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Energy landscapes of resting-state brain networks

During rest, the human brain performs essential functions such as memory maintenance, which are associated with resting-state brain networks (RSNs) including the default-mode network (DMN) and frontoparietal network (FPN). Previous studies based on spiking-neuron network models and their reduced mod...

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Autores principales: Watanabe, Takamitsu, Hirose, Satoshi, Wada, Hiroyuki, Imai, Yoshio, Machida, Toru, Shirouzu, Ichiro, Konishi, Seiki, Miyashita, Yasushi, Masuda, Naoki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3933812/
https://www.ncbi.nlm.nih.gov/pubmed/24611044
http://dx.doi.org/10.3389/fninf.2014.00012
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author Watanabe, Takamitsu
Hirose, Satoshi
Wada, Hiroyuki
Imai, Yoshio
Machida, Toru
Shirouzu, Ichiro
Konishi, Seiki
Miyashita, Yasushi
Masuda, Naoki
author_facet Watanabe, Takamitsu
Hirose, Satoshi
Wada, Hiroyuki
Imai, Yoshio
Machida, Toru
Shirouzu, Ichiro
Konishi, Seiki
Miyashita, Yasushi
Masuda, Naoki
author_sort Watanabe, Takamitsu
collection PubMed
description During rest, the human brain performs essential functions such as memory maintenance, which are associated with resting-state brain networks (RSNs) including the default-mode network (DMN) and frontoparietal network (FPN). Previous studies based on spiking-neuron network models and their reduced models, as well as those based on imaging data, suggest that resting-state network activity can be captured as attractor dynamics, i.e., dynamics of the brain state toward an attractive state and transitions between different attractors. Here, we analyze the energy landscapes of the RSNs by applying the maximum entropy model, or equivalently the Ising spin model, to human RSN data. We use the previously estimated parameter values to define the energy landscape, and the disconnectivity graph method to estimate the number of local energy minima (equivalent to attractors in attractor dynamics), the basin size, and hierarchical relationships among the different local minima. In both of the DMN and FPN, low-energy local minima tended to have large basins. A majority of the network states belonged to a basin of one of a few local minima. Therefore, a small number of local minima constituted the backbone of each RSN. In the DMN, the energy landscape consisted of two groups of low-energy local minima that are separated by a relatively high energy barrier. Within each group, the activity patterns of the local minima were similar, and different minima were connected by relatively low energy barriers. In the FPN, all dominant local minima were separated by relatively low energy barriers such that they formed a single coarse-grained global minimum. Our results indicate that multistable attractor dynamics may underlie the DMN, but not the FPN, and assist memory maintenance with different memory states.
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spelling pubmed-39338122014-03-07 Energy landscapes of resting-state brain networks Watanabe, Takamitsu Hirose, Satoshi Wada, Hiroyuki Imai, Yoshio Machida, Toru Shirouzu, Ichiro Konishi, Seiki Miyashita, Yasushi Masuda, Naoki Front Neuroinform Neuroscience During rest, the human brain performs essential functions such as memory maintenance, which are associated with resting-state brain networks (RSNs) including the default-mode network (DMN) and frontoparietal network (FPN). Previous studies based on spiking-neuron network models and their reduced models, as well as those based on imaging data, suggest that resting-state network activity can be captured as attractor dynamics, i.e., dynamics of the brain state toward an attractive state and transitions between different attractors. Here, we analyze the energy landscapes of the RSNs by applying the maximum entropy model, or equivalently the Ising spin model, to human RSN data. We use the previously estimated parameter values to define the energy landscape, and the disconnectivity graph method to estimate the number of local energy minima (equivalent to attractors in attractor dynamics), the basin size, and hierarchical relationships among the different local minima. In both of the DMN and FPN, low-energy local minima tended to have large basins. A majority of the network states belonged to a basin of one of a few local minima. Therefore, a small number of local minima constituted the backbone of each RSN. In the DMN, the energy landscape consisted of two groups of low-energy local minima that are separated by a relatively high energy barrier. Within each group, the activity patterns of the local minima were similar, and different minima were connected by relatively low energy barriers. In the FPN, all dominant local minima were separated by relatively low energy barriers such that they formed a single coarse-grained global minimum. Our results indicate that multistable attractor dynamics may underlie the DMN, but not the FPN, and assist memory maintenance with different memory states. Frontiers Media S.A. 2014-02-25 /pmc/articles/PMC3933812/ /pubmed/24611044 http://dx.doi.org/10.3389/fninf.2014.00012 Text en Copyright © 2014 Watanabe, Hirose, Wada, Imai, Machida, Shirouzu, Konishi, Miyashita and Masuda. http://creativecommons.org/licenses/by/3.0/ 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) or licensor 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
Watanabe, Takamitsu
Hirose, Satoshi
Wada, Hiroyuki
Imai, Yoshio
Machida, Toru
Shirouzu, Ichiro
Konishi, Seiki
Miyashita, Yasushi
Masuda, Naoki
Energy landscapes of resting-state brain networks
title Energy landscapes of resting-state brain networks
title_full Energy landscapes of resting-state brain networks
title_fullStr Energy landscapes of resting-state brain networks
title_full_unstemmed Energy landscapes of resting-state brain networks
title_short Energy landscapes of resting-state brain networks
title_sort energy landscapes of resting-state brain networks
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3933812/
https://www.ncbi.nlm.nih.gov/pubmed/24611044
http://dx.doi.org/10.3389/fninf.2014.00012
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