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Rapid eye movement sleep affects interictal epileptic activity differently in mesiotemporal and neocortical areas
Objective Rapid eye movement (REM) sleep reduces the rate and extent of interictal epileptiform discharges (IEDs). Breakthrough epileptic activity during REM sleep is therefore thought to best localize the seizure onset zone (SOZ). We utilized polysomnography combined with direct cortical recordings...
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| Published in: | Epilepsia (Copenhagen) 2023-11, Vol.64 (11), p.3036-3048 |
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| cites | cdi_FETCH-LOGICAL-c3653-4e6b06e81b5d5208c73a0703cbaa5120a5eeb905c4be49d3d1df9e9b06462e5f3 |
| container_end_page | 3048 |
| container_issue | 11 |
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| container_title | Epilepsia (Copenhagen) |
| container_volume | 64 |
| creator | Ho, Alyssa Hannan, Sana Thomas, John Avigdor, Tamir Abdallah, Chifaou Dubeau, François Gotman, Jean Frauscher, Birgit |
| description | Objective
Rapid eye movement (REM) sleep reduces the rate and extent of interictal epileptiform discharges (IEDs). Breakthrough epileptic activity during REM sleep is therefore thought to best localize the seizure onset zone (SOZ). We utilized polysomnography combined with direct cortical recordings to investigate the influences of anatomical locations and the time of night on the suppressive effect of REM sleep on IEDs.
Methods
Forty consecutive patients with drug‐resistant focal epilepsy underwent combined polysomnography and stereo‐electroencephalography during presurgical evaluation. Ten‐minute interictal epochs were selected 2 h prior to sleep onset (wakefulness), and from the first and second half of the night during non‐REM (NREM) sleep and REM sleep. IEDs were detected automatically across all channels. Anatomic localization, time of night, and channel type (within or outside the SOZ) were tested as modulating factors.
Results
Relative to wakefulness, there was a suppression of IEDs by REM sleep in neocortical regions (median = −27.6%), whereas mesiotemporal regions showed an increase in IEDs (19.1%, p = .01, d = .39). This effect was reversed when comparing the regional suppression of IEDs by REM sleep relative to NREM sleep (−35.1% in neocortical, −58.7% in mesiotemporal, p |
| doi_str_mv | 10.1111/epi.17763 |
| format | article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2865784026</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2886338619</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3653-4e6b06e81b5d5208c73a0703cbaa5120a5eeb905c4be49d3d1df9e9b06462e5f3</originalsourceid><addsrcrecordid>eNp10E9LwzAYBvAgCs7pwW8Q8KKHbknTJO1RxtTBQBE9hzR9Cxn9tySb9NubWU-CubwEfs_Ly4PQLSULGt8SBrugUgp2hmaUp3lCqZDnaEYIZUnBc3KJrrzfEUKkkGyG9u96sBWGEXDbH6GFLmDfAAxY1zWY4LHtAjhrgm5wXN7AEKzB2gR7tGHElY3MxVQzRolb8LYP0A69i153Fe6gN72LmdPfgfbX6KLWjYeb3zlHn0_rj9VLsn193qwet4lhgrMkA1ESATktecVTkhvJNJGEmVJrTlOiOUBZEG6yErKiYhWt6gKKmMlECrxmc3Q_7R1cvz-AD6q13kDT6HjSwas0F1zmGUlFpHd_6K4_uC5eF1UuGMsFLaJ6mJRxvfcOajU422o3KkrUqXwV-1E_5Ue7nOxXbGz8H6r122ZKfANBD4fz</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2886338619</pqid></control><display><type>article</type><title>Rapid eye movement sleep affects interictal epileptic activity differently in mesiotemporal and neocortical areas</title><source>Wiley Online Library</source><creator>Ho, Alyssa ; Hannan, Sana ; Thomas, John ; Avigdor, Tamir ; Abdallah, Chifaou ; Dubeau, François ; Gotman, Jean ; Frauscher, Birgit</creator><creatorcontrib>Ho, Alyssa ; Hannan, Sana ; Thomas, John ; Avigdor, Tamir ; Abdallah, Chifaou ; Dubeau, François ; Gotman, Jean ; Frauscher, Birgit</creatorcontrib><description>Objective
Rapid eye movement (REM) sleep reduces the rate and extent of interictal epileptiform discharges (IEDs). Breakthrough epileptic activity during REM sleep is therefore thought to best localize the seizure onset zone (SOZ). We utilized polysomnography combined with direct cortical recordings to investigate the influences of anatomical locations and the time of night on the suppressive effect of REM sleep on IEDs.
Methods
Forty consecutive patients with drug‐resistant focal epilepsy underwent combined polysomnography and stereo‐electroencephalography during presurgical evaluation. Ten‐minute interictal epochs were selected 2 h prior to sleep onset (wakefulness), and from the first and second half of the night during non‐REM (NREM) sleep and REM sleep. IEDs were detected automatically across all channels. Anatomic localization, time of night, and channel type (within or outside the SOZ) were tested as modulating factors.
Results
Relative to wakefulness, there was a suppression of IEDs by REM sleep in neocortical regions (median = −27.6%), whereas mesiotemporal regions showed an increase in IEDs (19.1%, p = .01, d = .39). This effect was reversed when comparing the regional suppression of IEDs by REM sleep relative to NREM sleep (−35.1% in neocortical, −58.7% in mesiotemporal, p < .001, d = .39). Across all patients, no clinically relevant novel IED regions were observed in REM sleep versus NREM or wakefulness based on our predetermined thresholds (4 IEDs/min in REM, 0 IEDs/min in NREM and wakefulness). Finally, there was a reduction in IEDs in late (NREM: 1.08/min, REM: .61/min) compared to early sleep (NREM: 1.22/min, REM: .69/min) for both NREM (p < .001, d = .21) and REM (p = .04, d = .14).
Significance
Our results demonstrate a spatiotemporal effect of IED suppression by REM sleep relative to wakefulness in neocortical but not mesiotemporal regions, and in late versus early sleep. This suggests the importance of considering sleep stage interactions and the potential influences of anatomical locations when using IEDs to define the epileptic focus.</description><identifier>ISSN: 0013-9580</identifier><identifier>EISSN: 1528-1167</identifier><identifier>DOI: 10.1111/epi.17763</identifier><language>eng</language><publisher>Hoboken: Wiley Subscription Services, Inc</publisher><subject>EEG ; Epilepsy ; Eye movements ; Firing pattern ; interictal activity ; Localization ; NREM sleep ; rapid eye movement ; REM sleep ; Seizures ; Sleep ; Sleep and wakefulness ; stereo‐electroencephalography</subject><ispartof>Epilepsia (Copenhagen), 2023-11, Vol.64 (11), p.3036-3048</ispartof><rights>2023 The Authors. published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3653-4e6b06e81b5d5208c73a0703cbaa5120a5eeb905c4be49d3d1df9e9b06462e5f3</citedby><cites>FETCH-LOGICAL-c3653-4e6b06e81b5d5208c73a0703cbaa5120a5eeb905c4be49d3d1df9e9b06462e5f3</cites><orcidid>0000-0003-0144-3746 ; 0000-0003-1283-7978 ; 0000-0001-6064-1529</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fepi.17763$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fepi.17763$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>315,786,790,27957,27958,50923,51032</link.rule.ids></links><search><creatorcontrib>Ho, Alyssa</creatorcontrib><creatorcontrib>Hannan, Sana</creatorcontrib><creatorcontrib>Thomas, John</creatorcontrib><creatorcontrib>Avigdor, Tamir</creatorcontrib><creatorcontrib>Abdallah, Chifaou</creatorcontrib><creatorcontrib>Dubeau, François</creatorcontrib><creatorcontrib>Gotman, Jean</creatorcontrib><creatorcontrib>Frauscher, Birgit</creatorcontrib><title>Rapid eye movement sleep affects interictal epileptic activity differently in mesiotemporal and neocortical areas</title><title>Epilepsia (Copenhagen)</title><description>Objective
Rapid eye movement (REM) sleep reduces the rate and extent of interictal epileptiform discharges (IEDs). Breakthrough epileptic activity during REM sleep is therefore thought to best localize the seizure onset zone (SOZ). We utilized polysomnography combined with direct cortical recordings to investigate the influences of anatomical locations and the time of night on the suppressive effect of REM sleep on IEDs.
Methods
Forty consecutive patients with drug‐resistant focal epilepsy underwent combined polysomnography and stereo‐electroencephalography during presurgical evaluation. Ten‐minute interictal epochs were selected 2 h prior to sleep onset (wakefulness), and from the first and second half of the night during non‐REM (NREM) sleep and REM sleep. IEDs were detected automatically across all channels. Anatomic localization, time of night, and channel type (within or outside the SOZ) were tested as modulating factors.
Results
Relative to wakefulness, there was a suppression of IEDs by REM sleep in neocortical regions (median = −27.6%), whereas mesiotemporal regions showed an increase in IEDs (19.1%, p = .01, d = .39). This effect was reversed when comparing the regional suppression of IEDs by REM sleep relative to NREM sleep (−35.1% in neocortical, −58.7% in mesiotemporal, p < .001, d = .39). Across all patients, no clinically relevant novel IED regions were observed in REM sleep versus NREM or wakefulness based on our predetermined thresholds (4 IEDs/min in REM, 0 IEDs/min in NREM and wakefulness). Finally, there was a reduction in IEDs in late (NREM: 1.08/min, REM: .61/min) compared to early sleep (NREM: 1.22/min, REM: .69/min) for both NREM (p < .001, d = .21) and REM (p = .04, d = .14).
Significance
Our results demonstrate a spatiotemporal effect of IED suppression by REM sleep relative to wakefulness in neocortical but not mesiotemporal regions, and in late versus early sleep. This suggests the importance of considering sleep stage interactions and the potential influences of anatomical locations when using IEDs to define the epileptic focus.</description><subject>EEG</subject><subject>Epilepsy</subject><subject>Eye movements</subject><subject>Firing pattern</subject><subject>interictal activity</subject><subject>Localization</subject><subject>NREM sleep</subject><subject>rapid eye movement</subject><subject>REM sleep</subject><subject>Seizures</subject><subject>Sleep</subject><subject>Sleep and wakefulness</subject><subject>stereo‐electroencephalography</subject><issn>0013-9580</issn><issn>1528-1167</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><recordid>eNp10E9LwzAYBvAgCs7pwW8Q8KKHbknTJO1RxtTBQBE9hzR9Cxn9tySb9NubWU-CubwEfs_Ly4PQLSULGt8SBrugUgp2hmaUp3lCqZDnaEYIZUnBc3KJrrzfEUKkkGyG9u96sBWGEXDbH6GFLmDfAAxY1zWY4LHtAjhrgm5wXN7AEKzB2gR7tGHElY3MxVQzRolb8LYP0A69i153Fe6gN72LmdPfgfbX6KLWjYeb3zlHn0_rj9VLsn193qwet4lhgrMkA1ESATktecVTkhvJNJGEmVJrTlOiOUBZEG6yErKiYhWt6gKKmMlECrxmc3Q_7R1cvz-AD6q13kDT6HjSwas0F1zmGUlFpHd_6K4_uC5eF1UuGMsFLaJ6mJRxvfcOajU422o3KkrUqXwV-1E_5Ue7nOxXbGz8H6r122ZKfANBD4fz</recordid><startdate>202311</startdate><enddate>202311</enddate><creator>Ho, Alyssa</creator><creator>Hannan, Sana</creator><creator>Thomas, John</creator><creator>Avigdor, Tamir</creator><creator>Abdallah, Chifaou</creator><creator>Dubeau, François</creator><creator>Gotman, Jean</creator><creator>Frauscher, Birgit</creator><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-0144-3746</orcidid><orcidid>https://orcid.org/0000-0003-1283-7978</orcidid><orcidid>https://orcid.org/0000-0001-6064-1529</orcidid></search><sort><creationdate>202311</creationdate><title>Rapid eye movement sleep affects interictal epileptic activity differently in mesiotemporal and neocortical areas</title><author>Ho, Alyssa ; Hannan, Sana ; Thomas, John ; Avigdor, Tamir ; Abdallah, Chifaou ; Dubeau, François ; Gotman, Jean ; Frauscher, Birgit</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3653-4e6b06e81b5d5208c73a0703cbaa5120a5eeb905c4be49d3d1df9e9b06462e5f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>EEG</topic><topic>Epilepsy</topic><topic>Eye movements</topic><topic>Firing pattern</topic><topic>interictal activity</topic><topic>Localization</topic><topic>NREM sleep</topic><topic>rapid eye movement</topic><topic>REM sleep</topic><topic>Seizures</topic><topic>Sleep</topic><topic>Sleep and wakefulness</topic><topic>stereo‐electroencephalography</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ho, Alyssa</creatorcontrib><creatorcontrib>Hannan, Sana</creatorcontrib><creatorcontrib>Thomas, John</creatorcontrib><creatorcontrib>Avigdor, Tamir</creatorcontrib><creatorcontrib>Abdallah, Chifaou</creatorcontrib><creatorcontrib>Dubeau, François</creatorcontrib><creatorcontrib>Gotman, Jean</creatorcontrib><creatorcontrib>Frauscher, Birgit</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Online Library Open Access</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Epilepsia (Copenhagen)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ho, Alyssa</au><au>Hannan, Sana</au><au>Thomas, John</au><au>Avigdor, Tamir</au><au>Abdallah, Chifaou</au><au>Dubeau, François</au><au>Gotman, Jean</au><au>Frauscher, Birgit</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Rapid eye movement sleep affects interictal epileptic activity differently in mesiotemporal and neocortical areas</atitle><jtitle>Epilepsia (Copenhagen)</jtitle><date>2023-11</date><risdate>2023</risdate><volume>64</volume><issue>11</issue><spage>3036</spage><epage>3048</epage><pages>3036-3048</pages><issn>0013-9580</issn><eissn>1528-1167</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Objective
Rapid eye movement (REM) sleep reduces the rate and extent of interictal epileptiform discharges (IEDs). Breakthrough epileptic activity during REM sleep is therefore thought to best localize the seizure onset zone (SOZ). We utilized polysomnography combined with direct cortical recordings to investigate the influences of anatomical locations and the time of night on the suppressive effect of REM sleep on IEDs.
Methods
Forty consecutive patients with drug‐resistant focal epilepsy underwent combined polysomnography and stereo‐electroencephalography during presurgical evaluation. Ten‐minute interictal epochs were selected 2 h prior to sleep onset (wakefulness), and from the first and second half of the night during non‐REM (NREM) sleep and REM sleep. IEDs were detected automatically across all channels. Anatomic localization, time of night, and channel type (within or outside the SOZ) were tested as modulating factors.
Results
Relative to wakefulness, there was a suppression of IEDs by REM sleep in neocortical regions (median = −27.6%), whereas mesiotemporal regions showed an increase in IEDs (19.1%, p = .01, d = .39). This effect was reversed when comparing the regional suppression of IEDs by REM sleep relative to NREM sleep (−35.1% in neocortical, −58.7% in mesiotemporal, p < .001, d = .39). Across all patients, no clinically relevant novel IED regions were observed in REM sleep versus NREM or wakefulness based on our predetermined thresholds (4 IEDs/min in REM, 0 IEDs/min in NREM and wakefulness). Finally, there was a reduction in IEDs in late (NREM: 1.08/min, REM: .61/min) compared to early sleep (NREM: 1.22/min, REM: .69/min) for both NREM (p < .001, d = .21) and REM (p = .04, d = .14).
Significance
Our results demonstrate a spatiotemporal effect of IED suppression by REM sleep relative to wakefulness in neocortical but not mesiotemporal regions, and in late versus early sleep. This suggests the importance of considering sleep stage interactions and the potential influences of anatomical locations when using IEDs to define the epileptic focus.</abstract><cop>Hoboken</cop><pub>Wiley Subscription Services, Inc</pub><doi>10.1111/epi.17763</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-0144-3746</orcidid><orcidid>https://orcid.org/0000-0003-1283-7978</orcidid><orcidid>https://orcid.org/0000-0001-6064-1529</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | EEG Epilepsy Eye movements Firing pattern interictal activity Localization NREM sleep rapid eye movement REM sleep Seizures Sleep Sleep and wakefulness stereo‐electroencephalography |
| title | Rapid eye movement sleep affects interictal epileptic activity differently in mesiotemporal and neocortical areas |
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