Epilepsy & Behavior 60 (2016) 81–85

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Epilepsy & Behavior

journal homepage: www.elsevier.com/locate/yebeh

Auditory temporal processing in patients with temporal lobe epilepsy

Azam Navaei Lavasani a, Ghassem Mohammadkhani a,⁎, Mahmoud Motamedi b, Leyla Jalilvand Karimi c,
Shohreh Jalaei d, Fereshteh Sadat Shojaei e, Ali Danesh f, Hadi Azimi g
a
Department of Audiology, School of Rehabilitation, Tehran University of Medical Sciences, Iran
b
Department of Neurology, School of Medicine, Tehran University of Medical Sciences, Iran
c
Department of Audiology, School of Rehabilitation, Shahid Beheshti University of Medical Sciences, Tehran, Iran
d
Department of Physiotherapy, School of Rehabilitation, Tehran University of Medical Sciences, Iran
e
Department of Psychology, School of Psychology, Islamic Azad University, Tehran Central Branch, Iran
f
Department of Communication Sciences and Disorders, Florida Atlantic University, Boca Raton, FL, USA
g
Department of English Language Teaching, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

a r t i c l e i n f o a b s t r a c t

Article history: Objective: Auditory temporal processing is the main feature of speech processing ability. Patients with temporal
Received 2 August 2015 lobe epilepsy, despite their normal hearing sensitivity, may present speech recognition disorders. The present
Revised 2 April 2016 study was carried out to evaluate the auditory temporal processing in patients with unilateral TLE.
Accepted 4 April 2016 Materials and methods: The present study was carried out on 25 patients with epilepsy: 11 patients with right
Available online xxxx
temporal lobe epilepsy and 14 with left temporal lobe epilepsy with a mean age of 31.1 years and 18 control
participants with a mean age of 29.4 years. The two experimental and control groups were evaluated via gap-
Keywords:
Temporal processing
in-noise and duration pattern sequence tests. One-way ANOVA was run to analyze the data.
Temporal resolution Results: The mean of the threshold of the GIN test in the control group was observed to be better than that in
Gap-in-noise test participants with LTLE and RTLE. Also, it was observed that the percentage of correct responses on the DPS test
Duration pattern sequencing test in the control group and in participants with RTLE was better than that in participants with LTLE.
Temporal lobe epilepsy Conclusion: Patients with TLE have difficulties in temporal processing. Difficulties are more significant in patients
with LTLE, likely because the left temporal lobe is specialized for the processing of temporal information.
© 2016 Elsevier Inc. All rights reserved.

1. Introduction
Temporal lobe epilepsy (TLE) is one type of epilepsy that can bring
about significant effect on auditory processing. The temporal lobe
encompasses primary and secondary auditory areas, which require
anatomical and functional integrity. This integrity is necessary for
correct perception and interpretation of auditory signals. Temporal
lobe epilepsy can cause numerous electrical discharges in these areas
[1]. Even though patients with TLE may have normal hearing sensitivity,
they may show speech recognition or speech processing disorders [2].
Sensory encoding of temporal characteristics of signals such as duration,
interval, and the order of stimuli provides information to the nervous
system for speech perception [3].
Temporal resolution is the minimal time required to segregate
acoustic events and plays an important role in speech recognition. For
example, in order to discriminate between two phonemes /ba/ and /
pa/, the voice onset time (VOT) is essential. This is because the identifi-
cation of consonant–vowel syllables depends on the interval between
⁎ Corresponding author at: Audiology Dept., Faculty of Rehabilitation, Tehran University
of Medical Sciences, Iran. Tel.: +98 21 88053299.
E-mail address: mohamadkhani@tums.ac.ir (G. Mohammadkhani).
air release and vocal vibration [3]. The gap-in-noise (GIN) test is a
new test that evaluates temporal resolution [4]. In addition, temporal
ordering or sequencing refers to the processing of two or more auditory
stimuli in their order of occurrence in time, which has a particular im-
portance in speech perception. One of the tests available to evaluate
the ability of temporal sequencing is the duration pattern sequence
(DPS) test [5]. It is a specialized test which is sensitive to cortical lesions,
particularly in the temporal lobe.
In two studies carried out on patients who underwent anterior tem-
poral lobectomy surgery, gap detection threshold was reported to in-
crease for the contralateral ear to the lesion [6,7]. In a study on twelve
participants with brain damage, Musiek et al. revealed that pitch pattern
sequence test and duration pattern sequence test involve different pro-
cesses of higher auditory areas [5].
Ehrlé et al. found that patients with left temporal lobe epilepsy
(LTLE), compared with those with right temporal lobe epilepsy (RTLE)
and healthy participants, had poorer performance in anisonchrony
discrimination of auditory rapid sequences [8]. Bamiou et al. reported
that patients with left hemisphere lesions, compared with those with
right hemisphere lesions, had a lower percentage of correct responses
in the DPS test, and both groups had an increased GIN threshold in
one or both ears [9]. In a study on patients with split brain damage, it

http://dx.doi.org/10.1016/j.yebeh.2016.04.017
1525-5050/© 2016 Elsevier Inc. All rights reserved.
82 A.N. Lavasani et al. / Epilepsy & Behavior 60 (2016) 81–85
was shown that neither hemisphere is able to process temporal patterns
alone [10]. In another study, it was revealed that patients with temporal
lobe epilepsy have a processing disorder in duration detection indepen-
dent of the side of lesion [2]. Aravindkumar and colleagues studied pa-
tients with complex partial seizures and mesial temporal sclerosis
(MTS) and found that the thresholds of GIN were abnormal for the ma-
jority of patients with MTS in at least one ear [11].
Since classic gap detection procedures are often time-consuming
and not available to clinicians, the present study employed the GIN
test to evaluate temporal resolution [3]. In general, there is little infor-
mation on auditory temporal processing in this clinical population. As-
sessment of temporal processes are essential for the proper diagnosis
and management of disorders associated with temporal processing
[12]. These include clinical measures of temporal ordering and temporal
resolution. In the current study, The GIN and DPS tests were used; both
of which are sensitive to the measures mentioned.
There are many unanswered questions about temporal processing
abilities in patients with RTLE and LTLE, such as the asymmetry of
hemispheric performance on a variety of functions. The present study
aimed at evaluating auditory temporal processing in patients with
unilateral temporal lobe epilepsy utilizing the GIN and DPS tests.
2. Methods
2.1. Participants and procedures
The present cross-sectional noninterventional study was conducted
on 25 participants with TLE with a mean age of ±31.1 years.
Participants were comprised of 11 patients with RTLE and 14 with LTLE
as well as 18 age-matched healthy controls with a mean age of
±29.4 years in the Audiology Clinic of the Faculty of Rehabilitation at
Tehran University of Medical Sciences. Experimental participants with
temporal epilepsy were diagnosed by a neurologist following presurgical
investigations, including MRI and video-EEG monitoring, and were then
referred to the researchers (Table 1).
The inclusion criteria were age range between 20 and 50 years,
normal peripheral hearing sensitivity ≤ 20 dB HL in frequencies from
250 to 8000 Hz, bilateral normal tympanograms, and normal acoustic
reflexes in both ears. Speech recognition thresholds (SRTs) were also
established using standardized spondee words using live voice. The
SRTs were confirmed by pure tone averages in all the participants.
Right-handedness was revealed via Edinburgh Handedness Scale
(EHS). Additionally, participants had no previous history of depression
or brain trauma, which could affect the nervous system. In addition, par-
ticipants had no history of brain or brainstem surgery, or otologic, and
audiologic impairment.
All the participants signed a consent form after they were informed
about the nature and purpose of the study. The informed consent form
was approved by the Ethics Committee, Tehran University of Medical
Sciences. Participants underwent an ear inspection by a licensed audiol-
ogist for cerumen impact. Pure-tone audiometry was performed utilizing
a clinical audiometer (AC40, Interacoustics, Denmark) in a sound-treated
Table 1
Distribution of epileptic foci based on the hemisphere with temporal lobe epilepsy (25 =
number).
Groups Location Number Relative
frequency
Right temporal lobe epilepsy (n = 11) Anterior 8 72.7%
Posterior medial 1 9.1%
Occipitotemporal 2 18.2%
Total 11 100%
Left temporal lobe epilepsy (n = 14) Anterior 8 57.1%
Posterior medial 4 28.6%
Occipitotemporal 2 14.3%
Total 14 100%
acoustic booth and TDH 39 headphones calibrated within one year of the
evaluation based on the current 2006 ANSI standards. Tympanometry
and acoustic reflex tests (ipsilateral and contralateral) were performed
using a clinical tympanometer (Zodiac 901, Madsen, Denmark) calibrat-
ed to 2006 ANSI standards.
The GIN and DPS tests were conducted in a sound-treated room.
Stimuli were routed via a CD and the diagnostic audiometer to TDH-
39 headphones. Participants were instructed regarding their response
to the GIN and DPS tests by the examiner. Stimuli to the GIN test includ-
ed a series of 6-second segments of broadband noise that were present-
ed at 50 dB SL (sensation level) compared with the speech recognition
threshold separately on each ear. Each of the segments contained
anywhere from 0 to 3 gaps of silence. The participants responded to
the examiner by pushing a button as soon as they perceived a gap.
Each segment was separated with a five-second gap, and the order of
the gap duration was randomized. The durations of the silence
gaps were 2, 3, 4, 5, 6, 8, 10, 12, 15, or 20 ms. The GIN test was composed
of four different lists. Each gap was presented 6 times in each GIN list. As
a result, each GIN list contained a total of 60 gaps per list. A practice list
consisted of 10 items presented prior to the beginning of the test to en-
sure that the participant understood the task. Participants were
instructed to press a button whenever they perceived the gap. An
error response was recorded when the participants missed a gap. Gap
threshold and percentage of the correct responses are two criteria for
this test. Gap threshold is the shortest gap duration for which there
were at least “four of six” correct identifications. This performance
was recorded as the participants' threshold for duration. The previous
research [4] supports the sufficiency of only two lists, and thus, the
current study employed only two lists.
The conditions for administrating the DBS test were similar to those
for GIN (sound-treated room and presentation of stimuli by CD via a di-
agnostic audiometer). The DPS test was composed of three pure tones
with the same frequency (1000 Hz) and two durations (250 ms or
short duration and 500 ms or long duration) and a 300-ms interstimu-
lus interval with 10-ms fall/rise time. Each tone has a longer or shorter
duration compared with the other two tones, and it is presented in 6
different pattern randomizations (LLS, LSL, SLL, SLS, LSS, and SSL). The
interval between each pattern was 6 s. The test was administrated at
50 dB SL compared with the threshold at 1000 Hz. Each pattern was rep-
resented 10 times randomly for a total of 60 practice presentations. Each
ear was separately presented with the stimuli 30 times. Participants
were instructed to respond to the signal patterns verbally (long or
short). They were also instructed to guess if they were not certain. The
practice list consisted of 10 items, which were presented prior to the
actual test in order to ensure that the participant understood the task.
Subsequently, 30 items were presented to each ear, and participants
were asked to identify the pattern. The data registry criterion for this
test was the percentage of the correct responses.
2.2. Statistical analysis
The SPSS (v. 16) was used to analyze the data. Following the confir-
mation of the normal distribution of the data by Kolmogrov–Smirnov
test, data were analyzed by one-way analysis of variance (ANOVA),
paired t-test, and Pearson's correlation coefficient. The statistical
significance was set at p b 0.05.
3. Results
The means and standard deviations of GIN and DPS test parameters
in controls and participants with LTLE and RTLE are given in Table 2. The
mean of GIN threshold in the right ear and the left ear in the control
group was observed to be better than that in participants with LTLE
and RTLE, and the percentage of correct responses in GIN evaluation in
the control group was better than that in the participants with LTLE
and RTLE. The percentage of the correct responses on the DPS test in
 A.N. Lavasani et al. / Epilepsy & Behavior 60 (2016) 81–85
Table 2
Comparison of threshold of the GIN test (ms) and the percentage of correct responses of two tests between right and left ears in the three groups of control participants and participants
with RTLE and LTLE (43 = number).
Test measures Mean (SD) in group with LTLE
(n = 14)
Left ear Right ear
Threshold of the GIN test (ms) 7.2 (2.6) 6.64 (2.9)
p-Value 0.18
Percentage of correct response [GIN] (%) 58.3 (1.3) 61.06 (1.3)
p-Value 0.23
Percentage of correct response [DPS] (%) 63.5 (2.34) 63.08 (2.2)
p-Value 0.9
control participants and participants with RTLE was better than that in
participants with LTLE. No statistically significant difference was detect-
ed between the control participants and group with RTLE. None of the
three groups demonstrated a significant difference in the mean scores
of the two tests between right and left ears (p N 0.05).
Based on the studies by Musiek et al. [4,5] and Aravindkumar et al.
[11], the cutoff criterion between normal and abnormal performance
was determined by two standard deviations from the mean scores in
the control group. The data obtained in the present study showed that
the GIN threshold above 6.16 ms and the percentage of correct re-
sponses below 56.32 in the GIN test and 84.67 in the DPS test were con-
sidered abnormal. Based on the suggested cutoff scores, 56% of the
participants with temporal lobe epilepsy (14 out of 25 participants)
had an abnormal threshold in the GIN test while 28% (7 out of 25 partic-
ipants) had an abnormal percentage of correct responses.
All the control participants had GIN thresholds better or less than
6.16 ms. In the group with RTLE, two participants had abnormal scores
only in the right ear, two participants only in the left ear, and three
participants in both ears. In the group with LTLE, two participants had
abnormal scores only in the left ear, and four participants had abnormal
scores in both ears (Fig. 1). Abnormal scores in the DPS test were ob-
served in 85.7% of the group with LTLE (11 out of 14 participants in
both ears and 1 in the left ear) and 27.27% of the group with RTLE (3
out of 11 participants, 2 participants in the right ear, and 1 in the left
ear) (Fig. 2).
The ANOVA revealed significant differences between the three
groups in the mean GIN threshold scores (p = 0.006 & p = 0.007 in
the right and left ears, respectively). This difference was significant be-
tween control participants and participants with RTLE (p = 0.01 &
0.02 in the right and left ears, respectively) and between the control
group and the group with LTLE (p = 0.03 & 0.012 in the right and left
ears, respectively). There was no significant difference between partici-
pants with RTLE and LTLE (p = 0.84 & 0.99 in the right and left ears,
respectively) (Fig. 3).
Fig. 1. Frequency of abnormal thresholds of the GIN test (ms) in the right, left, both, and
none of the ears of participants with right and left temporal lobe epilepsy with cutoff
criterion of 6.16 ms.
83
Mean (SD) in group with RTLE Mean (SD) in control
(n = 11) participants (n = 18)
Left ear Right ear Left ear Right ear
7.18 (2.3) 7.09 (2.2) 5.1 (0.83) 4.77 (0.54)
0.9 0.055
57.9 (1.3) 59.2 (2.8) 69.2 (8.3) 70.7 (6.4)
0.66 0.28
93.6 (6.2) 93.6 (6.04) 92.6 (5.5) 94.99 (4.9)
1 0.06
Significant differences were also observed between the three groups
in the DPS test (p = 0.000 & p = 0.000 in the right and left ears, respec-
tively). Moreover, there was a significant difference between partici-
pants with RTLE and LTLE (p = 0.000 in the right and left ears) and
between the control group and the group with LTLE (p = 0.000 in the
right and left ears), but no significant difference was observed between
the control group and the group with RTLE (p = 0.96 & 0.97 in the right
and left ears, respectively) (Fig. 4).
There was no significant correlation between the values obtained for
the DPS test (in percentage) and threshold of the GIN test in the right ear
of patients with RTLE (r = − 0.13, p = 0.7) and control participants
(r = −0.36, p = 0.14) and left ear of the group with LTLE (r = −0.27,
p = 0.35), according to Pearson's correlation coefficient. The correlation
was observed to be significant in the left ear of control participants
(r = −0.49, p = 0.04) and patients with RTLE (r = −0.83, p = 0.002)
and the right ear of the group with LTLE (r = −0.6, p = 0.02).
The ear effect on the GIN and DPS tests was evaluated via paired t-
test in the three groups. There was no significant difference in mean
scores of the two tests between the right and left ears of each group
(p N 0.05) (Table 2).
4. Discussion
The present study was designed to evaluate auditory temporal
processing in patients with unilateral temporal lobe epilepsy utilizing
the GIN and DPS tests. The results showed that the threshold of GIN
test was higher and the mean percentage of correct responses in partic-
ipants with temporal lobe epilepsy was lower than those in control
participants. This difference was statistically significant; however,
there was no significant difference between participants with RTLE
and LTLE. The mean percentage of correct responses in the DPS test in
the group with LTLE was significantly lower than that in the group
with RTLE and control group, yet no significant difference was found
between the control group and the group with RTLE.
Fig. 2. Frequency of abnormal scores of duration pattern sequence test (percent) in the
right, left, both, and none of the ears of participants with right and left temporal lobe
epilepsy with cutoff criterion of 84.67%.
84 A.N. Lavasani et al. / Epilepsy & Behavior 60 (2016) 81–85
Fig. 3. Comparison of the mean of the threshold of the GIN test (ms) between participants
with RTLE and LTLE and controls.
Since left hemisphere disorders lead to a decrease in scores on DPS
test in both ears and this test was shown to be insensitive to right
hemisphere disorders, the DPS test may recognize the site of lesion.
But if there is a disorder in each of the hemispheres, the approximate
threshold of the GIN test will increase in one or both ears, and thus, it
cannot recognize the site of the lesion. Therefore, if the purpose is to de-
termine cortical disorders, the GIN test may be more appropriate than
the DPS test, and when the lesion site is under investigation, the DPS
test may be preferable. Overall, both tests are useful for the purpose of
diagnosis and management of auditory processing disorders.
A significant source of information for every auditory signal depends
on its temporal structure. Perhaps, more than any other type of informa-
tion, temporal information is critical in the discrimination and identifi-
cation of the signals. The phase-locked activity of neurons enables
listeners to discriminate periodic from aperiodic signals, which is im-
portant in the recognition of complex sounds [13]. Speech processing
disorders associated with temporal processing disorders indicate the
main role of temporal signs in the formulation and resolution of speech
signals [14].
The present study revealed that the GIN and DPS tests are processed
differently in the brain and can identify temporal lobe lesions. This find-
ing is compatible with that reported by Musiek et al. [5]. In a study con-
ducted by Zatorre and Belin [15], positron emission tomography (PET)
was employed to evaluate auditory cortex response to temporal and
spectral changes. The results revealed that the core areas of auditory
cortex of the two hemispheres respond to temporal changes while the
superoanterior areas of both temporal lobes respond to spectral chang-
es. It is reported that the responses to temporal events are found more
in the left hemisphere and responses to spectral events are observed
Fig. 4. Comparison of the mean of the correct responses of the duration pattern sequence
test (percent) between participants with RTLE and LTLE and controls.
more in the right hemisphere [15]. The data collected in our study are
compatible with these findings.
In agreement with our study, some studies have shown that left
temporal lobe disorders impair duration discrimination and temporal
perception [16]. Ehrlé et al. stated that auditory rapid and sequence
information processing depends on the integration of left temporal
lobe structures [8].
Also, Bamiou et al. showed that patients with left hemisphere disor-
der, compared with those with right hemisphere disorder, had lower
scores on the DPS test, which is consistent with the theory of cortex spe-
cialization for temporal processing [9]. The data obtained in the present
study are compatible with these findings, too.
Some parts of the right hemisphere may indirectly analyze percep-
tions of time and duration. Duration perception may take place by
some factors unrelated to temporal cognition. The right hemisphere is
specialized for intensity analysis of both verbal and nonverbal sounds,
and one probable hypothesis is that duration alterations of brief sounds
(b200 ms) may be perceived as intensity alterations [17,18]. Therefore,
in the present study, the existence of durations longer than 200 ms in
the DPS test and shorter than 200 ms in the GIN test could be one of
the reasons for abnormality in the GIN test, and normal data outcomes
in the DPS test in participants with RTLE could be attributed to left audi-
tory cortex specialization for temporal ordering.
The threshold of the GIN test, compared with the percentage of cor-
rect response index, has a better sensitivity and specificity [4,19]. In the
present study, the sensitivity of percentage of correct responses was
28% weaker than that for GIN threshold. In this study, during the GIN
test, some patients had abnormal scores in the right ear, some in the
left ear, and some in both ears. However, no significant difference and
ear advantage were observed between the mean scores of right and
left ears in the three groups. In the DPS test, too, most of the patients
with LTLE had abnormal scores in both ears, and there was no ear ad-
vantage in any one of the two tests. This finding was similar to those re-
ported in other studies [1,4,11,19,20].
Efron et al. reported that all their participants with temporal lobe
epilepsy who had undergone surgery had an increased threshold in
the contralateral ear to the lesion [7]. The reason for the difference in
findings reported in their study and those obtained in the present
study can be due to the different types of stimuli used (broadband in
the present study versus narrowband noise in the other study) and
the type of lesion (lobectomy versus epilepsy disease, respectively).
Also, it is worth mentioning that our participants did not have any sur-
gical intervention for their epilepsy.
Bilaterally impaired gap detection abilities have been reported
secondary to the electrical discharge (seizure) propagation between
the two hemispheres [11]. However, in the previous studies such as
Bamiou et al. [9], on patients with insular stroke and adjacent areas,
and Musiek and colleagues [4] on patients with central auditory ner-
vous system disorders (cortex and brainstem), bilateral deficit has
been observed. Musiek [4] reported that only 4 patients had
abnormal performance on contralateral ear to the lesion in the GIN
test. Likewise, in the present study, only two patients with RTLE
showed abnormal gap detection performance with the left ear. The
results of the present study are consistent with a previous study car-
ried out by Musiek [4], and the small differences between the two
studies can be related to the differences in locus and the extent of le-
sions and cutoff criteria. Since epilepsy leads to progressive functional
and structural damage of the temporal lobe and the longer duration
of the disease may be associated with a bilateral decrease in hippo-
campal volume, brain glucose metabolism, and memory performance
[2], the differences between the results of our study and those of
other studies can be related to differences in the duration of
epilepsy and, more importantly, to the severity of the disease, locus,
and the extent of lesions. Patients in the present study were pre-
scribed one or more antiepileptic drugs. Bearing in mind a previous
study by Han et al. [2], who had shown that antiepileptic drugs do
 A.N. Lavasani et al. / Epilepsy & Behavior 60 (2016) 81–85
not have any effects on the tests used in this study, we ignored the
effects of the drugs on the test results.
5. Conclusions
Based on the findings of the present study, patients with temporal
lobe epilepsy suffer from disorders in temporal processing perfor-
mances. In keeping with the left hemisphere being the specialized
hemisphere for temporal processing, these disorders in patients with
LTLE are more significant. As an evaluation tool, the GIN test is more ap-
propriate for determining whether there is an cortical disorder underly-
ing an auditory processing disorder whereas the DPS test is better for
identifying the lesion site. Both tests are therefore useful for the diagno-
sis and management of auditory processing disorders in patients with
temporal lobe epilepsy.
Conflict of interest statement
The authors declare no conflict of interests.
Acknowledgment
The authors wish to acknowledge the invaluable help of Dr. Frank
Musiek who provided consultation and assistance to this project. The
current research was supported by Tehran University of Medical
Sciences, grant no. p/26/d4/192.
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