Abnormal Synchronization Between Cortical Delta Power and Ripples in Hippocampal Sclerosis

ABSTRACT Objective Discriminating between epileptogenic and physiological ripples in the hippocampus is important for identifying epileptogenic (EP) zones; however, distinguishing these ripples on the basis of their waveforms is difficult. We hypothesized that the nocturnal synchronization of hippoc...

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Main Authors: Takamitsu Iwata, Takufumi Yanagisawa, Ryohei Fukuma, Yuji Ikegaya, Satoru Oshino, Naoki Tani, Hui Ming Khoo, Hidenori Sugano, Yasushi Iimura, Hiroharu Suzuki, Haruhiko Kishima
Format: Article
Language:English
Published: Wiley 2025-05-01
Series:Annals of Clinical and Translational Neurology
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Online Access:https://doi.org/10.1002/acn3.70032
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author Takamitsu Iwata
Takufumi Yanagisawa
Ryohei Fukuma
Yuji Ikegaya
Satoru Oshino
Naoki Tani
Hui Ming Khoo
Hidenori Sugano
Yasushi Iimura
Hiroharu Suzuki
Haruhiko Kishima
author_facet Takamitsu Iwata
Takufumi Yanagisawa
Ryohei Fukuma
Yuji Ikegaya
Satoru Oshino
Naoki Tani
Hui Ming Khoo
Hidenori Sugano
Yasushi Iimura
Hiroharu Suzuki
Haruhiko Kishima
author_sort Takamitsu Iwata
collection DOAJ
description ABSTRACT Objective Discriminating between epileptogenic and physiological ripples in the hippocampus is important for identifying epileptogenic (EP) zones; however, distinguishing these ripples on the basis of their waveforms is difficult. We hypothesized that the nocturnal synchronization of hippocampal ripples and cortical delta power could be used to classify epileptogenic and physiological ripples in the hippocampus. Methods We enrolled 38 patients with electrodes implanted in the hippocampus or parahippocampal gyrus between April 2014 and March 2023 at our institution. We divided 11 patients (11 hippocampi) who were pathologically diagnosed with hippocampal sclerosis into the EP group and five patients (six hippocampi) with no epileptogenicity in the hippocampus into the nonepileptogenic (NE) group. Hippocampal ripples were detected using intracranial electroencephalography with hippocampal or parahippocampal electrodes. Cortical delta power (0.5–4 Hz) was assessed using cortical electrodes. The Pearson correlation coefficient between the ripple rates and cortical delta power (Corr‐RD) was calculated on the basis of the intracranial electroencephalographic signals recorded each night. Results Although hippocampal ripples were similar among the EP and NE groups based on their waveforms and frequency properties, the Corr‐RDs in the EP group (mean [standard deviation]: 0.20 [0.049]) were significantly lower than those in the NE group (0.67 [0.070]). On the basis of the minimum Corr‐RDs, the two groups were classified with 94.1% accuracy. Interpretation Our results demonstrate that the Corr‐RD is a biomarker of hippocampal epileptogenicity.
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spelling doaj-art-aa438b0093f44fe5aba5a10a94e7c6412025-08-20T02:25:34ZengWileyAnnals of Clinical and Translational Neurology2328-95032025-05-0112598699710.1002/acn3.70032Abnormal Synchronization Between Cortical Delta Power and Ripples in Hippocampal SclerosisTakamitsu Iwata0Takufumi Yanagisawa1Ryohei Fukuma2Yuji Ikegaya3Satoru Oshino4Naoki Tani5Hui Ming Khoo6Hidenori Sugano7Yasushi Iimura8Hiroharu Suzuki9Haruhiko Kishima10Department of Neurosurgery Graduate School of Medicine, Osaka University Suita Osaka JapanDepartment of Neurosurgery Graduate School of Medicine, Osaka University Suita Osaka JapanDepartment of Neurosurgery Graduate School of Medicine, Osaka University Suita Osaka JapanLaboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo Tokyo JapanDepartment of Neurosurgery Graduate School of Medicine, Osaka University Suita Osaka JapanDepartment of Neurosurgery Graduate School of Medicine, Osaka University Suita Osaka JapanDepartment of Neurosurgery Graduate School of Medicine, Osaka University Suita Osaka JapanDepartment of Neurosurgery Juntendo University Bunkyo‐ku Tokyo JapanDepartment of Neurosurgery Juntendo University Bunkyo‐ku Tokyo JapanDepartment of Neurosurgery Juntendo University Bunkyo‐ku Tokyo JapanDepartment of Neurosurgery Graduate School of Medicine, Osaka University Suita Osaka JapanABSTRACT Objective Discriminating between epileptogenic and physiological ripples in the hippocampus is important for identifying epileptogenic (EP) zones; however, distinguishing these ripples on the basis of their waveforms is difficult. We hypothesized that the nocturnal synchronization of hippocampal ripples and cortical delta power could be used to classify epileptogenic and physiological ripples in the hippocampus. Methods We enrolled 38 patients with electrodes implanted in the hippocampus or parahippocampal gyrus between April 2014 and March 2023 at our institution. We divided 11 patients (11 hippocampi) who were pathologically diagnosed with hippocampal sclerosis into the EP group and five patients (six hippocampi) with no epileptogenicity in the hippocampus into the nonepileptogenic (NE) group. Hippocampal ripples were detected using intracranial electroencephalography with hippocampal or parahippocampal electrodes. Cortical delta power (0.5–4 Hz) was assessed using cortical electrodes. The Pearson correlation coefficient between the ripple rates and cortical delta power (Corr‐RD) was calculated on the basis of the intracranial electroencephalographic signals recorded each night. Results Although hippocampal ripples were similar among the EP and NE groups based on their waveforms and frequency properties, the Corr‐RDs in the EP group (mean [standard deviation]: 0.20 [0.049]) were significantly lower than those in the NE group (0.67 [0.070]). On the basis of the minimum Corr‐RDs, the two groups were classified with 94.1% accuracy. Interpretation Our results demonstrate that the Corr‐RD is a biomarker of hippocampal epileptogenicity.https://doi.org/10.1002/acn3.70032delta band powerepileptogenicityhippocampuspathological ripplesharp‐wave ripple
spellingShingle Takamitsu Iwata
Takufumi Yanagisawa
Ryohei Fukuma
Yuji Ikegaya
Satoru Oshino
Naoki Tani
Hui Ming Khoo
Hidenori Sugano
Yasushi Iimura
Hiroharu Suzuki
Haruhiko Kishima
Abnormal Synchronization Between Cortical Delta Power and Ripples in Hippocampal Sclerosis
Annals of Clinical and Translational Neurology
delta band power
epileptogenicity
hippocampus
pathological ripple
sharp‐wave ripple
title Abnormal Synchronization Between Cortical Delta Power and Ripples in Hippocampal Sclerosis
title_full Abnormal Synchronization Between Cortical Delta Power and Ripples in Hippocampal Sclerosis
title_fullStr Abnormal Synchronization Between Cortical Delta Power and Ripples in Hippocampal Sclerosis
title_full_unstemmed Abnormal Synchronization Between Cortical Delta Power and Ripples in Hippocampal Sclerosis
title_short Abnormal Synchronization Between Cortical Delta Power and Ripples in Hippocampal Sclerosis
title_sort abnormal synchronization between cortical delta power and ripples in hippocampal sclerosis
topic delta band power
epileptogenicity
hippocampus
pathological ripple
sharp‐wave ripple
url https://doi.org/10.1002/acn3.70032
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