Cargando…

Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: An intracranial electroencephalographic study

Sleep is punctuated by transient elevations of vigilance level called arousals or awakenings depending on their durations. Understanding the dynamics of brain activity modifications during these transitional phases could help to better understand the changes in cognitive functions according to vigil...

Descripción completa

Detalles Bibliográficos
Autores principales: Ruby, Perrine, Eskinazi, Mickael, Bouet, Romain, Rheims, Sylvain, Peter‐Derex, Laure
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8519849/
https://www.ncbi.nlm.nih.gov/pubmed/34355461
http://dx.doi.org/10.1002/hbm.25609
_version_ 1784584540006645760
author Ruby, Perrine
Eskinazi, Mickael
Bouet, Romain
Rheims, Sylvain
Peter‐Derex, Laure
author_facet Ruby, Perrine
Eskinazi, Mickael
Bouet, Romain
Rheims, Sylvain
Peter‐Derex, Laure
author_sort Ruby, Perrine
collection PubMed
description Sleep is punctuated by transient elevations of vigilance level called arousals or awakenings depending on their durations. Understanding the dynamics of brain activity modifications during these transitional phases could help to better understand the changes in cognitive functions according to vigilance states. In this study, we investigated the activity of memory‐related areas (hippocampus and orbitofrontal cortex) during short (3 s to 2 min) arousing reactions detected from thalamic activity, using intracranial recordings in four drug‐resistant epilepsy patients. The average power of the signal between 0.5 and 128 Hz was compared across four time windows: 10 s of preceding sleep, the first part and the end of the arousal/awakening, and 10 s of wakefulness. We observed that (a) in most frequency bands, the spectral power during hippocampal arousal/awakenings is intermediate between wakefulness and sleep whereas frontal cortex shows an early increase in low and fast activities during non‐rapid‐eye‐movement (NREM) sleep arousals/awakenings; (b) this pattern depends on the preceding sleep stage with fewer modifications for REM than for non‐REM sleep arousal/awakenings, potentially reflecting the EEG similarities between REM sleep and wakefulness; (c) a greater activation at the arousing reaction onset in the prefrontal cortex predicts longer arousals/awakenings. Our findings suggest that hippocampus and prefrontal arousals/awakenings are progressive phenomena modulated by sleep stage, and, in the neocortex, by the intensity of the early activation. This pattern of activity could underlie the link between sleep stage, arousal/awakening duration and restoration of memory abilities including dream recall.
format Online
Article
Text
id pubmed-8519849
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher John Wiley & Sons, Inc.
record_format MEDLINE/PubMed
spelling pubmed-85198492021-10-22 Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: An intracranial electroencephalographic study Ruby, Perrine Eskinazi, Mickael Bouet, Romain Rheims, Sylvain Peter‐Derex, Laure Hum Brain Mapp Research Articles Sleep is punctuated by transient elevations of vigilance level called arousals or awakenings depending on their durations. Understanding the dynamics of brain activity modifications during these transitional phases could help to better understand the changes in cognitive functions according to vigilance states. In this study, we investigated the activity of memory‐related areas (hippocampus and orbitofrontal cortex) during short (3 s to 2 min) arousing reactions detected from thalamic activity, using intracranial recordings in four drug‐resistant epilepsy patients. The average power of the signal between 0.5 and 128 Hz was compared across four time windows: 10 s of preceding sleep, the first part and the end of the arousal/awakening, and 10 s of wakefulness. We observed that (a) in most frequency bands, the spectral power during hippocampal arousal/awakenings is intermediate between wakefulness and sleep whereas frontal cortex shows an early increase in low and fast activities during non‐rapid‐eye‐movement (NREM) sleep arousals/awakenings; (b) this pattern depends on the preceding sleep stage with fewer modifications for REM than for non‐REM sleep arousal/awakenings, potentially reflecting the EEG similarities between REM sleep and wakefulness; (c) a greater activation at the arousing reaction onset in the prefrontal cortex predicts longer arousals/awakenings. Our findings suggest that hippocampus and prefrontal arousals/awakenings are progressive phenomena modulated by sleep stage, and, in the neocortex, by the intensity of the early activation. This pattern of activity could underlie the link between sleep stage, arousal/awakening duration and restoration of memory abilities including dream recall. John Wiley & Sons, Inc. 2021-08-06 /pmc/articles/PMC8519849/ /pubmed/34355461 http://dx.doi.org/10.1002/hbm.25609 Text en © 2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Research Articles
Ruby, Perrine
Eskinazi, Mickael
Bouet, Romain
Rheims, Sylvain
Peter‐Derex, Laure
Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: An intracranial electroencephalographic study
title Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: An intracranial electroencephalographic study
title_full Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: An intracranial electroencephalographic study
title_fullStr Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: An intracranial electroencephalographic study
title_full_unstemmed Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: An intracranial electroencephalographic study
title_short Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: An intracranial electroencephalographic study
title_sort dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: an intracranial electroencephalographic study
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8519849/
https://www.ncbi.nlm.nih.gov/pubmed/34355461
http://dx.doi.org/10.1002/hbm.25609
work_keys_str_mv AT rubyperrine dynamicsofhippocampusandorbitofrontalcortexactivityduringarousingreactionsfromsleepanintracranialelectroencephalographicstudy
AT eskinazimickael dynamicsofhippocampusandorbitofrontalcortexactivityduringarousingreactionsfromsleepanintracranialelectroencephalographicstudy
AT bouetromain dynamicsofhippocampusandorbitofrontalcortexactivityduringarousingreactionsfromsleepanintracranialelectroencephalographicstudy
AT rheimssylvain dynamicsofhippocampusandorbitofrontalcortexactivityduringarousingreactionsfromsleepanintracranialelectroencephalographicstudy
AT peterderexlaure dynamicsofhippocampusandorbitofrontalcortexactivityduringarousingreactionsfromsleepanintracranialelectroencephalographicstudy