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BMC Neurology

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01-12-2020 | Epilepsy | Research article

The morphological characteristics of hippocampus and thalamus in mesial temporal lobe epilepsy

Authors: Dongyan Wu, Feiyan Chang, Dantao Peng, Sheng Xie, Xiaoxuan Li, Wenjing Zheng

Published in: BMC Neurology | Issue 1/2020

Abstract

Background

Mesial temporal lobe epilepsy (MTLE) is the most common form of focal epilepsy, which is frequently characterized by hippocampal sclerosis (HS). Accumulating studies have suggested widespread cortico-cortical connections related to MTLE. The role of subcortical structures involved in general epilepsy has been extensively investigated, but it is still limited in MTLE. Our purpose was to determine the specific morphological correlation between sclerotic hippocampal and thalamic sub-regions, using quantitative analysis, in MTLE.

Methods

In this study, 23 MTLE patients with unilateral hippocampal sclerosis and 24 healthy controls were examined with three-dimensional T1 MRI. Volume quantitative analysis in the hippocampus and thalamus was conducted and group-related volumetric difference was assessed. Moreover, vertex analysis was further performed using automated software to delineate detailed morphological patterns of the hippocampus and thalamus. The correlation was used to examine whether there is a relationship between volume changes of two subcortical structures and clinical characteristics.

Results

The patients had a significant volume decrease in the sclerotic hippocampus (p < 0.001). Compared to controls, obvious atrophic patterns were observed in the bilateral hippocampus in MTLE (p < 0.05). Only small patches of shrinkage were noted in the bilateral thalamus (p < 0.05). Moreover, the volume change of the hippocampus had a significant positive correlation with that of the thalamus (P < 0.001). Intriguingly, volume changes of the hippocampus and thalamus were correlated with the duration of epilepsy (hippocampus: P = 0.024; thalamus: P = 0.022). However, only volume changes of thalamus possibly differentiated between two prognostic groups in patients (P = 0.026).

Conclusions

We demonstrated the morphological characteristics of the hippocampus and thalamus in MTLE, providing new insights into the interrelated mechanisms between the hippocampus and thalamus, which have potential clinical significance for refining neuromodulated targets.

Margerison JHCJ. Epilepsy and the temporal lobes: a clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain. 1966;89:499–30.CrossRef

Wieser HG, Epilepsy ICoNo. ILAE commission report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia. 2004;45:695–714; doi: https://doi.org/10.1111/j.0013-9580.2004.09004.x.

McDonald CR, Hagler DJ Jr, Ahmadi ME, Tecoma E, Iragui V, Gharapetian L, et al. Regional neocortical thinning in mesial temporal lobe epilepsy. Epilepsia. 2008;49:794–803. https://doi.org/10.1111/j.1528-1167.2008.01539.x.CrossRefPubMed

Bernasconi N, Duchesne S, Janke A, Lerch J, Collins DL, Bernasconi A. Whole-brain voxel-based statistical analysis of gray matter and white matter in temporal lobe epilepsy. Neuroimage. 2004;23:717–23. https://doi.org/10.1016/j.neuroimage.2004.06.015.CrossRefPubMed

Bonilha L, Rorden C, Castellano G, Pereira F, Rio PA, Cendes F, et al. Voxel-based morphometry reveals gray matter network atrophy in refractory medial temporal lobe epilepsy. Arch Neurol. 2004;61:1379–84. https://doi.org/10.1001/archneur.61.9.1379.CrossRefPubMed

Lin JJ, Salamon N, Lee AD, Dutton RA, Geaga JA, Hayashi KM, et al. Reduced neocortical thickness and complexity mapped in mesial temporal lobe epilepsy with hippocampal sclerosis. Cereb Cortex. 2007;17:2007–18. https://doi.org/10.1093/cercor/bhl109.CrossRefPubMed

Bernhardt BC, Bernasconi N, Kim H, Bernasconi A. Mapping thalamocortical network pathology in temporal lobe epilepsy. Neurology. 2012;78:129–36. https://doi.org/10.1212/WNL.0b013e31823efd0d.CrossRefPubMed

Keller SS, Roberts N. Voxel-based morphometry of temporal lobe epilepsy: an introduction and review of the literature. Epilepsia. 2008;49:741–57. https://doi.org/10.1111/j.1528-1167.2007.01485.x.CrossRefPubMed

Guye M, Regis J, Tamura M, Wendling F, McGonigal A, Chauvel P, et al. The role of corticothalamic coupling in human temporal lobe epilepsy. Brain. 2006;129:1917–28. https://doi.org/10.1093/brain/awl151.CrossRefPubMed

10.

Mueller SG, Laxer KD, Barakos J, Cheong I, Finlay D, Garcia P, et al. Involvement of the thalamocortical network in TLE with and without mesiotemporal sclerosis. Epilepsia. 2010;51:1436–45. https://doi.org/10.1111/j.1528-1167.2009.02413.x.CrossRefPubMed

11.

Keller SS, Richardson MP, O'Muircheartaigh J, Schoene-Bake JC, Elger C, Weber B. Morphometric MRI alterations and postoperative seizure control in refractory temporal lobe epilepsy. Hum Brain Mapp. 2015;36:1637–47. https://doi.org/10.1002/hbm.22722.CrossRefPubMedPubMedCentral

12.

Barron DS, Fox PM, Laird AR, Robinson JL, Fox PT. Thalamic medial dorsal nucleus atrophy in medial temporal lobe epilepsy: a VBM meta-analysis. Neuroimage Clin. 2012;2:25–32. https://doi.org/10.1016/j.nicl.2012.11.004.CrossRefPubMedPubMedCentral

13.

Gong G, Concha L, Beaulieu C, Gross DW. Thalamic diffusion and volumetry in temporal lobe epilepsy with and without mesial temporal sclerosis. Epilepsy Res. 2008;80:184–93. https://doi.org/10.1016/j.eplepsyres.2008.04.002.CrossRefPubMed

14.

Dreifuss S, Vingerhoets FJ, Lazeyras F, Andino SG, Spinelli L, Delavelle J, et al. Volumetric measurements of subcortical nuclei in patients with temporal lobe epilepsy. Neurology. 2001;57:1636–41.CrossRef

15.

Wong CH, Bleasel A, Wen L, Eberl S, Byth K, Fulham M, et al. The topography and significance of extratemporal hypometabolism in refractory mesial temporal lobe epilepsy examined by FDG-PET. Epilepsia. 2010;51:1365–73. https://doi.org/10.1111/j.1528-1167.2010.02552.x.CrossRefPubMed

16.

Yu T, Wang X, Li Y, Zhang G, Worrell G, Chauvel P, et al. High-frequency stimulation of anterior nucleus of thalamus desynchronizes epileptic network in humans. Brain. 2018;141:2631–43. https://doi.org/10.1093/brain/awy187.CrossRefPubMed

17.

Saini J, Bagepally BS, Sandhya M, Pasha SA, Yadav R, Thennarasu K, et al. Subcortical structures in progressive supranuclear palsy: vertex-based analysis. Eur J Neurol. 2013;20:493–501. https://doi.org/10.1111/j.1468-1331.2012.03884.x.CrossRefPubMed

18.

Zarei M, Patenaude B, Damoiseaux J, Morgese C, Smith S, Matthews PM, et al. Combining shape and connectivity analysis: an MRI study of thalamic degeneration in Alzheimer's disease. Neuroimage. 2010;49:1–8. https://doi.org/10.1016/j.neuroimage.2009.09.001.CrossRefPubMed

19.

Dinkelacker V, Valabregue R, Thivard L, Lehericy S, Baulac M, Samson S, et al. Hippocampal-thalamic wiring in medial temporal lobe epilepsy: enhanced connectivity per hippocampal voxel. Epilepsia. 2015;56:1217–26. https://doi.org/10.1111/epi.13051.CrossRefPubMed

20.

Pardoe HR, Pell GS, Abbott DF, Jackson GD. Hippocampal volume assessment in temporal lobe epilepsy: how good is automated segmentation? Epilepsia. 2009;50:2586–92. https://doi.org/10.1111/j.1528-1167.2009.02243.x.CrossRefPubMedPubMedCentral

21.

Thomann PA, Wustenberg T, Nolte HM, Menzel PB, Wolf RC, Essig M, et al. Hippocampal and entorhinal cortex volume decline in cognitively intact elderly. Psychiatry Res. 2013;211:31–6. https://doi.org/10.1016/j.pscychresns.2012.06.002.CrossRefPubMed

22.

Ramezani M, Johnsrude I, Rasoulian A, Bosma R, Tong R, Hollenstein T, et al. Temporal-lobe morphology differs between healthy adolescents and those with early-onset of depression. Neuroimage Clin. 2014;6:145–55. https://doi.org/10.1016/j.nicl.2014.08.007.CrossRefPubMedPubMedCentral

23.

Keller SS, O'Muircheartaigh J, Traynor C, Towgood K, Barker GJ, Richardson MP. Thalamotemporal impairment in temporal lobe epilepsy: a combined MRI analysis of structure, integrity, and connectivity. Epilepsia. 2014;55:306–15. https://doi.org/10.1111/epi.12520.CrossRefPubMedPubMedCentral

24.

Bernhardt BC, Bernasconi A, Liu M, Hong SJ, Caldairou B, Goubran M, et al. The spectrum of structural and functional imaging abnormalities in temporal lobe epilepsy. Ann Neurol. 2016;80:142–53. https://doi.org/10.1002/ana.24691.CrossRefPubMed

25.

Van der Werf YD, Witter MP, Uylings HB, Jolles J. Neuropsychology of infarctions in the thalamus: a review. Neuropsychologia. 2000;38:613–27.CrossRef

26.

Morgan VL, Conrad BN, Abou-Khalil B, Rogers BP, Kang H. Increasing structural atrophy and functional isolation of the temporal lobe with duration of disease in temporal lobe epilepsy. Epilepsy Res. 2015;110:171–8. https://doi.org/10.1016/j.eplepsyres.2014.12.006.CrossRefPubMed

27.

Haneef Z, Chiang S, Yeh HJ, Engel J Jr, Stern JM. Functional connectivity homogeneity correlates with duration of temporal lobe epilepsy. Epilepsy Behav. 2015;46:227–33. https://doi.org/10.1016/j.yebeh.2015.01.025.CrossRefPubMedPubMedCentral

28.

He X, Doucet GE, Pustina D, Sperling MR, Sharan AD, Tracy JI. Presurgical thalamic "hubness" predicts surgical outcome in temporal lobe epilepsy. Neurology. 2017;88:2285–93. https://doi.org/10.1212/WNL.0000000000004035.CrossRefPubMed

29.

Chassoux F, Artiges E, Semah F, Laurent A, Landre E, Turak B, et al. (18) F-FDG-PET patterns of surgical success and failure in mesial temporal lobe epilepsy. Neurology. 2017;88:1045–53. https://doi.org/10.1212/WNL.0000000000003714.CrossRefPubMed

30.

Lin JJ, Salamon N, Dutton RA, Lee AD, Geaga JA, Hayashi KM, et al. Three-dimensional preoperative maps of hippocampal atrophy predict surgical outcomes in temporal lobe epilepsy. Neurology. 2005;65:1094–7. https://doi.org/10.1212/01.wnl.0000179003.95838.71.CrossRefPubMedPubMedCentral

31.

Keller SS, Cresswell P, Denby C, Wieshmann U, Eldridge P, Baker G, et al. Persistent seizures following left temporal lobe surgery are associated with posterior and bilateral structural and functional brain abnormalities. Epilepsy Res. 2007;74:131–9. https://doi.org/10.1016/j.eplepsyres.2007.02.005.CrossRefPubMed

32.

Fisher R, Salanova V, Witt T, Worth R, Henry T, Gross R, et al. Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia. 2010;51:899–908. https://doi.org/10.1111/j.1528-1167.2010.02536.x.CrossRefPubMed

33.

Mottonen T, Katisko J, Haapasalo J, Tahtinen T, Kiekara T, Kahara V, et al. Defining the anterior nucleus of the thalamus (ANT) as a deep brain stimulation target in refractory epilepsy: delineation using 3 T MRI and intraoperative microelectrode recording. Neuroimage Clin. 2015;7:823–9. https://doi.org/10.1016/j.nicl.2015.03.001.CrossRefPubMedPubMedCentral

34.

Bouwens van der Vlis TAM, Schijns O, Schaper F, Hoogland G, Kubben P, Wagner L, et al. Deep brain stimulation of the anterior nucleus of the thalamus for drug-resistant epilepsy. Neurosurg Rev. 2019;42:287–96; doi: https://doi.org/10.1007/s10143-017-0941-x.

Title: The morphological characteristics of hippocampus and thalamus in mesial temporal lobe epilepsy
Authors: Dongyan Wu
Feiyan Chang
Dantao Peng
Sheng Xie
Xiaoxuan Li
Wenjing Zheng
Publication date: 01-12-2020
Publisher: BioMed Central
Keyword: Epilepsy
Published in: BMC Neurology / Issue 1/2020
Electronic ISSN: 1471-2377
DOI: https://doi.org/10.1186/s12883-020-01817-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The morphological characteristics of hippocampus and thalamus in mesial temporal lobe epilepsy

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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