Evaluation of Resting Spatio-Temporal Dynamics of a Neural Mass Model Using Resting fMRI Connectivity and EEG Microstates

Resting-state brain activities have been extensively investigated to understand the macro-scale network architecture of the human brain using non-invasive imaging methods such as fMRI, EEG, and MEG. Previous studies revealed a mechanistic origin of resting-state networks (RSNs) using the connectome...

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Main Authors: Hidenori Endo, Nobuo Hiroe, Okito Yamashita
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-01-01
Series:Frontiers in Computational Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fncom.2019.00091/full
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author Hidenori Endo
Hidenori Endo
Nobuo Hiroe
Okito Yamashita
Okito Yamashita
author_facet Hidenori Endo
Hidenori Endo
Nobuo Hiroe
Okito Yamashita
Okito Yamashita
author_sort Hidenori Endo
collection DOAJ
description Resting-state brain activities have been extensively investigated to understand the macro-scale network architecture of the human brain using non-invasive imaging methods such as fMRI, EEG, and MEG. Previous studies revealed a mechanistic origin of resting-state networks (RSNs) using the connectome dynamics modeling approach, where the neural mass dynamics model constrained by the structural connectivity is simulated to replicate the resting-state networks measured with fMRI and/or fast synchronization transitions with EEG/MEG. However, there is still little understanding of the relationship between the slow fluctuations measured with fMRI and the fast synchronization transitions with EEG/MEG. In this study, as a first step toward evaluating experimental evidence of resting state activity at two different time scales but in a unified way, we investigate connectome dynamics models that simultaneously explain resting-state functional connectivity (rsFC) and EEG microstates. Here, we introduce empirical rsFC and microstates as evaluation criteria of simulated neuronal dynamics obtained by the Larter-Breakspear model in one cortical region connected with those in other cortical regions based on structural connectivity. We optimized the global coupling strength and the local gain parameter (variance of the excitatory and inhibitory threshold) of the simulated neuronal dynamics by fitting both rsFC and microstate spatial patterns to those of experimental ones. As a result, we found that simulated neuronal dynamics in a narrow optimal parameter range simultaneously reproduced empirical rsFC and microstates. Two parameter groups had different inter-regional interdependence. One type of dynamics was synchronized across the whole brain region, and the other type was synchronized between brain regions with strong structural connectivity. In other words, both fast synchronization transitions and slow BOLD fluctuation changed based on structural connectivity in the two parameter groups. Empirical microstates were similar to simulated microstates in the two parameter groups. Thus, fast synchronization transitions correlated with slow BOLD fluctuation based on structural connectivity yielded characteristics of microstates. Our results demonstrate that a bottom-up approach, which extends the single neuronal dynamics model based on empirical observations into a neural mass dynamics model and integrates structural connectivity, effectively reveals both macroscopic fast, and slow resting-state network dynamics.
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spelling doaj.art-a46df87c1eb2432cbf8571abba124f7d2022-12-22T01:54:08ZengFrontiers Media S.A.Frontiers in Computational Neuroscience1662-51882020-01-011310.3389/fncom.2019.00091502059Evaluation of Resting Spatio-Temporal Dynamics of a Neural Mass Model Using Resting fMRI Connectivity and EEG MicrostatesHidenori Endo0Hidenori Endo1Nobuo Hiroe2Okito Yamashita3Okito Yamashita4Graduate School of Information Science, Nara Institute of Science and Technology, Nara, JapanATR Neural Information Analysis Laboratories, Kyoto, JapanATR Neural Information Analysis Laboratories, Kyoto, JapanATR Neural Information Analysis Laboratories, Kyoto, JapanCenter for Advanced Intelligence Project, RIKEN, Tokyo, JapanResting-state brain activities have been extensively investigated to understand the macro-scale network architecture of the human brain using non-invasive imaging methods such as fMRI, EEG, and MEG. Previous studies revealed a mechanistic origin of resting-state networks (RSNs) using the connectome dynamics modeling approach, where the neural mass dynamics model constrained by the structural connectivity is simulated to replicate the resting-state networks measured with fMRI and/or fast synchronization transitions with EEG/MEG. However, there is still little understanding of the relationship between the slow fluctuations measured with fMRI and the fast synchronization transitions with EEG/MEG. In this study, as a first step toward evaluating experimental evidence of resting state activity at two different time scales but in a unified way, we investigate connectome dynamics models that simultaneously explain resting-state functional connectivity (rsFC) and EEG microstates. Here, we introduce empirical rsFC and microstates as evaluation criteria of simulated neuronal dynamics obtained by the Larter-Breakspear model in one cortical region connected with those in other cortical regions based on structural connectivity. We optimized the global coupling strength and the local gain parameter (variance of the excitatory and inhibitory threshold) of the simulated neuronal dynamics by fitting both rsFC and microstate spatial patterns to those of experimental ones. As a result, we found that simulated neuronal dynamics in a narrow optimal parameter range simultaneously reproduced empirical rsFC and microstates. Two parameter groups had different inter-regional interdependence. One type of dynamics was synchronized across the whole brain region, and the other type was synchronized between brain regions with strong structural connectivity. In other words, both fast synchronization transitions and slow BOLD fluctuation changed based on structural connectivity in the two parameter groups. Empirical microstates were similar to simulated microstates in the two parameter groups. Thus, fast synchronization transitions correlated with slow BOLD fluctuation based on structural connectivity yielded characteristics of microstates. Our results demonstrate that a bottom-up approach, which extends the single neuronal dynamics model based on empirical observations into a neural mass dynamics model and integrates structural connectivity, effectively reveals both macroscopic fast, and slow resting-state network dynamics.https://www.frontiersin.org/article/10.3389/fncom.2019.00091/fullresting-state networksresting-state functional connectivitymicrostatesneural mass modelcortico-cortical dynamics
spellingShingle Hidenori Endo
Hidenori Endo
Nobuo Hiroe
Okito Yamashita
Okito Yamashita
Evaluation of Resting Spatio-Temporal Dynamics of a Neural Mass Model Using Resting fMRI Connectivity and EEG Microstates
Frontiers in Computational Neuroscience
resting-state networks
resting-state functional connectivity
microstates
neural mass model
cortico-cortical dynamics
title Evaluation of Resting Spatio-Temporal Dynamics of a Neural Mass Model Using Resting fMRI Connectivity and EEG Microstates
title_full Evaluation of Resting Spatio-Temporal Dynamics of a Neural Mass Model Using Resting fMRI Connectivity and EEG Microstates
title_fullStr Evaluation of Resting Spatio-Temporal Dynamics of a Neural Mass Model Using Resting fMRI Connectivity and EEG Microstates
title_full_unstemmed Evaluation of Resting Spatio-Temporal Dynamics of a Neural Mass Model Using Resting fMRI Connectivity and EEG Microstates
title_short Evaluation of Resting Spatio-Temporal Dynamics of a Neural Mass Model Using Resting fMRI Connectivity and EEG Microstates
title_sort evaluation of resting spatio temporal dynamics of a neural mass model using resting fmri connectivity and eeg microstates
topic resting-state networks
resting-state functional connectivity
microstates
neural mass model
cortico-cortical dynamics
url https://www.frontiersin.org/article/10.3389/fncom.2019.00091/full
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