used
to approximate non-guassianity maximization. The algorithm
first performs PCA for whitening and centering.
The channels were reduced to 6 as it was found that for 23
channels in the recordings, the first 6, after PCA, preserved
at least ≈ 80% of the variance. The resulting signals are
then unmixed using FastICA,which may converge to a local
minimum result as an iterative algorithm, this is why the
algorithm was run several times and the resulting matrix of
the combined best result was saved per each patient.
Once the data dimension was reduced and the resulting
channels are as independent as possible, the feature extraction
was applied. A running window of the equivalent to one
second of data (256 samples) calculates the three features
proposed and are saved as the feature vector for all the
segments in the signal. The histograms for the calculated
features for both states are shown in Fig 3.
Several GMMs were fitted using samples from preictal and
interictal states using a range from 5 to 20 clusters to find the
model that best described the distribution. For the clustering of
the given features, 15 clusters were found as optimal according
to the BIC criterion. The results of the clustering are shown
in Fig. 4.
of preictal state and 393 clips of interictal state, equivalent
to a total of 93.6 hours of data. The log-likelihood was
calculated for each sequence of data for each state, and the
model that presents the greater was saved as the model for the
corresponding state.
For each patient, a pair of models, one for each state, were
saved and evaluated, to generate a confusion matrix. Table I
shows the results for all the patients, obtaining a sensitivity
of 0.95 and a specificity of 0.86. In these type of systems a
 Fig. 5. Sequence of the extracted Teager-Kaiser Energy for a preictal state.
A seizure is marked between the dashed lines.

Fig. 4. Scatter matrix of features with the clusters found by the GMM
algorithm, each color representing a cluster. The diagonal of the matrix
represents an estimate of the kernels densities.

higher value of sensitivity than the specificity is preferred as

patients prefer false alarms than not detected seizures [8].

TABLE I
C ONFUSION M ATRIX

Predicted State Fig. 6. Sequence of features in the 10 minutes prior to a seizure. The seizure
Interictal Preictal Total is marked by the dashed lines.
True Interictal 345 48 393
True Preictal 7 162 169
Total 352 210 562
and the entropy measures the disorder in the system, however,
this can also happen in the interictal state.
TP A key difference for the preictal state is that the kurtosis
Sensitivity = ≈ 0.95 value shows a mirroring behaviour with increments at the
TP + FN
same time that the entropy decreases. This can be seen in
TN Fig. 6 and 7 with 10-minutes segments of the sequence of
Specif icity = ≈ 0.86 features (entropy, Teager-Kaiser energy and kurtosis from top
TN + FP
to bottom) containing a seizure. Both were acquired from the
patient chb01. It is important to mention that the reviewers
V. D ISCUSSION AND C ONCLUSIONS
marked a seizure between the seconds 2996 and 3036 as
Although the resulting matrix for ICA reduces the amount of highlighted by the dashed lines in Fig. 6 and a seizure is
information, the calculated features in the signals after being between 1467 and 1494 in Fig. 7.
processed with PCA and ICA, display simmilar patterns as It was also observed that the Teager-Kaiser energy displays
in the non-processed counterpart. The sequence of features is an increment as shown in Fig. 6 and 7 at the onset of the
preserved with the scale being the main difference. This is seizure and sometimes a few seconds in advance. This allows
illustrated in Fig. 5 for the same segment of a recording with to exclude the ictal state from the ones considered for the
a seizure and the calculated Teager-Kaiser feature before and study and it was found useful for the identification of the
after the processing. beginning of a seizure, thus obtaining the average seizure
Something to be noted is that in the preictal states some horizon to exclude from the preictal state. This also may lead
authors present the tendency of the entropy to decrease [18], to a technique for efficient seizure detection in a further work.
[26], [27]. This is observed also in this work at many intervals The proposed system is able to detect the preictal signals
before seizures. This is to be expected, as a seizure by with an accuracy of 0.9, comparable to other systems [28]. The
definition is caused by synchronous activity of the neurons system described in this work is able to characterize each state

Fig. 7. Sequence of features in the 10 minutes prior to a seizure. The seizure
is marked by the dashed lines.
of the signals for the analyzed recordings in order to predict
the most probable state. The usage of dimensionality reduction
algorithms allows to extract features able to characterize each
state with less calculations, something required for real-time
applications.
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