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Amplitude synchronization of spontaneous activity of medial and lateral temporal gyri reveals altered thalamic connectivity in patients with temporal lobe epilepsy

In this study, we examined whether amplitude synchronization of medial (MTL) and lateral (LTL) temporal lobes can detect unique alterations in patients with MTL epilepsy (mTLE) with mesial temporal sclerosis (MTS). This was a retrospective study of preoperative resting-state fMRI (rsfMRI) data from...

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Autores principales: Sathe, Anish V., Kogan, Michael, Kang, KiChang, Miao, Jingya, Syed, Mashaal, Ailes, Isaiah, Matias, Caio M., Middleton, Devon, Mohamed, Feroze B., Faro, Scott, Tracy, Joseph, Sharan, Ashwini, Alizadeh, Mahdi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9626490/
https://www.ncbi.nlm.nih.gov/pubmed/36319701
http://dx.doi.org/10.1038/s41598-022-23297-4
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author Sathe, Anish V.
Kogan, Michael
Kang, KiChang
Miao, Jingya
Syed, Mashaal
Ailes, Isaiah
Matias, Caio M.
Middleton, Devon
Mohamed, Feroze B.
Faro, Scott
Tracy, Joseph
Sharan, Ashwini
Alizadeh, Mahdi
author_facet Sathe, Anish V.
Kogan, Michael
Kang, KiChang
Miao, Jingya
Syed, Mashaal
Ailes, Isaiah
Matias, Caio M.
Middleton, Devon
Mohamed, Feroze B.
Faro, Scott
Tracy, Joseph
Sharan, Ashwini
Alizadeh, Mahdi
author_sort Sathe, Anish V.
collection PubMed
description In this study, we examined whether amplitude synchronization of medial (MTL) and lateral (LTL) temporal lobes can detect unique alterations in patients with MTL epilepsy (mTLE) with mesial temporal sclerosis (MTS). This was a retrospective study of preoperative resting-state fMRI (rsfMRI) data from 31 patients with mTLE with MTS (age 23–69) and 16 controls (age 21–35). fMRI data were preprocessed based on a multistep preprocessing pipeline and registered to a standard space. Using each subject’s T1-weighted scan, the MTL and LTL were automatically segmented, manually revised and then fit to a standard space using a symmetric normalization registration algorithm. Dual regression analysis was applied on preprocessed rsfMRI data to detect amplitude synchronization of medial and lateral temporal segments with the rest of the brain. We calculated the overlapped volume ratio of synchronized voxels within specific target regions including the thalamus (total and bilateral). A general linear model was used with Bonferroni correction for covariates of epilepsy duration and age of patient at scan to statistically compare synchronization in patients with mTLE with MTS and controls, as well as with respect to whether patients remained seizure-free (SF) or not (NSF) after receiving epilepsy surgery. We found increased ipsilateral positive connectivity between the LTLs and the thalamus and contralateral negative connectivity between the MTLs and the thalamus in patients with mTLE with MTS compared to controls. We also found increased asymmetry of functional connectivity between temporal lobe subregions and the thalamus in patients with mTLE with MTS, with increased positive connectivity between the LTL and the lesional-side thalamus as well as increased negative connectivity between the MTL and the nonlesional-side thalamus. This asymmetry was also seen in NSF patients but was not seen in SF patients and controls. Amplitude synchronization was an effective method to detect functional connectivity alterations in patients with mTLE with MTS. Patients with mTLE with MTS overall showed increased temporal-thalamic connectivity. There was increased functional involvement of the thalamus in MTS, underscoring its role in seizure spread. Increased functional thalamic asymmetry patterns in NSF patients may have a potential role in prognosticating patient response to surgery. Elucidating regions with altered functional connectivity to temporal regions can improve understanding of the involvement of different regions in the disease to potentially target for intervention or use for prognosis for surgery. Future studies are needed to examine the effectiveness of using patient-specific abnormalities in patterns to predict surgical outcome.
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spelling pubmed-96264902022-11-03 Amplitude synchronization of spontaneous activity of medial and lateral temporal gyri reveals altered thalamic connectivity in patients with temporal lobe epilepsy Sathe, Anish V. Kogan, Michael Kang, KiChang Miao, Jingya Syed, Mashaal Ailes, Isaiah Matias, Caio M. Middleton, Devon Mohamed, Feroze B. Faro, Scott Tracy, Joseph Sharan, Ashwini Alizadeh, Mahdi Sci Rep Article In this study, we examined whether amplitude synchronization of medial (MTL) and lateral (LTL) temporal lobes can detect unique alterations in patients with MTL epilepsy (mTLE) with mesial temporal sclerosis (MTS). This was a retrospective study of preoperative resting-state fMRI (rsfMRI) data from 31 patients with mTLE with MTS (age 23–69) and 16 controls (age 21–35). fMRI data were preprocessed based on a multistep preprocessing pipeline and registered to a standard space. Using each subject’s T1-weighted scan, the MTL and LTL were automatically segmented, manually revised and then fit to a standard space using a symmetric normalization registration algorithm. Dual regression analysis was applied on preprocessed rsfMRI data to detect amplitude synchronization of medial and lateral temporal segments with the rest of the brain. We calculated the overlapped volume ratio of synchronized voxels within specific target regions including the thalamus (total and bilateral). A general linear model was used with Bonferroni correction for covariates of epilepsy duration and age of patient at scan to statistically compare synchronization in patients with mTLE with MTS and controls, as well as with respect to whether patients remained seizure-free (SF) or not (NSF) after receiving epilepsy surgery. We found increased ipsilateral positive connectivity between the LTLs and the thalamus and contralateral negative connectivity between the MTLs and the thalamus in patients with mTLE with MTS compared to controls. We also found increased asymmetry of functional connectivity between temporal lobe subregions and the thalamus in patients with mTLE with MTS, with increased positive connectivity between the LTL and the lesional-side thalamus as well as increased negative connectivity between the MTL and the nonlesional-side thalamus. This asymmetry was also seen in NSF patients but was not seen in SF patients and controls. Amplitude synchronization was an effective method to detect functional connectivity alterations in patients with mTLE with MTS. Patients with mTLE with MTS overall showed increased temporal-thalamic connectivity. There was increased functional involvement of the thalamus in MTS, underscoring its role in seizure spread. Increased functional thalamic asymmetry patterns in NSF patients may have a potential role in prognosticating patient response to surgery. Elucidating regions with altered functional connectivity to temporal regions can improve understanding of the involvement of different regions in the disease to potentially target for intervention or use for prognosis for surgery. Future studies are needed to examine the effectiveness of using patient-specific abnormalities in patterns to predict surgical outcome. Nature Publishing Group UK 2022-11-01 /pmc/articles/PMC9626490/ /pubmed/36319701 http://dx.doi.org/10.1038/s41598-022-23297-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Sathe, Anish V.
Kogan, Michael
Kang, KiChang
Miao, Jingya
Syed, Mashaal
Ailes, Isaiah
Matias, Caio M.
Middleton, Devon
Mohamed, Feroze B.
Faro, Scott
Tracy, Joseph
Sharan, Ashwini
Alizadeh, Mahdi
Amplitude synchronization of spontaneous activity of medial and lateral temporal gyri reveals altered thalamic connectivity in patients with temporal lobe epilepsy
title Amplitude synchronization of spontaneous activity of medial and lateral temporal gyri reveals altered thalamic connectivity in patients with temporal lobe epilepsy
title_full Amplitude synchronization of spontaneous activity of medial and lateral temporal gyri reveals altered thalamic connectivity in patients with temporal lobe epilepsy
title_fullStr Amplitude synchronization of spontaneous activity of medial and lateral temporal gyri reveals altered thalamic connectivity in patients with temporal lobe epilepsy
title_full_unstemmed Amplitude synchronization of spontaneous activity of medial and lateral temporal gyri reveals altered thalamic connectivity in patients with temporal lobe epilepsy
title_short Amplitude synchronization of spontaneous activity of medial and lateral temporal gyri reveals altered thalamic connectivity in patients with temporal lobe epilepsy
title_sort amplitude synchronization of spontaneous activity of medial and lateral temporal gyri reveals altered thalamic connectivity in patients with temporal lobe epilepsy
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9626490/
https://www.ncbi.nlm.nih.gov/pubmed/36319701
http://dx.doi.org/10.1038/s41598-022-23297-4
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