Effects of Speech Phonological Features During Passive Perception On Cortical Auditory Evoked Potential in Sensorineural Hearing Loss
Effects of Speech Phonological Features During Passive Perception On Cortical Auditory Evoked Potential in Sensorineural Hearing Loss
[Link]
HUA NONG TING*, ABDUL RAUF A BAKAR, JAYASREE SANTHOSH, MOHAMMED G. AL-ZIDI,
IBRAHIM AMER IBRAHIM & NG SIEW CHEOK
ABSTRACT
The deficiency in the human auditory system of individuals suffering from sensorineural hearing loss ( SNHL ) is
known to be associated with the difficulty in detecting of various speech phonological features that are frequently
related to speech perception. This study investigated the effects of speech articulation features on the amplitude
and latency of cortical auditory evoked potential ( CAEP) components. The speech articulation features included
the placing contrast and voicing contrast. 12 Malay subjects with normal hearing and 12 Malay subjects with
SNHL were recruited for the study. The CAEPs response recorded at higher amplitude with longer latency when
stimulated by voicing contrast cues compared to that of the placing contrast. Subjects with SNHL elicited greater
amplitude with prolonged latencies in the majority of the CAEP components in both speech stimuli. The existence
of different frequency spectral and time-varying acoustic cues of the speech stimuli was reflected by the CAEPs
response strength and timing. We anticipate that the CAEPs responses could equip audiologist and clinicians with
useful knowledge, concerning the potential deprivation experience by hearing impaired individuals, in auditory
passive perception. This would help to determine what type of speech stimuli that might be useful in measuring
speech perception abilities, especially in Malay Malaysian ethic group, for choosing a better rehabilitation
program, since no such study conducted for evaluating speech perception among Malaysian clinical population.
Keywords: Consonant-vowel (CV); cortical auditory evoked potential ( CAEP); electroencephalography (EEG);
mismatch negativity (MMN); sensorineural hearing loss (SNHL)
ABSTRAK
Kekurangan dalam sistem auditori manusia terhadap individu yang mengalami kehilangan pendengaran sensorineural
(SNHL) diketahui melalui kesukaran dalam mengesan pelbagai ciri ucapan fonologi yang sering berkait-rapat dengan
persepsi pertuturan. Kajian ini mengetengahkan kesan ucapan artikulasi terhadap amplitud dan kependaman pada
komponen potensi terbangkit auditori kortikal (CAEP). Ciri ucapan artikulasi termasuk kontras perletakan dan kontras
suara. Seramai 12 individu normal tahap pendengaran dan 12 individu yang memiliki SNHL telah direkrut untuk kajian
ini. Tindak balas CAEP terhadap isyarat kontras suara direkodkan pada amplitud lebih tinggi serta kependaman lebih
lama berbanding isyarat kontras perletakkan. Individu yang memiliki SNHL menghasilkan amplitud lebih tinggi berserta
kependaman lebih panjang dalam kebanyakan komponen CAEP s dan ini meliputi kedua- dua rangsangan ucapan.
Kewujudan perbezaan spektrum frekuensi dan beza-masa isyarat akustik pada rangsangan ucapan dicerminkan oleh
kekuatan tindak balas dan tempoh masa CAEPs. Kami menjangkakan bahawa tindak balas CAEPs dapat menyediakan
pengetahuan yang berguna kepada pakar audiologi dan doktor dalam memahami pengurangan potensi yang dihidapi
oleh individu persepsi auditori terjejas. Ini dapat membantu untuk menentukan apa jenis ransangan ucapan yang
bersesuaian dalam menilai keupayaan persepsi ucapan, terutamanya dalam kalangan etnik Melayu di Malaysia
seterusnya memilih program pemulihan yang lebih baik, kerana tidak ada kajian seumpama ini yang pernah dijalanlan
untuk menilai persepsi ucapan dalam kalangan penduduk klinikal Malaysia.
Kata kunci: Elektroensefalografi (EEG); hilang saraf deria pendengaran ( SNHL); konsonan-vokal (CV); korteks
auditori rangsang potensi (CAEP); kenegatifan tak padan (MMN)
FIGURE 1. Comparison of spectrogram for the three CV syllables. /ba/: 292 Hz (F0), 740 Hz (F1), 1481 Hz
(F2), 3228Hz (F3), 4310 Hz (F4); /da/: 291 Hz (F0), 759 Hz (F1), 1795 Hz (F2), 3155 Hz (F3), 4254 Hz
(F4); /pa/: 344 Hz (F0), 928 Hz (F1), 1523 Hz (F2), 3478 Hz (F3), 4437 Hz (F4)
and muscle movement. Since the study involved passive baseline level; and Inspected quantitatively in comparison with
listening conditions, all volunteers were informed to ignore the previous findings, and to be considered present if an
the incoming auditory stimulus, stay awake and focused on individual’s CAEP components had maximum correlation
the Malay reading material that was provided to them. Each coefficient (r) and significant value (P<0.05). The N1 and
N2 components were identified as the most negative
set of experiments was done in about 30 min per run.
peak occurred between 80-150 ms and 180-250 ms,
CORTICAL AUDITORY EVOKED POTENTIAL (CAEP) respectively, immediately after the stimulus onset. P1 and P2
WAVEFORMS MEASUREMENT AND DATA ANALYSIS were defined as the most positive deflection happened
After completion of the CAEP data recording, the evoked between 55-80 ms and 145-180 ms post-stimulus onset,
response was pre-processing offline to remove artifacts, respectively. P3 was scored between 220-380 ms, illustrated
correct baseline drift and filter the power supply. These by the most positive peak appeared after the stimulus onset
processes were done using a notch filter at 50 Hz and a within this response window. The difference of the CAEP
Butterworth band-pass filter of 1-45 Hz. For each set of waveform for each set of speech stimulus was used to measure
experiments, the two successive runs of each group’s standard the MMN response, which was obtained by subtracting the
and deviant stimuli were averaged. Due to the implementation averaged responses of the deviant stimuli from the averaged
of the counterbalance paradigm in this study, the evoked responses of the same stimuli presented as the standard. MMN
response obtained from the counterbalance standard and was defined as a component having the largest
deviant stimuli were summed and averaged with the previous negativity occurring between 100-250 ms at electrode
session. Finally, each set of stimulus presentation will produce positions Fz or Cz (Duncan et al. 2009; Li et al. 2016). The
evoked responses which were classified as ‘standard’ and appearance of MMN was confirmed when it had more
‘deviant’ and grouped separately. The standard average negative amplitudes at the fronto-central electrode site (Fz and
response which appeared immediately after the deviant Cz) in comparison with the parietal site (Pz). The amplitude of
stimulus was excluded from the analysis. evoked responses was compared with the prestimulus baseline
The rules used to justify the existence or absence of a and measured as the greatest amplitude recorded followed by
response to the passive condition were as follows: CAEP the latency measurements taken at the center of the peak
was inspected visually by two raters and considered to be obtained within the respective response window (Duncan et al.
present if an individual CAEP peak (e.g. P1, N1, P2, N2, 2009; Oates et al. 2002). The late CAEP amplitude and latency
components
MMN and P3) had higher amplitude than the pre-stimulus
were recorded from each individual response windows to
develop the grand-mean-waveforms for each CVs stimulus
(i.e. /ba/-/da/ and /ba/-/pa/) respectively as per the two 2481
types of experimental groups (i.e. normal hearing ( NH) and
sensorineural hearing loss (SNHL)). The amplitudes and factors highlighted in the ANOVAs were as follows;
latencies of various CAEP components were then assessed speech stimuli /ba/-/da/ and speech stimulus /ba/-/pa/.
independently between hearing impaired subjects ( SNHL) The main effects and interaction with the CAEPs
and controls as ‘standard’ and ‘deviant’. component were considered significant if p<0.05.
FIGURE [Link] CAEPs waveforms (Cz) recorded from a control subject. The top row waveforms are CAEP waveforms for the
averaged standard and deviant stimulus, which response to the placing contrast stimuli (/ba/-/da/). The bottom row waveforms are
CAEP waveforms for the averaged standard and deviant stimulus, which response to the voicing contrast stimuli (/ba/-/pa/)
2482
FIGURE [Link] CAEP s waveforms recoded from a SNHL subject. The top row illustrates the CAEP waveform response to the
placing contrast stimuli and the difference waveform recorded at Cz. The bottom row is CAEP waveform response to the voicing
contrast stimuli and difference waveform recorded at Cz
FIGURE 4. Mean and SD amplitude for both control and SNHL groups across two types of speech stimuli
Table 1 shows the amplitudes and latencies of the P3 components in response to both speech stimuli. SNHL
recorded CAEPs waveform at Cz electrode for both subject group showed a delayed and greater response towards
groups. P1 component experienced shorter timing response voicing contrast stimulus. The deviant response on each
in /ba/-/pa/ stimulus at both groups study. The same set of stimuli showed contradictory trend when it
response was shown by P2 component in /ba/-/da/ stimulus. showed higher latency and greater amplitude during
Both N1 and N2 components having similarity when both voicing contrast stimulus but happened at earlier
evoked longer average latencies in response to voicing response timing with the same pattern of neuron
contrast compared to the placing contrast stimulus. Figure activation in placing contrast stimulus, and these were
5 shows the individual’s data distribution of CAEP true for both SNHL and normal hearing groups.
2483
TABLE 1. Mean and SD latencies of CAEPs components and MMN for control and SNHL groups
FIGURE 5. Amplitude and latency plots for P3 component for different types of stimuli and subject
groups. Scatterplots demonstrate individual amplitude and latency values for P3 component
The result of two -way repeated measures ANOVAs ANOVAs outlined a significant effect for /ba/-/da/ stimuli on
showed that there are no significant differences in the P1, N1 and MMN amplitudes. The results of the ANOVAs
average CAEPs amplitude and latency between the response reported that a significant main effect was found on the
elicited by the standard and deviant stimuli. Evidence P1 amplitude in response to the placing contrast stimulus
found in both experimental groups with both sets of between groups (p<0.001). No significant difference was
stimuli; therefore, both types of stimuli were averaged found for P1 component in response to voicing contrast
together for that particular articulatory feature to find stimulus and there was no significant interaction between
any significant difference on CAEP components between both sets of speech stimulus (p=0.135 and p=0.406). Both
groups’ response to both speech stimuli. The result of the N1 and P3 amplitudes and latencies showed a significant
2484 main effect on both speech phonological features between
control and SNHL groups (N1: p<0.001 vs p =0.015, p=0.006
vs p<0.005; P3: p<0.001 vs p=0.029, p<0.001 vs p=0.001).
A significant interaction between both types of speech
features was found. However, no evidence of any significant increment compared to standard type for both stimuli.
interaction was found for N1 amplitude (N1: p=0.075, This finding complied with that of the earlier study
p=0.038; P3: p=0.042, p=0.003). As for MMN response, when the researchers outlined the enhancement of the
significant difference was reported in amplitude and latency P2 component when targeting infrequent stimulation
for their response to /ba/- /da/ stimulus compared to the (Davies et al. 2010; Luck 2005; Steinhauer 2014).
/ba/-/pa/ stimulus (p=0.036 and p=0.004). Similarly, no
statistical significance was found in the interaction between EFFECTS OF THE FEATURES OF SPEECH ARTICULATION ON THE
both sets of speech stimulus. AMPLITUDES AND LATENCIES OF BOTH N1 AND N2
N1 component which originally arising from superior temporal
DISCUSSION gyrus region provided important aspects in performing spectral
and temporal acoustic discrimination tasks during spatial
attentional process between various speech articulation
MAIN FINDINGS features. This is proven when it’s having significant main
The primary purpose of the present study aimed to determine effects on most of the ANOVAs testing (Luck 2005;
the implication of various speech phonological features Näätänen & Picton 1987). We reported that the average
towards amplitudes and latencies of late CAEPs components mean amplitude of the auditory N1 and N2 were attenuated in
between healthy group and individuals suffering from SNHL on SNHL subjects compared to that in normal subjects. This
Malaysian Malay native speaker population. The auditory suggested the encoding deficits in auditory processing
evoked responses were successfully recorded from both study information of hearing impaired subjects. Our finding
groups. Independent t-test showed that there was no agreed with that of the previous studies where the low-level
significant difference in age between the control group and of N1 auditory response was found in subjects with
the SNHL subjects (t22df=1.4, p>0.05). In this study, only misophonia and aphasia (Becker & Reinvang 2013; Schröder
Central (Cz) electrode was selected for further analysis as et al. 2014). These similarities suggested that the center
it had the most significant effects on CAEP waveforms in auditory process of sensorineural of the subject might interfere
response to speech stimuli and it showed the highest signal to with some speech perception disorder. Specifically, the
noise ratio compared to other electrode sites (Duncan et al. deprivation situation was more prominent in the auditory
2009; Korczak & Stapells 2010; Steinhauer 2014). The Cz N1 response towards the place of articulation feature
electrode provided clearer and more stable CAEP waveforms compared to voicing contrast stimulus. In contrast, there
compared to the Fronto-electrode (Fz) on both speech stimuli were no clear justification involving the resemblance
circumvent in both experimental groups. The presentation of finding between N1 and N2 components, however may
MMN response was maximal in the Cz which was in agreement indeed reflect the reliance of cortical auditory response
with the previously reported studies (Duncan et al. 2009; towards phonologic features of speech signal (Bien et al. 2016;
Steinhauer 2014). The percentage of detectability for the CAEP Carpenter & Shahin 2013; Scharinger et al. 2016).
components including both study groups were: P3 was
present in 100%, N2 was present in 96.25%, P2 was
76%, N1 was 82.5%, P1 was present in 74.8% and IMPLICATION OF SPEECH STIMULUS ON MISMATCH
finally MMN which was present in 75% of all averages. NEGATIVITY (MMN) RESPONSE AND P3 COMPONENT
The MMN response was elicited in contrast to Malay CV
stimuli due to the presence of the language memory traces.
EFFECTS OF THE FEATURES OF SPEECH ARTICULATION ON THE This finding supported the previous decision when
AMPLITUDES AND LATENCIES OF BOTH P1 AND P2 MMN response was shown in speech stimuli and were
P1 and P2 components both elicited higher mean amplitude in enhance when the individuals having automated access to
response to voicing contrast compared to the placing contrast the native-language phonetic prototypes (Becker &
stimulus. The result of P1 component reported here fostering Reinvang 2007; Näätänen 1995). Both normal and
similarity with the previous finding where the average SNHL subjects exhibited parallel neurons activation when
amplitude elicited from the SNHL subject was higher than the producing higher negativity response and delayed
control group for both stimuli (Schröder et al. 2014). The latencies in voicing contrast stimulus. Our finding
previous study emphasized the difficulty to assess showed that the MMN response elicited by the SNHL
accurately the P1 component due to the interaction with C1 subjects was smaller (almost half of the activation) and
waves from a visual event-related potential ( VERP) component recorded at longer latencies on both CVs speech stimuli
which created a major overlapping mechanism with the P1 compared to that of the control group. In other words, the
CAEP component (Luck 2005). The deviant stimulus of difference in MMN auditory response of hearing impaired
auditory P2 experienced some amplitude subjects was found to reflect not only the detection of
speech phonologic features, but also revealed the
anomalies in physiological measure of automatic
discriminant ability involving central processing in
audition (Näätänen 1995; Näätänen & Escera 2000).
The P3 component increased dramatically when
they had 100% appearance for all the average values.
The introduction of deviant stimuli resulted in
tremendous increment compared to other components; 2485
which showed the P3 component as the most influential
element in understanding CAEPs waveforms in response The rapidly changes of formant transition during CV
to various speech phonologic features as it reflects passage supported the occurrence of higher amplitudes
an involuntary switching of passive listening to the odd and prolongation timing responses of CAEPs components
or deviant stimulus (Reis & Iório 2007). happened in voicing contrast stimulus, thus underlying
In this study, the congruence of majority of the result passive discrimination process to be a difficult task
demonstrated larger CAEP amplitudes and longer latencies for to operate. Similar study was done by Tremblay et al.
response to the voicing contrast compared to that of the (2003) where they highlighted the delayed neuronal
placing contrast across both subject groups. A plausible synchronous response of the older adult population
explanation contributed to this pattern of responses may be associated with disruption on the speech discrimination
related to the spectrum energy correlates within these sets of when dealing with time varying speech cues along /ba/
stimuli. Agung et al. (2006) expressed the domination of low- and /pa/ CVs token stimulus. Larger amplitudes and
level spectral energy in speech sound which produced higher delayed response to stimuli with longer VOT duration
N1 and P2 amplitudes with longer latencies happened on P1, were experienced by older subjects.
N1 and P2 components in comparison with the speech sound The current study utilized the CAEP technique in obtaining
having higher frequency spectral energy. One possible valuable information using dynamic methods of monitoring
explanation coincided with the spectral difference occurred on the cognitive neurological disorder related to people having
the frequency separation between formant 1 (F1) and formant sensorineural hearing loss. One of the key advantages of the
2 (F2) frequencies of voicing contrast having approximately technique is the sensitivity of CAEP signal in compensating
500-750 Hz which was narrower compared to the placing their voltage deflections at higher level processing by
contrast which having 700-1100 Hz formant separation specific experimental manipulation especially during
(Korczak & Stapells 2010; Ting et al. 2011; Wunderlich & selective attention, expectancy, passive listening and memory
Cone-Wesson 2001). This condition likely increased the updating (Duncan et al. 2009; Picton et al. 2000). This
difficulty to the brain speech discrimination on voicing indirectly helps the researcher to focus on the stages of
contrast recognition in comparison with the two consonant processing which are affected by the given experimental
contrasts, thus lead to wider activation of cortical neurons manipulation (Luck 2005; Steinhauer 2014). Besides that,
resulting in higher voltage and delayed latency recorded during the second advantage of CAEP is the capability of this potential
phonemes discriminant task. Tavabi et al. (2009) proved that activity to be measured online without the need of behavioral
the deeper part of the brain responded better towards high- response. This greatest advantage makes CAEP recordings
frequency stimulation compared to superficial region of possible even without the subject’s attention and response. For
the human cortex which responded better to low frequency this reason, the present study assesses various speech CV
information, thus indirectly supported the present finding stimulation to understand how the brain performing CAEP
on greater response amplitude. Earlier studies also reported the discriminant task between impaired and normal hearing
higher amplitude response on speech stimulus due to the broad people.
frequency spectrum in comparison with that of the tonal On the other hand, CAEP also has disadvantages
stimuli (Wunderlich et al. 2006). especially during the data collection. CAEPs are microvolt
level electrical signals that are recorded together with
Another possible explanation contributed to this finding various types of artifact and random noises. Thus, lots of
was due to the increment in onset voicing duration of the successful trials are needed to maintain the data reliability
Malay CV /ba/-/pa/ stimulus in comparison to placing contrast and accuracy. The successful trials can range from
stimulus. As shown in Figure 1, the voice onset time ( VOT) fifty to few thousands per subject for each specific
duration differed between the three syllables. Namely, CV experimental condition (Bidelman 2015; Duncan et al.
syllables /ba/ and /da/ stimuli had the same configuration of 2009; Korczak & Stapells 2010; Oates et al. 2002;
the vocal tract but differ in their VOT, as the release sound Wunderlich & Cone-Wesson 2001). This will directly
for /b/ takes a shorter time than for /d/. During the stimulus prolong the data recording process and it will be
presentation involving CV transition, there were no great unpractical for certain patient’s conditions. In this study,
changes occurred in terms of VOT for /ba/-/da/ stimulus as both 160 deviant stimuli and 640 standard stimuli were recorded
for each subject. This number is in line with requirement of
exert the same voicing pattern with negative VOT. Conversely,
the optimal CAEP recording procedure.
during the CV transition in /ba/-/pa/ stimulus, there was a great
The highly complexity, nonlinearity and non-stationary
alteration in voicing onset duration when the /pa/ syllable
waveforms characterized by electroencephalogram ( EEG)
having positive VOT (longer), in which voicing for the vowel
signals make the clinical interpretation a challenging phase.
happened after the plosive burst. These temporal cues
Several non-linear methods presented by previous researchers
properties acted as a major identification of voiced and
including sample entropy (SampEnt), higher order spectra
voiceless phoneme.
(HOS), fractal dimension (FD) and recurrent quantification
analysis (RQA) provide a better and valuable mechanism for
result interpretation (Acharya et al. 2015, 2011; Chua et al.
2011, 2009). For the last two decades, more exploration was
conducted using nonlinear dynamic
2486 method in giving potential understanding as this technique
extracts hidden complexity in the time series brain signal
(Lehnertz 2008; Mormann et al. 2005, 2003).
According to Acharya et al. (2013), higher order spectra
(HOS) method is considered as one of powerful mechanisms CONCLUSION
to justify the presence of abnormalities, besides usefulness
Our study done on local ethnic Malay population, had
in the event of signal distortion due to Gaussian noise. This
proven the significant effects of cortical auditory
framework has been persistently used in the field to
evoked potential (CAEP), in discriminating speech
study epilepsy disorder (Chua et al. 2011, 2009).
acoustical complexity with various speech phonological
In earlier studies, Babloyantz et al. (1985) used
features in people with sensorineural hearing loss. CAEP
non-linear methods such as correlation dimension ( CD)
signals appeared to be an effective way to study the
and largest Lyapunov exponents (LLE) to study the
human brain signal during the sleep cycle. Besides that, auditory processing stages and ailments related to the brain.
Song et al. (2004) used recurrence quantification The mean CAEP amplitudes and latencies for most of the
CAEP components were considerably larger and delayed in
analysis (RQA) method to scrutinize cortical functional at
different sleep stages including people suffering from response to voicing contrast compared to placing contrast.
sleep apnea syndrome. MMN was clearly elicited in both study groups which
In 2012, a group of researchers took the initiative to showed that the MMN is a suitable tool in performing
propose a method using four different entropies, i.e. behavioral change detection as well as in the attention-
approximate entropy, sample entropy, phase entropy 1, and dependent physiological measures of the human auditory
phase entropy 2, to interpret EEG signals involving epilepsy pathway. It may be easier for brain to discriminate the cues
disorder. With the application of various classifiers, of the placing contrast compared to that of the voicing
fuzzy classifier was concluded as the best technique contrast through shorter response time and lower
and the most suitable tool in performing automatic amplitude. This result is likely due to the larger frequency
detection of normal, pre-ictal and ictal conditions of spectral and longer time varying that present between
epilepsy with an accuracy of 98.1% (Acharya et al. 2012). these speech contrasts. The present finding would be
Extended idea was done by the similar author Acharya of great help to clinicians in selecting appropriate features
et al. (2015) using several non-linear methods on EEG of speech articulation that can give good response in
signal analysis for developing robust automated diagnostic evaluating passive speech perception among people with
system for depression called depression diagnosis index sensorineural hearing loss. In light of this development the
(DDI). The authors also implemented several types of research also conveys better knowledge regarding brain
classifier, which finally conclude that support vector mechanisms in discriminating various speech phonemes.
machine (SVM) as the most effective classifier in terms The outcome of presence study might be helpful for clinical
of accuracy, sensitivity and specificity. The novel diagnosis, to help further in investigate the effects of
features combination in the study proved the efficacy
central auditory processing in elderly people with
of non-linearity method in assisting medical
sensorineural hearing impairment.
professionals by developing diagnostic index tools for
measuring the severity of depression (Acharya et al. 2015).
ACKNOWLEDGEMENTS
To improve signal denoising process, Wang et al.
(2013) proposed a method called empirical mode This research was funded by the University Malaya
decomposition (EMD). The adaptation of this method Research Grant (Grant Number: UMRG RP016D-
was widely used in short inter-stimulus intervals, i.e. 13AET). The authors expressed their gratitude to all
when inverse process of overlapping between desired volunteers who participated in the experiment. The
CAEPs may occur. The authors had successfully authors declared no conflict of interests.
improved the signal-to-noise (SNR) ratio in the raw EEG
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