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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...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
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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. |
format | Online Article Text |
id | pubmed-8790481 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
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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