Altered spontaneous brain activity in mesial temporal lobe epilepsy with unilateral hippocampal sclerosis: a meta-analysis of resting-state functional magnetic resonance imaging_West China Medical Journal

Authors：

ZHOU Baiwan , SUO Xueling , LI Wenbin , LI Lei , QIN Kun ,  LEI Du , GONG Qiyong

Huaxi MR Research Center, Department of Radiology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

LEI Du, Email: alien18@163.com

Keywords：

Mesial temporal lobe epilepsy; Hippocampal sclerosis; Resting-state functional magnetic resonance imaging; Amplitude of low-frequency fluctuations; Altered spontaneous brain activity

DOI：

10.7507/1002-0179.201904152

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To identify the most consistent and replicable characteristics of altered spontaneous brain activity in mesial temporal lobe epilepsy patients with unilateral hippocampal sclerosis (MTLE-HS). Methods A systematic literature search was performed in PubMed, Embase, The Cochrane Library, China National Knowledge Infrastructure, Wanfang, and CQVIP databases, to identify eligible whole-brain resting state functional magnetic resonance imaging studies that had measured differences in amplitude of low-frequency fluctuations or fractional amplitude of low-frequency fluctuations between patients with MTLE-HS and healthy controls from January 2000 to January 2019. After literature screening and data extraction, Anisotropic Effect-Size Signed Differential Mapping software was used for voxel based pooled meta-analysis. Results Nine datasets from six studies were finally included, which contained 207 MTLE-HS patients and 239 healthy controls. The results demonstrated that, compared with the healthy controls, the MTLE-HS patients showed increased spontaneous brain activity in right hippocampus and parahippocampal gyrus, right superior temporal gyrus, left cingulate gyrus, right fusiform gyrus, and right inferior temporal gyrus; while decreased spontaneous brain activity in left superior frontal gyrus, right angular gyrus, right middle frontal gyrus, left inferior parietal lobule, left precuneus, and right cerebellum (P<0.005, cluster extent≥10). Conclusion The current meta-analysis demonstrates that patients with MTLE-HS show increased spontaneous brain activity in lateral and mesial temporal regions and decreased spontaneous brain activity in default mode network, which preliminarily clarifies the characteristics of altered spontaneous brain activity in patients with MTLE-HS.

Citation： ZHOU Baiwan, SUO Xueling, LI Wenbin, LI Lei, QIN Kun, LEI Du, GONG Qiyong. Altered spontaneous brain activity in mesial temporal lobe epilepsy with unilateral hippocampal sclerosis: a meta-analysis of resting-state functional magnetic resonance imaging. West China Medical Journal, 2019, 34(10): 1154-1161. doi: 10.7507/1002-0179.201904152 Copy

1.	Engel J Jr. Mesial temporal lobe epilepsy: what have we learned?. Neuroscientist, 2001, 7(4): 340-352.
2.	Macdougall KW, Burneo JG, Mclachlan RS. Outcome of epilepsy surgery in patients investigated with subdural electrodes. Epilepsy Res, 2009, 85(2/3): 235-242.
3.	Elsharkawy AE, Alabbasi AH, Pannek H, et al. Long-term outcome after temporal lobe epilepsy surgery in 434 consecutive adult patients. J Neurosurg, 2009, 110(6): 1135-1146.
4.	Varoglu AO, Saygi S, Acemoglu H, et al. Prognosis of patients with mesial temporal lobe epilepsy due to hippocampal sclerosis. Epilepsy Res, 2009, 85(2/3): 206-211.
5.	Zang YF, He Y, Zhu CZ, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev, 2007, 29(2): 83-91.
6.	Zhang Z, Lu G, Zhong Y, et al. fMRI study of mesial temporal lobe epilepsy using amplitude of low-frequency fluctuation analysis. Hum Brain Mapp, 2010, 31(12): 1851-1861.
7.	Ji GJ, Zhang Z, Zhang H, et al. Disrupted causal connectivity in mesial temporal lobe epilepsy. PLoS One, 2013, 8(5): e63183.
8.	Wei W, Zhang ZQ, Xu Q, et al. More severe extratemporal damages in mesial temporal lobe epilepsy with hippocampal sclerosis than that with other lesions a multimodality MRI study. Medicine (Baltimore), 2016, 95(10): e3020.
9.	赵博峰, 纪东旭, 杨卫东, 等. 颞叶内侧癫痫患者自发脑活动的同步性与低频振幅: 静息态功能磁共振成像研究. 中国医学影像学杂志, 2014, 22(12): 885-890.
10.	鹿丽, 陈自谦, 杨朋范, 等. 右侧颞叶癫痫发作间期静息态脑功能磁共振成像研究. 功能与分子医学影像学(电子版), 2015, 4(2): 651-656.
11.	张浩. 基于fMRI与EEG对癫痫病的基础研究. 南京: 南京航空航天大学, 2010.
12.	Radua J, Mataix-Cols D, Phillips ML, et al. A new meta-analytic method for neuroimaging studies that combines reported peak coordinates and statistical parametric maps. Eur Psychiatry, 2012, 27(8): 605-611.
13.	Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia, 1989, 30(4): 389-399.
14.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
15.	Burwell RD. The parahippocampal region: corticocortical connectivity. Ann N Y Acad Sci, 2000, 911(1): 25-42.
16.	Opitz B. Memory function and the hippocampus. Front Neurol Neurosci, 2014, 34: 51-59.
17.	Alessio A, Damasceno BP, Camargo CH, et al. Differences in memory performance and other clinical characteristics in patients with mesial temporal lobe epilepsy with and without hippocampal atrophy. Epilepsy Behav, 2004, 5(1): 22-27.
18.	Chen SH, Wu XT, Lui S, et al. Resting-state fMRI study of treatment-naive temporal lobe epilepsy patients with depressive symptoms. Neuroimage, 2012, 60(1): 299-304.
19.	Morgan VL, Gore JC, Abou-Khalil B. Functional epileptic network in left mesial temporal lobe epilepsy detected using resting fMRI. Epilepsy Res, 2010, 88(2/3): 168-178.
20.	Coan AC, Campos BM, Beltramini GC, et al. Distinct functional and structural MRI abnormalities in mesial temporal lobe epilepsy with and without hippocampal sclerosis. Epilepsia, 2014, 55(8): 1187-1196.
21.	Pittau F, Grova C, Moeller F, et al. Patterns of altered functional connectivity in mesial temporal lobe epilepsy. Epilepsia, 2012, 53(6): 1013-1023.
22.	Zheng LY, Bin G, Zeng HW, et al. Meta-analysis of voxel-based morphometry studies of gray matter abnormalities in patients with mesial temporal lobe epilepsy and unilateral hippocampal sclerosis. Brain Imaging Behav, 2018, 12(5): 1497-1503.
23.	Zeng HW, Pizarro R, Nair VA, et al. Alterations in regional homogeneity of resting-state brain activity in mesial temporal lobe epilepsy. Epilepsia, 2013, 54(4): 658-666.
24.	Berkovic SF, Andermann F, Olivier A, et al. Hippocampal sclerosis in temporal-lobe epilepsy demonstrated by magnetic-resonance-imaging. Ann Neurol, 1991, 29(2): 175-182.
25.	Menon V. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn Sci, 2011, 15(10): 483-506.
26.	Shulman GL, Fiez JA, Corbetta M, et al. Common blood flow changes across visual tasks. 2. Decreases in cerebral cortex. J Cognitive Neurosci, 1997, 9(5): 648-663.
27.	Zhang C, Yang HY, Qin W, et al. Characteristics of resting-state functional connectivity in intractable unilateral temporal lobe epilepsy patients with impaired executive control function. Front Hum Neurosci, 2017, 11: 609.
28.	de Campos BM, Coan AC, Yasuda CL, et al. Large-scale brain networks are distinctly affected in right and left mesial temporal lobe epilepsy. Hum Brain Mapp, 2016, 37(9): 3137-3152.
29.	Haneef Z, Lenartowicz A, Yeh HJ, et al. Network analysis of the default mode network using functional connectivity MRI in temporal lobe epilepsy. Jove-J Vis Exp, 2014, 90: e51442.
30.	Liao W, Zhang Z, Pan Z, et al. Default mode network abnormalities in mesial temporal lobe epilepsy: a study combining fMRI and DTI. Hum Brain Mapp, 2011, 32(6): 883-895.
31.	Ortega GJ, Menendez de la Prida L, Sola RG, et al. Synchronization clusters of interictal activity in the lateral temporal cortex of epileptic patients: intraoperative electrocorticographic analysis. Epilepsia, 2008, 49(2): 269-280.

1. Engel J Jr. Mesial temporal lobe epilepsy: what have we learned?. Neuroscientist, 2001, 7(4): 340-352.
2. Macdougall KW, Burneo JG, Mclachlan RS. Outcome of epilepsy surgery in patients investigated with subdural electrodes. Epilepsy Res, 2009, 85(2/3): 235-242.
3. Elsharkawy AE, Alabbasi AH, Pannek H, et al. Long-term outcome after temporal lobe epilepsy surgery in 434 consecutive adult patients. J Neurosurg, 2009, 110(6): 1135-1146.
4. Varoglu AO, Saygi S, Acemoglu H, et al. Prognosis of patients with mesial temporal lobe epilepsy due to hippocampal sclerosis. Epilepsy Res, 2009, 85(2/3): 206-211.
5. Zang YF, He Y, Zhu CZ, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev, 2007, 29(2): 83-91.
6. Zhang Z, Lu G, Zhong Y, et al. fMRI study of mesial temporal lobe epilepsy using amplitude of low-frequency fluctuation analysis. Hum Brain Mapp, 2010, 31(12): 1851-1861.
7. Ji GJ, Zhang Z, Zhang H, et al. Disrupted causal connectivity in mesial temporal lobe epilepsy. PLoS One, 2013, 8(5): e63183.
8. Wei W, Zhang ZQ, Xu Q, et al. More severe extratemporal damages in mesial temporal lobe epilepsy with hippocampal sclerosis than that with other lesions a multimodality MRI study. Medicine (Baltimore), 2016, 95(10): e3020.
9. 赵博峰, 纪东旭, 杨卫东, 等. 颞叶内侧癫痫患者自发脑活动的同步性与低频振幅: 静息态功能磁共振成像研究. 中国医学影像学杂志, 2014, 22(12): 885-890.
10. 鹿丽, 陈自谦, 杨朋范, 等. 右侧颞叶癫痫发作间期静息态脑功能磁共振成像研究. 功能与分子医学影像学(电子版), 2015, 4(2): 651-656.
11. 张浩. 基于fMRI与EEG对癫痫病的基础研究. 南京: 南京航空航天大学, 2010.
12. Radua J, Mataix-Cols D, Phillips ML, et al. A new meta-analytic method for neuroimaging studies that combines reported peak coordinates and statistical parametric maps. Eur Psychiatry, 2012, 27(8): 605-611.
13. Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia, 1989, 30(4): 389-399.
14. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
15. Burwell RD. The parahippocampal region: corticocortical connectivity. Ann N Y Acad Sci, 2000, 911(1): 25-42.
16. Opitz B. Memory function and the hippocampus. Front Neurol Neurosci, 2014, 34: 51-59.
17. Alessio A, Damasceno BP, Camargo CH, et al. Differences in memory performance and other clinical characteristics in patients with mesial temporal lobe epilepsy with and without hippocampal atrophy. Epilepsy Behav, 2004, 5(1): 22-27.
18. Chen SH, Wu XT, Lui S, et al. Resting-state fMRI study of treatment-naive temporal lobe epilepsy patients with depressive symptoms. Neuroimage, 2012, 60(1): 299-304.
19. Morgan VL, Gore JC, Abou-Khalil B. Functional epileptic network in left mesial temporal lobe epilepsy detected using resting fMRI. Epilepsy Res, 2010, 88(2/3): 168-178.
20. Coan AC, Campos BM, Beltramini GC, et al. Distinct functional and structural MRI abnormalities in mesial temporal lobe epilepsy with and without hippocampal sclerosis. Epilepsia, 2014, 55(8): 1187-1196.
21. Pittau F, Grova C, Moeller F, et al. Patterns of altered functional connectivity in mesial temporal lobe epilepsy. Epilepsia, 2012, 53(6): 1013-1023.
22. Zheng LY, Bin G, Zeng HW, et al. Meta-analysis of voxel-based morphometry studies of gray matter abnormalities in patients with mesial temporal lobe epilepsy and unilateral hippocampal sclerosis. Brain Imaging Behav, 2018, 12(5): 1497-1503.
23. Zeng HW, Pizarro R, Nair VA, et al. Alterations in regional homogeneity of resting-state brain activity in mesial temporal lobe epilepsy. Epilepsia, 2013, 54(4): 658-666.
24. Berkovic SF, Andermann F, Olivier A, et al. Hippocampal sclerosis in temporal-lobe epilepsy demonstrated by magnetic-resonance-imaging. Ann Neurol, 1991, 29(2): 175-182.
25. Menon V. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn Sci, 2011, 15(10): 483-506.
26. Shulman GL, Fiez JA, Corbetta M, et al. Common blood flow changes across visual tasks. 2. Decreases in cerebral cortex. J Cognitive Neurosci, 1997, 9(5): 648-663.
27. Zhang C, Yang HY, Qin W, et al. Characteristics of resting-state functional connectivity in intractable unilateral temporal lobe epilepsy patients with impaired executive control function. Front Hum Neurosci, 2017, 11: 609.
28. de Campos BM, Coan AC, Yasuda CL, et al. Large-scale brain networks are distinctly affected in right and left mesial temporal lobe epilepsy. Hum Brain Mapp, 2016, 37(9): 3137-3152.
29. Haneef Z, Lenartowicz A, Yeh HJ, et al. Network analysis of the default mode network using functional connectivity MRI in temporal lobe epilepsy. Jove-J Vis Exp, 2014, 90: e51442.
30. Liao W, Zhang Z, Pan Z, et al. Default mode network abnormalities in mesial temporal lobe epilepsy: a study combining fMRI and DTI. Hum Brain Mapp, 2011, 32(6): 883-895.
31. Ortega GJ, Menendez de la Prida L, Sola RG, et al. Synchronization clusters of interictal activity in the lateral temporal cortex of epileptic patients: intraoperative electrocorticographic analysis. Epilepsia, 2008, 49(2): 269-280.

Previous Article
Effect of ELOVL6 gene on large artery atherosclerosis stroke risk in Han Chinese population in Chengdu
Next Article
Risk factors of care ability among main caregivers of stroke patients

West China Medical Journal

Altered spontaneous brain activity in mesial temporal lobe epilepsy with unilateral hippocampal sclerosis: a meta-analysis of resting-state functional magnetic resonance imaging

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content