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Spatiotemporal Patterns of Adaptation-Induced Slow Oscillations in a Whole-Brain Model of Slow-Wave Sleep

During slow-wave sleep, the brain is in a self-organized regime in which slow oscillations (SOs) between up- and down-states travel across the cortex. While an isolated piece of cortex can produce SOs, the brain-wide propagation of these oscillations are thought to be mediated by the long-range axon...

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Autores principales: Cakan, Caglar, Dimulescu, Cristiana, Khakimova, Liliia, Obst, Daniela, Flöel, Agnes, Obermayer, Klaus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8790481/
https://www.ncbi.nlm.nih.gov/pubmed/35095451
http://dx.doi.org/10.3389/fncom.2021.800101
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author Cakan, Caglar
Dimulescu, Cristiana
Khakimova, Liliia
Obst, Daniela
Flöel, Agnes
Obermayer, Klaus
author_facet Cakan, Caglar
Dimulescu, Cristiana
Khakimova, Liliia
Obst, Daniela
Flöel, Agnes
Obermayer, Klaus
author_sort Cakan, Caglar
collection PubMed
description During slow-wave sleep, the brain is in a self-organized regime in which slow oscillations (SOs) between up- and down-states travel across the cortex. While an isolated piece of cortex can produce SOs, the brain-wide propagation of these oscillations are thought to be mediated by the long-range axonal connections. We address the mechanism of how SOs emerge and recruit large parts of the brain using a whole-brain model constructed from empirical connectivity data in which SOs are induced independently in each brain area by a local adaptation mechanism. Using an evolutionary optimization approach, good fits to human resting-state fMRI data and sleep EEG data are found at values of the adaptation strength close to a bifurcation where the model produces a balance between local and global SOs with realistic spatiotemporal statistics. Local oscillations are more frequent, last shorter, and have a lower amplitude. Global oscillations spread as waves of silence across the undirected brain graph, traveling from anterior to posterior regions. These traveling waves are caused by heterogeneities in the brain network in which the connection strengths between brain areas determine which areas transition to a down-state first, and thus initiate traveling waves across the cortex. Our results demonstrate the utility of whole-brain models for explaining the origin of large-scale cortical oscillations and how they are shaped by the connectome.
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spelling pubmed-87904812022-01-27 Spatiotemporal Patterns of Adaptation-Induced Slow Oscillations in a Whole-Brain Model of Slow-Wave Sleep Cakan, Caglar Dimulescu, Cristiana Khakimova, Liliia Obst, Daniela Flöel, Agnes Obermayer, Klaus Front Comput Neurosci Neuroscience During slow-wave sleep, the brain is in a self-organized regime in which slow oscillations (SOs) between up- and down-states travel across the cortex. While an isolated piece of cortex can produce SOs, the brain-wide propagation of these oscillations are thought to be mediated by the long-range axonal connections. We address the mechanism of how SOs emerge and recruit large parts of the brain using a whole-brain model constructed from empirical connectivity data in which SOs are induced independently in each brain area by a local adaptation mechanism. Using an evolutionary optimization approach, good fits to human resting-state fMRI data and sleep EEG data are found at values of the adaptation strength close to a bifurcation where the model produces a balance between local and global SOs with realistic spatiotemporal statistics. Local oscillations are more frequent, last shorter, and have a lower amplitude. Global oscillations spread as waves of silence across the undirected brain graph, traveling from anterior to posterior regions. These traveling waves are caused by heterogeneities in the brain network in which the connection strengths between brain areas determine which areas transition to a down-state first, and thus initiate traveling waves across the cortex. Our results demonstrate the utility of whole-brain models for explaining the origin of large-scale cortical oscillations and how they are shaped by the connectome. Frontiers Media S.A. 2022-01-12 /pmc/articles/PMC8790481/ /pubmed/35095451 http://dx.doi.org/10.3389/fncom.2021.800101 Text en Copyright © 2022 Cakan, Dimulescu, Khakimova, Obst, Flöel and Obermayer. 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 Neuroscience
Cakan, Caglar
Dimulescu, Cristiana
Khakimova, Liliia
Obst, Daniela
Flöel, Agnes
Obermayer, Klaus
Spatiotemporal Patterns of Adaptation-Induced Slow Oscillations in a Whole-Brain Model of Slow-Wave Sleep
title Spatiotemporal Patterns of Adaptation-Induced Slow Oscillations in a Whole-Brain Model of Slow-Wave Sleep
title_full Spatiotemporal Patterns of Adaptation-Induced Slow Oscillations in a Whole-Brain Model of Slow-Wave Sleep
title_fullStr Spatiotemporal Patterns of Adaptation-Induced Slow Oscillations in a Whole-Brain Model of Slow-Wave Sleep
title_full_unstemmed Spatiotemporal Patterns of Adaptation-Induced Slow Oscillations in a Whole-Brain Model of Slow-Wave Sleep
title_short Spatiotemporal Patterns of Adaptation-Induced Slow Oscillations in a Whole-Brain Model of Slow-Wave Sleep
title_sort spatiotemporal patterns of adaptation-induced slow oscillations in a whole-brain model of slow-wave sleep
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8790481/
https://www.ncbi.nlm.nih.gov/pubmed/35095451
http://dx.doi.org/10.3389/fncom.2021.800101
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