Interictal suppression in patients with mesial temporal lobe epilepsy: A simultaneous PET/fMRI study

Previous stereotactic-electroencephalography (SEEG) results have suggested that seizure-onset zones (SOZs) could be suppressed by strengthened inward connectivity from the rest of the brain during interictal periods, which might explain why people with epilepsy did not have seizures continuously. Ho...

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Main Authors: Jie Hu, Liwei Sun, Kun Guo, Bixiao Cui, Chenyang Yao, Jingjuan Wang, Hui Ouyang, Xu Zhang, Chunlin Li, Jie Lu
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811925002101
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author Jie Hu
Liwei Sun
Kun Guo
Bixiao Cui
Chenyang Yao
Jingjuan Wang
Hui Ouyang
Xu Zhang
Chunlin Li
Jie Lu
author_facet Jie Hu
Liwei Sun
Kun Guo
Bixiao Cui
Chenyang Yao
Jingjuan Wang
Hui Ouyang
Xu Zhang
Chunlin Li
Jie Lu
author_sort Jie Hu
collection DOAJ
description Previous stereotactic-electroencephalography (SEEG) results have suggested that seizure-onset zones (SOZs) could be suppressed by strengthened inward connectivity from the rest of the brain during interictal periods, which might explain why people with epilepsy did not have seizures continuously. However, the limited coverage of SEEG contacts and allocation bias hindered a more comprehensive survey of interictal suppression at the whole-brain level. Previous studies also lacked a direct comparison between patients and healthy controls due to the invasive nature of SEEG. In the present study, we introduced metabolic connectivity mapping (MCM), a simultaneous FDG-PET/fMRI-based measure of effective connectivity, to evaluate the inward and outward connectivity of the SOZs in patients with mesial temporal lobe epilepsy (MTLE). Specifically, simultaneous FDG-PET/fMRI data was acquired from 23 patients with left MTLE, 24 patients with right MTLE, and 25 healthy controls. At the whole-brain level, there was significant increase of inward MCM connectivity to the SOZs, which mostly came from mesial-temporo-limbic, anterior and posterior midline regions of the default mode network (DMN) and subcortical nuclei. There was also significant decrease of outward MCM connectivity from the SOZs, which mainly projected to the regions within DMN. The increased net inward MCM to the SOZs, calculated by subtracting outward MCM from the inward MCM, was positively correlated with seizure frequency. Within DMN, MTLE patients showed decreased MCM from the SOZs to posterior cingulate cortex and right ventromedial prefrontal cortex and increased effective connectivity from posterior cingulate cortex to the SOZs. Based on the MCM patterns within DMN, we were able to classify the epileptic side of MTLE with an accuracy of 91.67 % (79.17 % for MRI-negative patients). Overall, our results provide whole-brain evidences for the interictal suppression hypothesis. We also found that the regions within DMN play a critical role in the suppression of SOZs. The pattern of such suppressive network might also serve as potential features for the localization of SOZs. Our neuroimaging results does not only provide a comprehensive understanding of interictal suppression at the whole-brain level, but also shed lights on a non-invasive and time-efficient way for SOZs localization.
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spelling doaj-art-9502482f0bf64f4cb9b1ecc182ac3d052025-08-20T03:53:51ZengElsevierNeuroImage1095-95722025-07-0131412120710.1016/j.neuroimage.2025.121207Interictal suppression in patients with mesial temporal lobe epilepsy: A simultaneous PET/fMRI studyJie Hu0Liwei Sun1Kun Guo2Bixiao Cui3Chenyang Yao4Jingjuan Wang5Hui Ouyang6Xu Zhang7Chunlin Li8Jie Lu9Department of Radiology and Nuclear Medicine, Xuanwu Hospital, Capital Medical University, Beijing, China; Beijing Key Laboratory of Magnetic Resonance Imaging and Brain Informatics, Beijing, ChinaSchool of Biomedical Engineering, Capital Medical University, Beijing 100069, China; Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, Beijing 100069, ChinaDepartment of Radiology and Nuclear Medicine, Xuanwu Hospital, Capital Medical University, Beijing, ChinaDepartment of Radiology and Nuclear Medicine, Xuanwu Hospital, Capital Medical University, Beijing, ChinaDepartment of Radiology and Nuclear Medicine, Xuanwu Hospital, Capital Medical University, Beijing, ChinaDepartment of Radiology and Nuclear Medicine, Xuanwu Hospital, Capital Medical University, Beijing, ChinaSchool of Biomedical Engineering, Capital Medical University, Beijing 100069, China; Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, Beijing 100069, ChinaSchool of Biomedical Engineering, Capital Medical University, Beijing 100069, China; Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, Beijing 100069, ChinaSchool of Biomedical Engineering, Capital Medical University, Beijing 100069, China; Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, Beijing 100069, China; Corresponding authors.Department of Radiology and Nuclear Medicine, Xuanwu Hospital, Capital Medical University, Beijing, China; Beijing Key Laboratory of Magnetic Resonance Imaging and Brain Informatics, Beijing, China; Corresponding authors.Previous stereotactic-electroencephalography (SEEG) results have suggested that seizure-onset zones (SOZs) could be suppressed by strengthened inward connectivity from the rest of the brain during interictal periods, which might explain why people with epilepsy did not have seizures continuously. However, the limited coverage of SEEG contacts and allocation bias hindered a more comprehensive survey of interictal suppression at the whole-brain level. Previous studies also lacked a direct comparison between patients and healthy controls due to the invasive nature of SEEG. In the present study, we introduced metabolic connectivity mapping (MCM), a simultaneous FDG-PET/fMRI-based measure of effective connectivity, to evaluate the inward and outward connectivity of the SOZs in patients with mesial temporal lobe epilepsy (MTLE). Specifically, simultaneous FDG-PET/fMRI data was acquired from 23 patients with left MTLE, 24 patients with right MTLE, and 25 healthy controls. At the whole-brain level, there was significant increase of inward MCM connectivity to the SOZs, which mostly came from mesial-temporo-limbic, anterior and posterior midline regions of the default mode network (DMN) and subcortical nuclei. There was also significant decrease of outward MCM connectivity from the SOZs, which mainly projected to the regions within DMN. The increased net inward MCM to the SOZs, calculated by subtracting outward MCM from the inward MCM, was positively correlated with seizure frequency. Within DMN, MTLE patients showed decreased MCM from the SOZs to posterior cingulate cortex and right ventromedial prefrontal cortex and increased effective connectivity from posterior cingulate cortex to the SOZs. Based on the MCM patterns within DMN, we were able to classify the epileptic side of MTLE with an accuracy of 91.67 % (79.17 % for MRI-negative patients). Overall, our results provide whole-brain evidences for the interictal suppression hypothesis. We also found that the regions within DMN play a critical role in the suppression of SOZs. The pattern of such suppressive network might also serve as potential features for the localization of SOZs. Our neuroimaging results does not only provide a comprehensive understanding of interictal suppression at the whole-brain level, but also shed lights on a non-invasive and time-efficient way for SOZs localization.http://www.sciencedirect.com/science/article/pii/S1053811925002101Mesial temporal lobe epilepsyPET/fMRIMetabolic connectivity mappingInterictal suppression
spellingShingle Jie Hu
Liwei Sun
Kun Guo
Bixiao Cui
Chenyang Yao
Jingjuan Wang
Hui Ouyang
Xu Zhang
Chunlin Li
Jie Lu
Interictal suppression in patients with mesial temporal lobe epilepsy: A simultaneous PET/fMRI study
NeuroImage
Mesial temporal lobe epilepsy
PET/fMRI
Metabolic connectivity mapping
Interictal suppression
title Interictal suppression in patients with mesial temporal lobe epilepsy: A simultaneous PET/fMRI study
title_full Interictal suppression in patients with mesial temporal lobe epilepsy: A simultaneous PET/fMRI study
title_fullStr Interictal suppression in patients with mesial temporal lobe epilepsy: A simultaneous PET/fMRI study
title_full_unstemmed Interictal suppression in patients with mesial temporal lobe epilepsy: A simultaneous PET/fMRI study
title_short Interictal suppression in patients with mesial temporal lobe epilepsy: A simultaneous PET/fMRI study
title_sort interictal suppression in patients with mesial temporal lobe epilepsy a simultaneous pet fmri study
topic Mesial temporal lobe epilepsy
PET/fMRI
Metabolic connectivity mapping
Interictal suppression
url http://www.sciencedirect.com/science/article/pii/S1053811925002101
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