Abstract

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.

Highlights

  • Research on resting-state networks is attracting much attention in human neuroimaging

  • We investigated whether there is a model that simultaneously explains two experimentally observed phenomena in the resting state: slow fluctuation manifested by resting-state functional connectivity and fast transient dynamics manifested by EEG microstates

  • We simulated a neural mass model using the Larter-Breakspear model constrained by the structural connectivity and optimized the model parameters [the global coupling parameter and the local gain parameter] by fitting the simulated resting-state functional connectivity (rsFC) to the experimental rsFC and the simulated microstates to the experimental microstates

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Summary

Introduction

Research on resting-state networks is attracting much attention in human neuroimaging. Simultaneous fMRI and EEG measurements have been used to reveal the relationship between the slow fluctuation related to rsFC and the fast synchronization transition related to microstates in terms of the spatiotemporal dynamics of the human brain’s information processing (Britz et al, 2010; Van de Ville et al, 2010; Yuan et al, 2012; Schwab et al, 2015; Bréchet et al, 2019). Roberts et al showed that the Larter-Breakspear model (SanzLeon et al, 2015) constrained by the connectome generated rich repertoires of rapidly changing spatiotemporal patterns that are in agreement with the temporal statistics of experimental data such as electrical waves in cortical tissue, sequential spatiotemporal patterns in the resting state MEG data, and largescale waves in human electrocorticography as well as static rsFC (Roberts et al, 2019). Similarities between experimental and simulated fast-transient spatial patterns have not yet been investigated

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