Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.

The resting-state brain is often considered a nonlinear dynamic system transitioning among multiple coexisting stable states. Despite the increasing number of studies on the multistability of the brain system, the processes of state transitions have rarely been systematically explored. Thus, we inve...

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Main Authors: Jiyoung Kang, Chongwon Pae, Hae-Jeong Park
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0222161
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spelling doaj-392405493a2f401fac9f17e9cd1b51fb2021-03-04T11:21:51ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-01149e022216110.1371/journal.pone.0222161Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.Jiyoung KangChongwon PaeHae-Jeong ParkThe resting-state brain is often considered a nonlinear dynamic system transitioning among multiple coexisting stable states. Despite the increasing number of studies on the multistability of the brain system, the processes of state transitions have rarely been systematically explored. Thus, we investigated the state transition processes of the human cerebral cortex system at rest by introducing a graph-theoretical analysis of the state transition network. The energy landscape analysis of brain state occurrences, estimated using the pairwise maximum entropy model for resting-state fMRI data, identified multiple local minima, some of which mediate multi-step transitions toward the global minimum. The state transition among local minima is clustered into two groups according to state transition rates and most inter-group state transitions were mediated by a hub transition state. The distance to the hub transition state determined the path length of the inter-group transition. The cortical system appeared to have redundancy in inter-group transitions when the hub transition state was removed. Such a hub-like organization of transition processes disappeared when the connectivity of the cortical system was altered from the resting-state configuration. In the state transition, the default mode network acts as a transition hub, while coactivation of the prefrontal cortex and default mode network is captured as the global minimum. In summary, the resting-state cerebral cortex has a well-organized architecture of state transitions among stable states, when evaluated by a graph-theoretical analysis of the nonlinear state transition network of the brain.https://doi.org/10.1371/journal.pone.0222161
collection DOAJ
language English
format Article
sources DOAJ
author Jiyoung Kang
Chongwon Pae
Hae-Jeong Park
spellingShingle Jiyoung Kang
Chongwon Pae
Hae-Jeong Park
Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.
PLoS ONE
author_facet Jiyoung Kang
Chongwon Pae
Hae-Jeong Park
author_sort Jiyoung Kang
title Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.
title_short Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.
title_full Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.
title_fullStr Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.
title_full_unstemmed Graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.
title_sort graph-theoretical analysis for energy landscape reveals the organization of state transitions in the resting-state human cerebral cortex.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2019-01-01
description The resting-state brain is often considered a nonlinear dynamic system transitioning among multiple coexisting stable states. Despite the increasing number of studies on the multistability of the brain system, the processes of state transitions have rarely been systematically explored. Thus, we investigated the state transition processes of the human cerebral cortex system at rest by introducing a graph-theoretical analysis of the state transition network. The energy landscape analysis of brain state occurrences, estimated using the pairwise maximum entropy model for resting-state fMRI data, identified multiple local minima, some of which mediate multi-step transitions toward the global minimum. The state transition among local minima is clustered into two groups according to state transition rates and most inter-group state transitions were mediated by a hub transition state. The distance to the hub transition state determined the path length of the inter-group transition. The cortical system appeared to have redundancy in inter-group transitions when the hub transition state was removed. Such a hub-like organization of transition processes disappeared when the connectivity of the cortical system was altered from the resting-state configuration. In the state transition, the default mode network acts as a transition hub, while coactivation of the prefrontal cortex and default mode network is captured as the global minimum. In summary, the resting-state cerebral cortex has a well-organized architecture of state transitions among stable states, when evaluated by a graph-theoretical analysis of the nonlinear state transition network of the brain.
url https://doi.org/10.1371/journal.pone.0222161
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