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The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes

The large multicomponent K-complex (KC) and the rhythmic spindle are the hallmarks of non-rapid eye movement (NREM)-2 sleep stage. We studied with magnetoencephalography (MEG) the progress of light sleep (NREM-1 and NREM-2) and emergence of KCs and spindles. Seven periods of interest (POI) were anal...

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Autores principales: Ioannides, Andreas A., Liu, Lichan, Kostopoulos, George K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6692490/
https://www.ncbi.nlm.nih.gov/pubmed/31447635
http://dx.doi.org/10.3389/fnins.2019.00814
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author Ioannides, Andreas A.
Liu, Lichan
Kostopoulos, George K.
author_facet Ioannides, Andreas A.
Liu, Lichan
Kostopoulos, George K.
author_sort Ioannides, Andreas A.
collection PubMed
description The large multicomponent K-complex (KC) and the rhythmic spindle are the hallmarks of non-rapid eye movement (NREM)-2 sleep stage. We studied with magnetoencephalography (MEG) the progress of light sleep (NREM-1 and NREM-2) and emergence of KCs and spindles. Seven periods of interest (POI) were analyzed: wakefulness, the two quiet “core” periods of light sleep (periods free from any prominent phasic or oscillatory events) and four periods before and during spindles and KCs. For each POI, eight 2-s (1250 time slices) segments were used. We employed magnetic field tomography (MFT) to extract an independent tomographic estimate of brain activity from each MEG data sample. The spectral power was then computed for each voxel in the brain for each segment of each POI. The sets of eight maps from two POIs were contrasted using a voxel-by-voxel t-test. Only increased spectral power was identified in the four key contrasts between POIs before and during spindles and KCs versus the NREM2 core. Common increases were identified for all four subjects, especially within and close to the anterior cingulate cortex (ACC). These common increases were widespread for low frequencies, while for higher frequencies they were focal, confined to specific brain areas. For the pre-KC POI, only one prominent increase was identified, confined to the theta/alpha bands in a small area in the dorsal caudal part of ACC (dcACC). During KCs, the activity in this area grows in intensity and extent (in space and frequency), filling the space between the areas that expanded their low frequency activity (in the delta band) during NREM2 compared to NREM1. Our main finding is that prominent spectral power increases before NREM2 graphoelements are confined to the dcACC, and only for KCs, sharing common features with changes of activity in dcACC of the well-studied error related negativity (ERN). ERN is seen in awake state, in perceptual conflict and situations where there is a difference between expected and actual environmental or internal events. These results suggest that a KC is the sleep side of the awake state ERN, both serving their putative sentinel roles in the frame of the saliency network.
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spelling pubmed-66924902019-08-23 The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes Ioannides, Andreas A. Liu, Lichan Kostopoulos, George K. Front Neurosci Neuroscience The large multicomponent K-complex (KC) and the rhythmic spindle are the hallmarks of non-rapid eye movement (NREM)-2 sleep stage. We studied with magnetoencephalography (MEG) the progress of light sleep (NREM-1 and NREM-2) and emergence of KCs and spindles. Seven periods of interest (POI) were analyzed: wakefulness, the two quiet “core” periods of light sleep (periods free from any prominent phasic or oscillatory events) and four periods before and during spindles and KCs. For each POI, eight 2-s (1250 time slices) segments were used. We employed magnetic field tomography (MFT) to extract an independent tomographic estimate of brain activity from each MEG data sample. The spectral power was then computed for each voxel in the brain for each segment of each POI. The sets of eight maps from two POIs were contrasted using a voxel-by-voxel t-test. Only increased spectral power was identified in the four key contrasts between POIs before and during spindles and KCs versus the NREM2 core. Common increases were identified for all four subjects, especially within and close to the anterior cingulate cortex (ACC). These common increases were widespread for low frequencies, while for higher frequencies they were focal, confined to specific brain areas. For the pre-KC POI, only one prominent increase was identified, confined to the theta/alpha bands in a small area in the dorsal caudal part of ACC (dcACC). During KCs, the activity in this area grows in intensity and extent (in space and frequency), filling the space between the areas that expanded their low frequency activity (in the delta band) during NREM2 compared to NREM1. Our main finding is that prominent spectral power increases before NREM2 graphoelements are confined to the dcACC, and only for KCs, sharing common features with changes of activity in dcACC of the well-studied error related negativity (ERN). ERN is seen in awake state, in perceptual conflict and situations where there is a difference between expected and actual environmental or internal events. These results suggest that a KC is the sleep side of the awake state ERN, both serving their putative sentinel roles in the frame of the saliency network. Frontiers Media S.A. 2019-08-07 /pmc/articles/PMC6692490/ /pubmed/31447635 http://dx.doi.org/10.3389/fnins.2019.00814 Text en Copyright © 2019 Ioannides, Liu and Kostopoulos. http://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 Neuroscience
Ioannides, Andreas A.
Liu, Lichan
Kostopoulos, George K.
The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes
title The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes
title_full The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes
title_fullStr The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes
title_full_unstemmed The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes
title_short The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes
title_sort emergence of spindles and k-complexes and the role of the dorsal caudal part of the anterior cingulate as the generator of k-complexes
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6692490/
https://www.ncbi.nlm.nih.gov/pubmed/31447635
http://dx.doi.org/10.3389/fnins.2019.00814
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