Widespread slow oscillations support interictal epileptiform discharge networks in focal epilepsy

Hongyi Ye; Lingqi Ye; Lingli Hu; Yuyu Yang; Yi Ge; Ruotong Chen; Shan Wang; Bo Jin; Wenjie Ming; Zhongjin Wang; Sha Xu; Cenglin Xu; Yi Wang; Yao Ding; Junming Zhu; Meiping Ding; Zhong Chen; Shuang Wang; Cong Chen

Neurobiology of Disease (Feb 2024)

Widespread slow oscillations support interictal epileptiform discharge networks in focal epilepsy

Hongyi Ye,
Lingqi Ye,
Lingli Hu,
Yuyu Yang,
Yi Ge,
Ruotong Chen,
Shan Wang,
Bo Jin,
Wenjie Ming,
Zhongjin Wang,
Sha Xu,
Cenglin Xu,
Yi Wang,
Yao Ding,
Junming Zhu,
Meiping Ding,
Zhong Chen,
Shuang Wang,
Cong Chen

Affiliations

Hongyi Ye: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China; Nanhu Brain-computer Interface Institute, Hangzhou, China
Lingqi Ye: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Lingli Hu: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Yuyu Yang: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Yi Ge: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Ruotong Chen: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Shan Wang: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Bo Jin: Department of Neurology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China
Wenjie Ming: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Zhongjin Wang: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Sha Xu: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Cenglin Xu: Key Laboratory of Neuropharmacology and Translational Medicine of Zhejiang Province, School of Pharmaceutical Sciences, Zhejiang Chinese Medical University, Hangzhou, China
Yi Wang: Key Laboratory of Neuropharmacology and Translational Medicine of Zhejiang Province, School of Pharmaceutical Sciences, Zhejiang Chinese Medical University, Hangzhou, China
Yao Ding: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Junming Zhu: Department of Neurosurgery and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Meiping Ding: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China
Zhong Chen: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China; Key Laboratory of Neuropharmacology and Translational Medicine of Zhejiang Province, School of Pharmaceutical Sciences, Zhejiang Chinese Medical University, Hangzhou, China
Shuang Wang: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China; Nanhu Brain-computer Interface Institute, Hangzhou, China; Corresponding authors at: Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310009, China.
Cong Chen: Department of Neurology and Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China; Corresponding authors at: Epilepsy Center, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310009, China.

Journal volume & issue: Vol. 191
p. 106409

Abstract

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Interictal epileptiform discharges (IEDs) often co-occur across spatially-separated cortical regions, forming IED networks. However, the factors prompting IED propagation remain unelucidated. We hypothesized that slow oscillations (SOs) might facilitate IED propagation. Here, the amplitude and phase synchronization of SOs preceding propagating and non-propagating IEDs were compared in 22 patients with focal epilepsy undergoing intracranial electroencephalography (EEG) evaluation. Intracranial channels were categorized into the irritative zone (IZ) and normal zone (NOZ) regarding the presence of IEDs. During wakefulness, we found that pre-IED SOs within the IZ exhibited higher amplitudes for propagating IEDs than non-propagating IEDs (delta band: p = 0.001, theta band: p < 0.001). This increase in SOs was also concurrently observed in the NOZ (delta band: p = 0.04). Similarly, the inter-channel phase synchronization of SOs prior to propagating IEDs was higher than those preceding non-propagating IEDs in the IZ (delta band: p = 0.04). Through sliding window analysis, we observed that SOs preceding propagating IEDs progressively increased in amplitude and phase synchronization, while those preceding non-propagating IEDs remained relatively stable. Significant differences in amplitude occurred approximately 1150 ms before IEDs. During non-rapid eye movement (NREM) sleep, SOs on scalp recordings also showed higher amplitudes before intracranial propagating IEDs than before non-propagating IEDs (delta band: p = 0.006). Furthermore, the analysis of IED density around sleep SOs revealed that only high-amplitude sleep SOs demonstrated correlation with IED propagation. Overall, our study highlights that transient but widely distributed SOs are associated with IED propagation as well as generation in focal epilepsy during sleep and wakefulness, providing new insight into the EEG substrate supporting IED networks.

Published in Neurobiology of Disease

ISSN: 0969-9961 (Print); 1095-953X (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry
Website: https://www.journals.elsevier.com/neurobiology-of-disease

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