Synopsis
This study aimed
to observe dynamic functional organization changes of large-scale resting state
network (RSN) in MTLE and the patient who got
seizure free after surgical treatment. Subject specific RSNs of three groups
(healthy controls, presurgical group and posttreatment group) were extracted
using group-information guided independent component analysis. Then, we calculated
and compared the FC results between three groups, and we found FC altered
markedly before and after surgical treatment. In addition, there was no statistical
difference between posttreatment group and healthy
controls. Our results may provide valuable information for further
understanding of the pathophysiological mechanisms of intractable MTLE.
Introduction
Intractable
mesial temporal lobe epilepsy (MTLE) is the most common epilepsy and most of which
will receive surgical treatment. 1,
2 The concept of
the whole brain network disorder of MTLE has been accepted as a result of many
previous studies, 3-5 though its
frequent pathological findings were limited in mesial temporal lobe structure.
Many resting state functional MRI (rs-fMRI) studies have revealed resting-state
networks (RSNs) aberrant in MTLE, 6-8 however, few
studies have focused on dynamic changes of functional connectivity (FC) in RSNs
before and after surgical treatment. Furthermore, the mechanism of epilepsy
network is largely unknown now [9]. The aim of
this study was to investigate dynamic changes of FC within and between RSNs in
unilateral MTLE patients before and after surgical treatment. Method
Rs-fMRI
data were acquired from 7 unilateral intractable MTLE patients (3 males, 4 females;
age=26.86
± 7.89, range=16 - 34 years) and all this 7 patients received surgical
treatment. The control group included 18 healthy volunteers (10 males, 8 females;
age=26.61 ± 2.89, range=23 - 35 years). Patients were
divided into two groups: presurgical group and posttreatment group. The
diagnosis and lateralization of the seizure focus were determined by a
comprehensive evaluation in our epilepsy consultation
center. None of the patient had a mass lesion (tumor, cortical, or vascular malformations)
or traumatic brain injury. All patients were confirmed with hippocampal
sclerosis (HS) though imaging examination and/or postoperative pathology studies,
in addition, no patient got relapse after surgical treatment. Data were
collected on a MAGNETOM Trio Tim 3T MR scanner (Siemens Healthcare, Erlangen,
Germany) with a 32-channel head coil. The resting blood oxygen level-dependent
images were acquired with echo-planar imaging sequence with the following
parameters: TR/TE = 2000/30 ms, FOV = 220 mm × 220 mm, GRAPPA (PE) 2, slice
thickness = 3 mm, voxel size = 3.4 mm × 3.4mm × 3.0 mm, 35 slices, flip angle =
90°, and total acquisition time = 6:08 min and 180 volumes. T1-weighted images
were acquired using a 3D-MP-RAGE, providing isotropic voxels of 1mm × 1mm × 1
mm. The resting-state fMRI data of all subjects were preprocessing using Data
Processing Assistant for Resting-State fMRI (DPARSF). Subject specific RSNs for
three groups were estimated through group-information guided independent
component analysis (GIG-ICA). 10 One-way ANOVA was
used for analyzing intranetwork and internetwork FC differences among three
groups. p<0.05 was
considered statistically significant.Result
ECN (executive
control network), SMN (sensorimotor network) and DMN (default mode
network) were identified with significant FC changes using One-way ANOVA (p < 0.05, FDR corrected). Presurgical
MTLE patients showed significantly increased FC
between ECN and rSMN, as well as between DMN and SMN when compared
with healthy controls (p < 0.05,
FDR corrected) (Figure 1). The same extrinsic FCs were decreased significantly after
surgical treatment when compared with presurgical
group (p < 0.05, FDR corrected)
(Figure 1). Additionally, posttreatment patients exhibited no significantly
FC change within and between all RSNs when compared with healthy controls (p > 0.05, uncorrected). Compared with
healthy controls, only presurgical MTLE patients exhibited intranetwork FC in
the left ECN (p<0.05, GRF corrected)
(Figure 2) and intra-DMN FC between left supramarginal and right inferior parietal
lobule changes (p=0.0013, uncorrected)
(Figure 1).Discussion
Previous studies have revealed aberrant FC
within several RSNs in unilateral MTLE, such as DMN, AN and perceptual networks. 6, 11-13 Postoperation study also demonstrated dorsal
DMN impaired in TLE. 7 Our result of FC in DMN was agreement with
previous reports. However, they mainly focused on a single RSN which can’t represent
the entire epileptic network. To the best of our knowledge,
this is the first study that investigates functional organization
dynamic changes of whole brain large-scale
networks in unilateral intractable MTLE. We observed abnormal FC pattern between the ECN and the rSMN and
between the rSMN and the DMN in MTLE. Additionally, such abnormal
functional organization can be eliminated though successful surgical treatment. These findings not only confirmed
MTLE a brain network disorder again, but also further imply that the abnormal
internetwork FC of RSN may act as a potential biomarker of MTLE and provides
insights into biological mechanism of the disease.Conclusion
Our
study suggested that, the large-scale functional organization in presurgical
patients may complement the characteristics
of epileptic
network in another way.
Moreover, the dynamic changes of FC before and
after surgical treatment may help us to further understand physiological mechanism
of unilateral intractable MTLE. Acknowledgements
No acknowledgement found.References
1. Jobst B C, Cascino G D. Resective epilepsy
surgery for drug-resistant focal epilepsy: a review. JAMA, 2015, 313(3):
285-293.
2. Ryvlin P, Cross J H, Rheims S. Epilepsy
surgery in children and adults. Lancet Neurol, 2014, 13(11): 1114-1126.
3. Zhang Z, Liao W, Chen H, et al. Altered
functional-structural coupling of large-scale brain networks in idiopathic
generalized epilepsy. Brain, 2011, 134(Pt 10): 2912-2928.
4. Liu M, Bernhardt B C, Hong S J, et al. The
superficial white matter in temporal lobe epilepsy: a key link between
structural and functional network disruptions. Brain, 2016, 139(Pt 9):
2431-2440.
5. Voets N L, Beckmann C F, Cole D M, et al.
Structural substrates for resting network disruption in temporal lobe epilepsy.
Brain, 2012, 135(Pt 8): 2350-2357.
6. Zhang Z, Lu G, Zhong Y, et al. Impaired
perceptual networks in temporal lobe epilepsy revealed by resting fMRI. J.
Neurol., 2009, 256(10): 1705-1713.
7. Doucet G E, Skidmore C, Evans J, et al.
Temporal lobe epilepsy and surgery selectively alter the dorsal, not the
ventral, default-mode network. Front Neurol, 2014, 5: 23.
8. Cataldi M, Avoli M, De Villers-Sidani E.
Resting state networks in temporal lobe epilepsy. Epilepsia, 2013, 54(12):
2048-2059.
9. Paz J T, Huguenard J R. Microcircuits and
their interactions in epilepsy: is the focus out of focus? Nat. Neurosci.,
2015, 18(3): 351-359.
10. Du Y, Fan Y. Group information guided ICA
for fMRI data analysis. Neuroimage, 2013, 69:157-197.
11. Li W, Chen Z, Yan N, et al. Temporal Lobe
Epilepsy Alters Auditory-motor Integration For Voice Control. Sci Rep, 2016, 6:28909.
12. James G A, Tripathi S P, Ojemann J G, et al.
Diminished default mode network recruitment of the hippocampus and
parahippocampus in temporal lobe epilepsy. J Neurosurg, 2013, 119(2): 288-300.
13. Zhang Z, Lu G, Zhong Y, et al. Impaired
attention network in temporal lobe epilepsy: a resting FMRI study. Neurosci.
Lett., 2009, 458(3): 97-101.