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Magnetic Resonance Imaging 31 (2013) 53 59

Altered hemispheric symmetry found in left-sided mesial temporal lobe

epilepsy with hippocampal sclerosis (MTLE/HS) but not found in
right-sided MTLE/HS
Jingjing Lua,, Wenjing Lib , Huiguang Heb,, Feng Fenga , Zhengyu Jina , Liwen Wuc
a
Department of Radiology, Peking Union Medical College Hospital, No. 1 Shuai Fu Yuan, Wang Fu Jing Avenue, Dong Cheng District, Beijing 100730, China
b
State Key Laboratory of Management and Control for Complex Systems, Institute of Automation, Chinese Academy of Sciences, Beijing 100190, China
c
Comprehensive Epilepsy Center, Peking Union Medical College Hospital, No. 1 Shuai Fu Yuan, Wang Fu Jing Avenue, Dong Cheng District,
Beijing 100730, China
Received 22 March 2012; revised 27 May 2012; accepted 25 June 2012

Abstract

Purpose: The purpose was to investigate the altered hemispheric asymmetry in patients with mesial temporal lobe epilepsy with unilateral
hippocampus sclerosis (MTLE/HS).
Materials and methods: This study examined the hemispheric asymmetry of regional gray matter (GM) and white matter (WM) volume
among a group of 13 patients with left-sided MTLE/HS, a group of 10 patients with right-sided MTLE/HS and a group of 21 age- and
gender- matched healthy controls by optimized voxel-based morphometry (VBM) based on magnetic resonance imaging.
Results: Compared to healthy controls, abnormal asymmetries were detected in the left-sided MTLE/HS patients. The left-sided MTLE/HS patients
had more GM asymmetries (LbR) in the temporal lobes, including the inferior temporal gyrus, middle temporal gyrus and parahippocampal gyrus.
There was significant asymmetry (LbR) in subcortical WM of the mesial temporal lobe in left-sided MTLE/HS patients. However, no significant
difference was detected in terms of GM and WM asymmetry between the group with right-sided MTLE/HS and normal controls.
Conclusion: We should approach hemispheric asymmetry in left- and right-sided MTLE/HS patients differently. The study also
demonstrates potential future use of VBM in detecting hemispheric asymmetries and lateralization of brain functions.
2013 Elsevier Inc. All rights reserved.

Keywords: Brain asymmetry; Magnetic resonance imaging (MRI); Voxel-based morphometry (VBM); Mesial temporal lobe epilepsy; Hippocampal sclerosis

1. Introduction related to a variety of reasons, including but not limited to

Hemispheric asymmetry in normal human brains has been
well established. Regional brain asymmetries were found either
through postmortem or through in vivo morphometric studies
[13]. Hemispheric asymmetries in brain anatomy may be
Corresponding authors. J. Lu is to be contacted at Department of
Radiology, Peking Union Medical College Hospital, Beijing 100730, China.
Tel.: +86 10 69155479; fax: +86 10 69155441. H. He, State Key Laboratory
of Management and Control for Complex Systems, Institute of Automation,
Chinese Academy of Sciences, Beijing 100190, China. Tel.: +86 10
62650799; fax: +86 10 62650799.
E-mail addresses: cjr.lujingjing@vip.163.com (J. Lu),
leafrain@163.com (W. Li), huiguang.he@ia.ac.cn (H. He),
cjr.fengfeng@vip.163 (F. Feng), jinzhengyupumch@gmail.com (Z. Jin),
wlw1946@yahoo.com.cn (L. Wu).
0730-725X/$ see front matter 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.mri.2012.06.030
hemisphere-specic functional specializations, genetics, devel-
opmental factors, gender and various pathologies [4]. Altered
brain asymmetry has been demonstrated in patients of
Alzheimer's disease [5] and dyslexia [6].
Mesial temporal lobe epilepsy (MTLE) is the most
common type of refractory focal epilepsy, and hippocampal
sclerosis (HS) is the most frequent underlying pathology [7].
Resection of the sclerotic hippocampus is associated with cure
or signicant reduction of seizure frequency in a majority of
patients [8,9]. The hippocampus is part of the limbic system,
which is composed of hippocampus, fornix, mammillary
bodies, anterior thalamus, cingulum and the parahippocam-
pus. The limbic system has a key role in memory, with
lateralization for verbal memory in the dominant hemisphere
(usually left) and nonverbal memory in the nondominant
hemisphere (usually right) [10].
54 J. Lu et al. / Magnetic Resonance Imaging 31 (2013) 5359

The seizures are not restricted to the mesial temporal lobe
ipsilateral to seizure onset, but involving the other brain areas
during the seizure spread [11,12]. There have been many
past structural and functional studies demonstrating exten-
sive involvement of gray matter (GM) and white matter
(WM) in MTLE patients. Changes in gray matter volume
(GMV) and white matter volume (WMV) were repeatedly
shown to extend to other brain regions surrounding the
hippocampus (the parahippocampal gyrus and the amygdala)
[13] and other more distant structures (several neocortical
regions, the thalamus, the striatal nuclei, the cerebellum and
the brainstem) [11,1417].
Since the introduction of voxel-based morphometry (VBM),
VBM has been applied to study the brain matter changes of
MTLE which shed much light on anatomical changes in the
disease [17]. A signicant asymmetrical distribution of
temporal lobe abnormalities preferentially to the ipsilateral
side of the seizure focus has been observed. There is also a much
more bilateral distribution of extratemporal lobe atrophy.
Despite a large number of VBM studies exploring the extensive
reduction of GMV and WMV in MTLE, less attention has been
paid to hemispheric structural asymmetry in these patients.
Because of the vulnerability to seizure attack and subsequent
functional reorganization, different patterns of volume reduc-
tion and hemispheric asymmetry may be present as related to the
side of seizure onset.
In this study, we hypothesized that the refractory MTLE
may alter the structural hemispheric asymmetry differently in
patients with left-sided MTLE/HS from those with right-
sided MTLE/HS as compared to the normal control. We have
optimized VBM to investigate asymmetrical abnormalities
of GMV and WMV in MTLE/HS patients.
and coronal slices)] by two independent physicians (radiol-
ogist and epileptologist) revealed unequivocal unilateral HS in
13 patients on the left side and in 10 patients on the right side.
All of our patients had MRI evidence of unilateral HS
concordant with the EEG lateralization of the epileptogenic
zone. None of the patients revealed other structural lesions on
MRI, and none of the patients had undergone any prior
neurosurgery. The patients were scanned on the same MR
machine with identical protocol. All patients had been seizure
free for 24 h before the MRI.
The age of onset and duration of epilepsy of each patient
were recorded. In the group with left-sided MTLE/HS,
the age of seizure onset ranged from 1 to 28 years (mean:
14.3 years, S.D.=8.7), and the duration of epilepsy ranged
from 3 to 33 years (mean: 13.1 years, S.D.=8.5). In the group
with right-sided MTLE/HS, the age of seizure onset ranged
from 7 to 39 years (mean: 22.6 years, S.D.=10.3), and the
duration of epilepsy ranged from 3 to 21 years (mean:
8.6 years, S.D.=6.1). There were three patients with history
of febrile seizures in the left-sided MTLE/HS group and the
right-sided MTLE/HS group, respectively. The 21 healthy
controls (11 female, 10 male) have no history of neuro-
logical and psychiatric diseases. The controls were scanned
on the same MR scanner with the same protocol as the
patients. The demographic and clinical data of the patients
and the controls are detailed in Table 1.
2.2. MRI data acquisition
High-resolution three-dimensional T1-weighted images
[3D spoiled gradient echo sequence (SPGR), Repetition
time/ Echo time/ Inversion time, 7/3.3/450 ms; 15 ip angle;
1.01.0-mm 2 in-plane resolution; slice thickness, 1.6 mm;

2. Materials and methods

Table 1
2.1. Subjects Demographic and clinical characteristics of left-sided and right-sided
MTLE/HS patients and healthy controls
Twenty-three patients with unilateral MTLE/HS (13 left-
Characteristic Left-sided Right-sided Healthy Analysis
sided MTLE/HS and 10 right-sided MTLE/HS patients) were MTLE/HS MTLE/HS controls P value
recruited from the Peking Union Medical College Hospital (n=13) (n=10) (n=21)
Comprehensive Epilepsy Center. Twenty-one healthy controls
Age at MRI scan ( years) 27.42.7 31.23.0 32.26.0 .247 a
were recruited from the community. All participants were Gender (male/female) 4/9 6/4 10/11 .364 b
right-handed. The committee of human research at the Peking Age at rst seizure 14.38.7 22.610.3 .063 c
Union Medical College Hospital approved the study, and onset (years)
written informed consent was obtained from each subject. Duration of disease (years) 13.18.5 8.66.1 .10 c
Seizure frequency 4.25.4 2.31.7 .613 c
All the patients fullled the diagnostic criteria for MLTE/
(per month)
HS. The diagnosis was made according to the International History of febrile 23.1% 30.0% .537 d
League Against Epilepsy (ILAE) criteria (Commission on seizures (%)
Classication and Terminology of ILAE, 1989). All patients History of CNS 7.7% 0 .565 d
underwent comprehensive clinical evaluation including infection (%)
History of head trauma (%) 7.7% 0 .565 d
history acquisition and electroencephalography (EEG) map-
ping. The identication of the epileptogenic focus was based Note: Data are shown as meanstandard deviation of the mean.
CNS=central nervous system.
on seizure semiology and prolonged ictal and interictal video- a
One-way analysis of variance.
EEG telemetry in all patients. Interpretation of the magnetic b
2 test.
resonance imaging (MRI) studies [MRI protocol included T1, c
MannWhitney test.
T2 and uid-attenuated inversion recovery sequences (axial c
Fisher's Exact Test.
 J. Lu et al. / Magnetic Resonance Imaging 31 (2013) 5359
Fig. 1. Summary of image processing using SPM5 software.
90100 transverse images] were obtained for all subjects
using a 3.0-T MR system (Signa, General Electric, Milwau-
kee, WI, USA) with an eight-channel phase array head coil.
2.3. Data processing
All T1-weighted images were rst skull-stripped using
the BET tool implemented in MRIcroN. Subsequent data
preprocessing was performed using Statistical Parametric
Mapping (SPM5) software package (http://www.l.ion.ucl.
ac.uk/spm, Wellcome Department of Cognitive Neurology,
London, UK, 2005) running on a Matlab 7.6 platform
(MathWorks, Natick, MA, USA). All the image processing
steps were summarized in Fig. 1.
The skull-stripped images were rst automatically
reoriented with the origin set close to the anterior
commissure and then segmented into GM, WM and
cerebrospinal uid (CSF) in native space using unied
segmentation [18]. The GM and WM were left-right ipped,
and diffeomorphic anatomical registration through exponen-
tiated lie algebra (DARTEL) algorithm was conducted to
align all the ipped and nonipped images [19]. All these
images from all the subjects were used to create the
symmetrical GM and WM templates, including six iterations
of average and registration. Then, the nonipped aligned
55
images were normalized to the symmetrical templates.
Modulation was then performed to correct for volume
changes. In addition, all the preprocessed images were then
afne-transformed from native space to the Montreal
Neurological Institute (MNI) space and then smoothed
using a 6-mm full-width at half-maximum isotropic
Gaussian kernel.
All the preprocessed GM and WM images were leftright
ipped, obtaining corresponding mirrored images. Asym-
metry index (AI) was dened as:
AIGMV = WMV = 2original imagemirrored image
= original imagemirrored image:
Positive values in the left hemisphere represented LNR
asymmetries, while the ones in the right hemisphere
represented LbR asymmetries.
2.4. Statistical analysis
First, one-sample t test was performed to investigate
asymmetry patterns within each group [Pb.05, multiple
comparisons were corrected by false discovery rate (FDR)].
Then, two-sample t test was used to detect abnormal
asymmetries in the MTLE/HS groups relative to normal
controls, respectively. Age, gender and total intracranial
56 J. Lu et al. / Magnetic Resonance Imaging 31 (2013) 5359
volume were further considered as covariates affecting the
brain asymmetries [20,21]. Statistically signicant threshold
was set at Pb.05, corrected for multiple comparisons by
FDR. We only reported the clusters with no less than
30 voxels.
3. Results
3.1. Basic characteristics of the patients and the
normal control
As shown in Table 1, no signicant differences in age and
gender distribution were observed among the left-sided
MTLE/HS patient group, the right-sided MTLE/HS patient
group and the normal control group. No statistically
signicant difference in age, gender, duration of disease
and seizure frequency was observed between the left- and
right-sided MTLE/HS groups.
3.2. VBM analysis
3.2.1. GM and WM asymmetry within each group
Analysis of brain asymmetry within each group revealed
an extensive and consistent pattern of GMV and WMV
asymmetries over the MTLE/HS groups and the normal
controls, as shown in Fig. 2. The positive signicant regions
were shown, of which the regions shown in the left
hemisphere were larger than the right hemisphere and vice
versa. The voxel-based analysis of GM differences between
the left and right hemispheres detected a number of GMV
asymmetries including the well-known right frontal and left
occipital petalias. [2,3].
3.2.2. Altered hemispheric asymmetry found in the left-sided
MTLE/HS patients but not in the right-sided patients as
compared to the normal control
Compared to the normal controls, the following abnormal
asymmetry patterns were detected in the left HS patients. In
terms of GM pattern, the left-sided MTLE/HS patients have
more LbR asymmetries in the temporal lobe than the right-
sided MTLE/HS group, including the inferior temporal
gyrus, middle temporal gyrus and parahippocampal gyrus
(shown in Fig. 3, detailed in Table 2). In terms of WM
asymmetry, there is signicant LbR asymmetry in the left-
sided MTLE/HS patients in the subcortical WM of mesial
temporal lobe compared with the normal controls (shown in
Fig. 3, detailed in Table 2).
In contrast to the left-sided MTLE/HS group, no
signicant abnormal GM and WM asymmetries were
found in the right-sided MTLE/HS patients when compared
to the normal controls.
4. Discussion
Studies in patients with MTLE/HS repeatedly demon-
strated structural and functional abnormalities extending
beyond hippocampus and mesial temporal lobe in recent
years. The reported involved brain regions include the
hippocampus and the parahippocampal gyrus [13], several
neocortical regions [16,22], the thalamus [23], the cerebel-
lum [15] and the brain stem [17].
VBM is a computational quantitative MRI analysis to
assess brain tissue composition on a voxel-by-voxel basis,
and it has been performed to explore GM and WM
asymmetries throughout the entire brain. In the present
study, the preprocessing steps of VBM have been improved
with the DARTEL registration method, which was initially
proposed by Ashburner et al. [19] and was then proved by
Yassa et al. [24]. This study aimed to use the optimized
VBM to detect the abnormal cerebral asymmetries in the
MTLE/HS patients. To our knowledge, this is the rst study
to use VBM to detect altered hemispheric asymmetry of
MTLE/HS which was relative to the side of seizure onset.
In the study, the left- and right-sided MTLE patients were
matched in age, gender, seizure frequency and duration of
illness. We observed altered LbR asymmetries in the left-
sided MTLE/HS patients relative to the normal controls,
while no altered hemispheric asymmetry was found in the
right-sided MTLE/HS patients. For the left-sided MTLE/HS
patients, the involved area of GM included the middle
temporal gyrus, inferior temporal gyrus and parahippocam-
pal gyrus, and the involved WM area was located in the
mesial temporal lobe. A number of possible presumptions
are as follows: First of all, recurrent epileptic discharge
causes bilateral tissue damage, but the damage is greater in
the hemisphere ipsilateral to seizures that originate in the left
mesial temporal lobe. Left hemisphere is the dominant side
in most cases [25], especially when all our subjects were
right-handed as in this study. Seizures originating in the
dominant hemisphere may cause more excitotoxic damage,
and also, brain tissue in the dominant hemisphere may be
more susceptible to the damage. A number of studies
investigated left- and right-sided MTLE as subgroups using
different approaches and reported different distribution
patterns of brain matter reduction between the left- and
right-sided MTLE patients. Riederer et al. [26] reported that
distinct neuronal network damage in MTLE was more
widespread in patients with left-sided seizure focus. In the
longitudinal MTLE study performed by Coan et al. [27],
progressive WM and GM atrophy was found in patients with
MTLE, which was more signicant in patients with left
MTLE compared with right MTLE. Additionally, more
signicant cognitive impairment [28,29] and atypical
language lateralization [30] in patients with left-sided
MTLE were described in recent studies. Since the involved
areas were associated with memory and cognitive functions
[28,31], we speculate that there would be more functional
and anatomical reorganization in the dominant hemisphere
than that in the nondominant hemisphere, which contributes
to the difference in asymmetry patterns between the two
subtypes as compared to the normal control. But in any case,
these assumptions are based on the knowledge from previous
 J. Lu et al. / Magnetic Resonance Imaging 31 (2013) 5359 57

Fig. 2. The signicantly asymmetrical regions in GM and WM of the normal controls, left-sided MTLE/HS patients and right-sided MTLE/HS patients. We
showed the positive signicant regions, of which the regions shown in the right hemisphere are larger than the left hemisphere and vice versa. Multiple
comparisons were corrected by FDR, Pb.05.
58 J. Lu et al. / Magnetic Resonance Imaging 31 (2013) 5359

Fig. 3. The signicantly altered asymmetrical regions in GM and WM of the left-sided MTLE/HS patients compared with normal controls. The positive
signicant regions in the right hemisphere are larger than those in the left hemisphere. Multiple comparisons were corrected by FDR, Pb.05.

studies and require additional studies for conrmation, for
example, correlation with cognitive decline and longitudinal
comparison of the two subgroups.
Interestingly, the study did not detect asymmetries in the
bilateral hippocampi but found asymmetry in the parahippo-
campal gyrus, which is part of the limbic system and mesial
temporal lobe as well. The possible reason is that there exists
the synchronized atrophy in the contralateral hippocampi
which is associated to the ipsilateral hippocampal atrophy. A
number of studies have found the volume reduction of the
bilateral hippocampi in unilateral temporal lobe epilepsy,
especially in the patients with hippocampal sclerosis [29,32].
Due to synchronized atrophy of the bilateral hippocampi and
subsequent subtle volume in-between difference, asymmet-
ric index in this region may fail to reach signicance.
Prior studies have attempted to relate structural asymme-
try in cortical regions [4,33] and WM [34,35] between the
hemispheres in regard to important functions such as
language lateralization. Ellmore et al. [35] studied the
possibility of using asymmetric index in the relative density
of WM pathways, using diffusion tensor imaging implicated
in language function to predict lateralization of language.
This preliminary study found that laterality indices computed
from asymmetry of high-anisotropy arcuate fasciculus
pathways correctly classied the majority of patients. Our
results may serve as an important basis whenever structural
asymmetry measured using VBM is used in lateralization of
functions; the fundamental differences between left- and
right-sided MTLE patients should be taken into account.
There are several limitations in the present study. First,
the sample size is relatively small, which might result in a
reduction of statistical power. Second, we are not able to
compare the whole disease progression and treatment of
these subgroups due to somewhat incomplete clinical data.
Further prospective study is warranted, which would be our
future work.

Table 2
Signicantly asymmetrical changes in GMV and WMV of the left-sided MTLE/HS patients compared with the normal controls
MNI coordinates P T score Cluster size (mm3) Anatomical regions BA Side
x (mm) y (mm) z (mm)
GM 57 2 36 b.001 8.63 456 Inferior temporal gyrus 20 R
60 12 14 .004 5.62 37 Middle temporal gyrus 21 R
29 14 23 .007 5.35 231 Parahippocampal gyrus 20 R
30 9 29 .01 5.04 45 Parahippocampal gyrus 36 R
WM 20 36 8 .019 5.98 101 Sublobal, temporal 27 R
Note: the T score is the highest value in the cluster which it belongs. Multiple comparisons were corrected by FDR. The clusters larger than 30 voxels were
reported.
BA=Brodmann's area; R=right hemisphere.
 J. Lu et al. / Magnetic Resonance Imaging 31 (2013) 5359
5. Conclusion
In conclusion, our ndings demonstrated different pat-
terns of hemispheric asymmetry of the left- and right-sided
MTLE/HS patients, which suggested that we should use
distinct ways of addressing the anatomical asymmetry of the
brain in patients with MTLE. The data also provided a basis
for the future employment of VBM in detecting hemispheric
asymmetries and lateralization of brain functions.
Acknowledgments
This work is supported by the National Natural Science
Foundation of China (No. 30600578, No. 60875079), the
Beijing Nova Plan (No.2007A102, No.2007A094), the
Foundation for Returned Scholars, Ministry of Human
Resources and Social Security of China, and Youth
Innovation Promotion Association, Chinese Academy of
Sciences. We thank Dr. Hui Jie Chen from Department of
Radiology, Massachusetts General Hospital for great help in
language editing and manuscript preparation.
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