Abstract

Spontaneous neural activities are endowed with specific patterning characterized by synchronizations within functionally relevant distant regions that are termed as resting-state networks (RSNs). Although the mechanisms that organize the large-scale neural systems are still largely unknown, recent studies have proposed a hypothesis that network-specific coactivations indeed emerge as the result of globally propagating neural activities with specific paths of transmission. However, the extent to which such a centralized global regulation, rather than network-specific control, contributes to the RSN synchronization remains unknown. In the present study, we investigated the contribution from each mechanism by directly identifying the global as well as local component of resting-state functional MRI (fMRI) data provided by human connectome project, using temporal independent component analysis (ICA). Based on the spatial distribution pattern, each ICA component was classified as global or local. Time lag mapping of each IC revealed several paths of global or semi-global propagations that are partially overlapping yet spatially distinct to each other. Consistent with previous studies, the time lag of global oscillation, although being less spatially homogenous than what was assumed to be, contributed to the RSN synchronization. However, an equivalent contribution was also shown on the part of the more locally confined activities that are independent to each other. While allowing the view that network-specific coactivation occurs as part of the sequences of global neural activities, these results further confirm an equally important role of the network-specific regulation for its coactivation, regardless of whether vascular artifacts contaminate the global component in fMRI measures.

Highlights

  • Once considered to be a noisy, stochastic process, spontaneous activity of the cortical neuron is understood to be by no means random but is endowed with specific patterning that reflects the functional architecture of the underlying network at the level of micro- or meso-circuits (Tsodyks et al, 1999; Kenet et al, 2003)

  • While conventional rs-functional MRI (fMRI) analyses based on seed-based correlation or independent component analysis (ICA) implicitly assume that the spatial distribution of the synchronous neural activity is temporally constant, animal studies have revealed that spontaneous neural activity is spatiotemporally structured, and propagating waves of activity have been recorded in a variety of species

  • Using synthetic time series embedded with the measured time lag structures of the rsfMRI data, Mitra et al (2015a) showed that the functional connectivity (FC) matrix representing the resting-state networks (RSNs) synchronization could be reconstructed to a fair approximation

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Summary

Introduction

Once considered to be a noisy, stochastic process, spontaneous activity of the cortical neuron is understood to be by no means random but is endowed with specific patterning that reflects the functional architecture of the underlying network at the level of micro- or meso-circuits (Tsodyks et al, 1999; Kenet et al, 2003). Using synthetic time series embedded with the measured time lag structures of the rsfMRI data, Mitra et al (2015a) showed that the functional connectivity (FC) matrix representing the RSN synchronization could be reconstructed to a fair approximation In support of this idea, a recent animal study showed that a global wave of spontaneous neuronal activity propagating across the networks contributes to within-network coactivations of the neurons that correspond to RSN synchronization (Matsui et al, 2016). In the respiratory central pattern generator of the mammals, rhythm generation is dependent on the endogenously oscillatory neurons that serve as pacemaker, as well as the pattern of synaptic connections within the network that forms a network pacemaker (hybrid pacemakernetwork mechanism) (Calabrese, 1998; Rybak et al, 2004, 2007; Sohal et al, 2006; Johnson et al, 2007)

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