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A comprehensive neural simulation of slow-wave sleep and highly responsive wakefulness dynamics

Hallmarks of neural dynamics during healthy human brain states span spatial scales from neuromodulators acting on microscopic ion channels to macroscopic changes in communication between brain regions. Developing a scale-integrated understanding of neural dynamics has therefore remained challenging....

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Autores principales: Goldman, Jennifer S., Kusch, Lionel, Aquilue, David, Yalçınkaya, Bahar Hazal, Depannemaecker, Damien, Ancourt, Kevin, Nghiem, Trang-Anh E., Jirsa, Viktor, Destexhe, Alain
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9880280/
https://www.ncbi.nlm.nih.gov/pubmed/36714530
http://dx.doi.org/10.3389/fncom.2022.1058957
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author Goldman, Jennifer S.
Kusch, Lionel
Aquilue, David
Yalçınkaya, Bahar Hazal
Depannemaecker, Damien
Ancourt, Kevin
Nghiem, Trang-Anh E.
Jirsa, Viktor
Destexhe, Alain
author_facet Goldman, Jennifer S.
Kusch, Lionel
Aquilue, David
Yalçınkaya, Bahar Hazal
Depannemaecker, Damien
Ancourt, Kevin
Nghiem, Trang-Anh E.
Jirsa, Viktor
Destexhe, Alain
author_sort Goldman, Jennifer S.
collection PubMed
description Hallmarks of neural dynamics during healthy human brain states span spatial scales from neuromodulators acting on microscopic ion channels to macroscopic changes in communication between brain regions. Developing a scale-integrated understanding of neural dynamics has therefore remained challenging. Here, we perform the integration across scales using mean-field modeling of Adaptive Exponential (AdEx) neurons, explicitly incorporating intrinsic properties of excitatory and inhibitory neurons. The model was run using The Virtual Brain (TVB) simulator, and is open-access in EBRAINS. We report that when AdEx mean-field neural populations are connected via structural tracts defined by the human connectome, macroscopic dynamics resembling human brain activity emerge. Importantly, the model can qualitatively and quantitatively account for properties of empirically observed spontaneous and stimulus-evoked dynamics in space, time, phase, and frequency domains. Large-scale properties of cortical dynamics are shown to emerge from both microscopic-scale adaptation that control transitions between wake-like to sleep-like activity, and the organization of the human structural connectome; together, they shape the spatial extent of synchrony and phase coherence across brain regions consistent with the propagation of sleep-like spontaneous traveling waves at intermediate scales. Remarkably, the model also reproduces brain-wide, enhanced responsiveness and capacity to encode information particularly during wake-like states, as quantified using the perturbational complexity index. The model was run using The Virtual Brain (TVB) simulator, and is open-access in EBRAINS. This approach not only provides a scale-integrated understanding of brain states and their underlying mechanisms, but also open access tools to investigate brain responsiveness, toward producing a more unified, formal understanding of experimental data from conscious and unconscious states, as well as their associated pathologies.
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spelling pubmed-98802802023-01-28 A comprehensive neural simulation of slow-wave sleep and highly responsive wakefulness dynamics Goldman, Jennifer S. Kusch, Lionel Aquilue, David Yalçınkaya, Bahar Hazal Depannemaecker, Damien Ancourt, Kevin Nghiem, Trang-Anh E. Jirsa, Viktor Destexhe, Alain Front Comput Neurosci Neuroscience Hallmarks of neural dynamics during healthy human brain states span spatial scales from neuromodulators acting on microscopic ion channels to macroscopic changes in communication between brain regions. Developing a scale-integrated understanding of neural dynamics has therefore remained challenging. Here, we perform the integration across scales using mean-field modeling of Adaptive Exponential (AdEx) neurons, explicitly incorporating intrinsic properties of excitatory and inhibitory neurons. The model was run using The Virtual Brain (TVB) simulator, and is open-access in EBRAINS. We report that when AdEx mean-field neural populations are connected via structural tracts defined by the human connectome, macroscopic dynamics resembling human brain activity emerge. Importantly, the model can qualitatively and quantitatively account for properties of empirically observed spontaneous and stimulus-evoked dynamics in space, time, phase, and frequency domains. Large-scale properties of cortical dynamics are shown to emerge from both microscopic-scale adaptation that control transitions between wake-like to sleep-like activity, and the organization of the human structural connectome; together, they shape the spatial extent of synchrony and phase coherence across brain regions consistent with the propagation of sleep-like spontaneous traveling waves at intermediate scales. Remarkably, the model also reproduces brain-wide, enhanced responsiveness and capacity to encode information particularly during wake-like states, as quantified using the perturbational complexity index. The model was run using The Virtual Brain (TVB) simulator, and is open-access in EBRAINS. This approach not only provides a scale-integrated understanding of brain states and their underlying mechanisms, but also open access tools to investigate brain responsiveness, toward producing a more unified, formal understanding of experimental data from conscious and unconscious states, as well as their associated pathologies. Frontiers Media S.A. 2023-01-13 /pmc/articles/PMC9880280/ /pubmed/36714530 http://dx.doi.org/10.3389/fncom.2022.1058957 Text en Copyright © 2023 Goldman, Kusch, Aquilue, Yalçınkaya, Depannemaecker, Ancourt, Nghiem, Jirsa and Destexhe. 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
Goldman, Jennifer S.
Kusch, Lionel
Aquilue, David
Yalçınkaya, Bahar Hazal
Depannemaecker, Damien
Ancourt, Kevin
Nghiem, Trang-Anh E.
Jirsa, Viktor
Destexhe, Alain
A comprehensive neural simulation of slow-wave sleep and highly responsive wakefulness dynamics
title A comprehensive neural simulation of slow-wave sleep and highly responsive wakefulness dynamics
title_full A comprehensive neural simulation of slow-wave sleep and highly responsive wakefulness dynamics
title_fullStr A comprehensive neural simulation of slow-wave sleep and highly responsive wakefulness dynamics
title_full_unstemmed A comprehensive neural simulation of slow-wave sleep and highly responsive wakefulness dynamics
title_short A comprehensive neural simulation of slow-wave sleep and highly responsive wakefulness dynamics
title_sort comprehensive neural simulation of slow-wave sleep and highly responsive wakefulness dynamics
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9880280/
https://www.ncbi.nlm.nih.gov/pubmed/36714530
http://dx.doi.org/10.3389/fncom.2022.1058957
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