Exploring mechanisms of spontaneous functional connectivity in MEG: How delayed network interactions lead to structured amplitude envelopes of band-pass filtered oscillations

Joana Cabral; Henry Luckhoo; Mark W. Woolrich; Morten Joensson; Hamid Mohseni; Adam Baker; Morten L. Kringelbach; Gustavo Deco

doi:10.1016/j.neuroimage.2013.11.047

Exploring mechanisms of spontaneous functional connectivity in MEG: How delayed network interactions lead to structured amplitude envelopes of band-pass filtered oscillations

Joana Cabral, Henry Luckhoo, Mark W. Woolrich, Morten Joensson, Hamid Mohseni, Adam Baker, Morten L. Kringelbach, Gustavo Deco

Research output: Contribution to journal › Article › Research › peer-review

172 Citations (Scopus)

Abstract

Spontaneous (or resting. state) brain activity has attracted a growing body of neuroimaging research over the last decades. Whole-brain network models have proved helpful to investigate the source of slow (<. 0.1. Hz) correlated hemodynamic fluctuations revealed in fMRI during rest. However, the mechanisms mediating resting-state long-distance correlations and the relationship with the faster neural activity remain unclear. Novel insights coming from MEG studies have shown that the amplitude envelopes of alpha- and beta-frequency oscillations (~. 8-30. Hz) display similar correlation patterns as the fMRI signals.In this work, we combine experimental and theoretical work to investigate the mechanisms of spontaneous MEG functional connectivity. Using a simple model of coupled oscillators adapted to incorporate realistic whole-brain connectivity and conduction delays, we explore how slow and structured amplitude envelopes of band-pass filtered signals - fairly reproducing MEG data collected from 10 healthy subjects at rest - are generated spontaneously in the space-time structure of the brain network.Our simulation results show that the large-scale neuroanatomical connectivity provides an optimal network structure to support a regime with metastable synchronization. In this regime, different subsystems may temporarily synchronize at reduced collective frequencies (falling in the 8-30. Hz range due to the delays) while the global system never fully synchronizes. This mechanism modulates the frequency of the oscillators on a slow time-scale (<. 0.1. Hz) leading to structured amplitude fluctuations of band-pass filtered signals. Taken overall, our results reveal that the structured amplitude envelope fluctuations observed in resting-state MEG data may originate from spontaneous synchronization mechanisms naturally occurring in the space-time structure of the brain.

Original language	English
Pages (from-to)	423-435
Number of pages	13
Journal	NeuroImage
Volume	90
DOIs	https://doi.org/10.1016/j.neuroimage.2013.11.047
Publication status	Published - 15 Apr 2014
Externally published	Yes

Keywords

Functional connectivity
Kuramoto
MEG
Modeling
Network
Oscillations
Resting state
Structural connectivity

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title = "Exploring mechanisms of spontaneous functional connectivity in MEG: How delayed network interactions lead to structured amplitude envelopes of band-pass filtered oscillations",

abstract = "Spontaneous (or resting. state) brain activity has attracted a growing body of neuroimaging research over the last decades. Whole-brain network models have proved helpful to investigate the source of slow (<. 0.1. Hz) correlated hemodynamic fluctuations revealed in fMRI during rest. However, the mechanisms mediating resting-state long-distance correlations and the relationship with the faster neural activity remain unclear. Novel insights coming from MEG studies have shown that the amplitude envelopes of alpha- and beta-frequency oscillations (~. 8-30. Hz) display similar correlation patterns as the fMRI signals.In this work, we combine experimental and theoretical work to investigate the mechanisms of spontaneous MEG functional connectivity. Using a simple model of coupled oscillators adapted to incorporate realistic whole-brain connectivity and conduction delays, we explore how slow and structured amplitude envelopes of band-pass filtered signals - fairly reproducing MEG data collected from 10 healthy subjects at rest - are generated spontaneously in the space-time structure of the brain network.Our simulation results show that the large-scale neuroanatomical connectivity provides an optimal network structure to support a regime with metastable synchronization. In this regime, different subsystems may temporarily synchronize at reduced collective frequencies (falling in the 8-30. Hz range due to the delays) while the global system never fully synchronizes. This mechanism modulates the frequency of the oscillators on a slow time-scale (<. 0.1. Hz) leading to structured amplitude fluctuations of band-pass filtered signals. Taken overall, our results reveal that the structured amplitude envelope fluctuations observed in resting-state MEG data may originate from spontaneous synchronization mechanisms naturally occurring in the space-time structure of the brain.",

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author = "Joana Cabral and Henry Luckhoo and Woolrich, {Mark W.} and Morten Joensson and Hamid Mohseni and Adam Baker and Kringelbach, {Morten L.} and Gustavo Deco",

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doi = "10.1016/j.neuroimage.2013.11.047",

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T2 - How delayed network interactions lead to structured amplitude envelopes of band-pass filtered oscillations

AU - Cabral, Joana

AU - Luckhoo, Henry

AU - Woolrich, Mark W.

AU - Joensson, Morten

AU - Mohseni, Hamid

AU - Baker, Adam

AU - Kringelbach, Morten L.

AU - Deco, Gustavo

PY - 2014/4/15

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AB - Spontaneous (or resting. state) brain activity has attracted a growing body of neuroimaging research over the last decades. Whole-brain network models have proved helpful to investigate the source of slow (<. 0.1. Hz) correlated hemodynamic fluctuations revealed in fMRI during rest. However, the mechanisms mediating resting-state long-distance correlations and the relationship with the faster neural activity remain unclear. Novel insights coming from MEG studies have shown that the amplitude envelopes of alpha- and beta-frequency oscillations (~. 8-30. Hz) display similar correlation patterns as the fMRI signals.In this work, we combine experimental and theoretical work to investigate the mechanisms of spontaneous MEG functional connectivity. Using a simple model of coupled oscillators adapted to incorporate realistic whole-brain connectivity and conduction delays, we explore how slow and structured amplitude envelopes of band-pass filtered signals - fairly reproducing MEG data collected from 10 healthy subjects at rest - are generated spontaneously in the space-time structure of the brain network.Our simulation results show that the large-scale neuroanatomical connectivity provides an optimal network structure to support a regime with metastable synchronization. In this regime, different subsystems may temporarily synchronize at reduced collective frequencies (falling in the 8-30. Hz range due to the delays) while the global system never fully synchronizes. This mechanism modulates the frequency of the oscillators on a slow time-scale (<. 0.1. Hz) leading to structured amplitude fluctuations of band-pass filtered signals. Taken overall, our results reveal that the structured amplitude envelope fluctuations observed in resting-state MEG data may originate from spontaneous synchronization mechanisms naturally occurring in the space-time structure of the brain.

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KW - Network

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JO - NeuroImage

JF - NeuroImage

SN - 1053-8119

ER -

Exploring mechanisms of spontaneous functional connectivity in MEG: How delayed network interactions lead to structured amplitude envelopes of band-pass filtered oscillations

Abstract

Keywords

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