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The effect of interictal epileptic discharges and following spindles on motor sequence learning in epilepsy patients

PURPOSE: Interictal epileptic discharges (IEDs) are known to affect cognitive function in patients with epilepsy, but the mechanism has not been elucidated. Sleep spindles appearing in synchronization with IEDs were recently demonstrated to impair memory consolidation in rat, but this has not been i...

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Autores principales: Okadome, Toshiki, Yamaguchi, Takahiro, Mukaino, Takahiko, Sakata, Ayumi, Ogata, Katsuya, Shigeto, Hiroshi, Isobe, Noriko, Uehara, Taira
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9686303/
https://www.ncbi.nlm.nih.gov/pubmed/36438951
http://dx.doi.org/10.3389/fneur.2022.979333
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author Okadome, Toshiki
Yamaguchi, Takahiro
Mukaino, Takahiko
Sakata, Ayumi
Ogata, Katsuya
Shigeto, Hiroshi
Isobe, Noriko
Uehara, Taira
author_facet Okadome, Toshiki
Yamaguchi, Takahiro
Mukaino, Takahiko
Sakata, Ayumi
Ogata, Katsuya
Shigeto, Hiroshi
Isobe, Noriko
Uehara, Taira
author_sort Okadome, Toshiki
collection PubMed
description PURPOSE: Interictal epileptic discharges (IEDs) are known to affect cognitive function in patients with epilepsy, but the mechanism has not been elucidated. Sleep spindles appearing in synchronization with IEDs were recently demonstrated to impair memory consolidation in rat, but this has not been investigated in humans. On the other hand, the increase of sleep spindles at night after learning is positively correlated with amplified learning effects during sleep for motor sequence learning. In this study, we examined the effects of IEDs and IED-coupled spindles on motor sequence learning in patients with epilepsy, and clarified their pathological significance. MATERIALS AND METHODS: Patients undergoing long-term video-electroencephalography (LT-VEEG) at our hospital from June 2019 to November 2021 and age-matched healthy subjects were recruited. Motor sequence learning consisting of a finger-tapping task was performed before bedtime and the next morning, and the improvement rate of performance was defined as the sleep-dependent learning effect. We searched for factors associated with the changes in learning effect observed between the periods of when antiseizure medications (ASMs) were withdrawn for LT-VEEG and when they were returned to usual doses after LT-VEEG. RESULTS: Excluding six patients who had epileptic seizures at night after learning, nine patients and 11 healthy subjects were included in the study. In the patient group, there was no significant learning effect when ASMs were withdrawn. The changes in learning effect of the patient group during ASM withdrawal were not correlated with changes in sleep duration or IED density; however, they were significantly negatively correlated with changes in IED-coupled spindle density. CONCLUSION: We found that the increase of IED-coupled spindles correlated with the decrease of sleep-dependent learning effects of procedural memory. Pathological IED-coupled sleep spindles could hinder memory consolidation, that is dependent on physiological sleep spindles, resulting in cognitive dysfunction in patients with epilepsy.
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spelling pubmed-96863032022-11-25 The effect of interictal epileptic discharges and following spindles on motor sequence learning in epilepsy patients Okadome, Toshiki Yamaguchi, Takahiro Mukaino, Takahiko Sakata, Ayumi Ogata, Katsuya Shigeto, Hiroshi Isobe, Noriko Uehara, Taira Front Neurol Neurology PURPOSE: Interictal epileptic discharges (IEDs) are known to affect cognitive function in patients with epilepsy, but the mechanism has not been elucidated. Sleep spindles appearing in synchronization with IEDs were recently demonstrated to impair memory consolidation in rat, but this has not been investigated in humans. On the other hand, the increase of sleep spindles at night after learning is positively correlated with amplified learning effects during sleep for motor sequence learning. In this study, we examined the effects of IEDs and IED-coupled spindles on motor sequence learning in patients with epilepsy, and clarified their pathological significance. MATERIALS AND METHODS: Patients undergoing long-term video-electroencephalography (LT-VEEG) at our hospital from June 2019 to November 2021 and age-matched healthy subjects were recruited. Motor sequence learning consisting of a finger-tapping task was performed before bedtime and the next morning, and the improvement rate of performance was defined as the sleep-dependent learning effect. We searched for factors associated with the changes in learning effect observed between the periods of when antiseizure medications (ASMs) were withdrawn for LT-VEEG and when they were returned to usual doses after LT-VEEG. RESULTS: Excluding six patients who had epileptic seizures at night after learning, nine patients and 11 healthy subjects were included in the study. In the patient group, there was no significant learning effect when ASMs were withdrawn. The changes in learning effect of the patient group during ASM withdrawal were not correlated with changes in sleep duration or IED density; however, they were significantly negatively correlated with changes in IED-coupled spindle density. CONCLUSION: We found that the increase of IED-coupled spindles correlated with the decrease of sleep-dependent learning effects of procedural memory. Pathological IED-coupled sleep spindles could hinder memory consolidation, that is dependent on physiological sleep spindles, resulting in cognitive dysfunction in patients with epilepsy. Frontiers Media S.A. 2022-11-10 /pmc/articles/PMC9686303/ /pubmed/36438951 http://dx.doi.org/10.3389/fneur.2022.979333 Text en Copyright © 2022 Okadome, Yamaguchi, Mukaino, Sakata, Ogata, Shigeto, Isobe and Uehara. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Okadome, Toshiki
Yamaguchi, Takahiro
Mukaino, Takahiko
Sakata, Ayumi
Ogata, Katsuya
Shigeto, Hiroshi
Isobe, Noriko
Uehara, Taira
The effect of interictal epileptic discharges and following spindles on motor sequence learning in epilepsy patients
title The effect of interictal epileptic discharges and following spindles on motor sequence learning in epilepsy patients
title_full The effect of interictal epileptic discharges and following spindles on motor sequence learning in epilepsy patients
title_fullStr The effect of interictal epileptic discharges and following spindles on motor sequence learning in epilepsy patients
title_full_unstemmed The effect of interictal epileptic discharges and following spindles on motor sequence learning in epilepsy patients
title_short The effect of interictal epileptic discharges and following spindles on motor sequence learning in epilepsy patients
title_sort effect of interictal epileptic discharges and following spindles on motor sequence learning in epilepsy patients
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9686303/
https://www.ncbi.nlm.nih.gov/pubmed/36438951
http://dx.doi.org/10.3389/fneur.2022.979333
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