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

被引:221
作者
Cabral, Joana [1 ,2 ]
Luckhoo, Henry [3 ,4 ]
Woolrich, Mark [3 ]
Joensson, Morten [2 ,5 ]
Mohseni, Hamid [2 ]
Baker, Adam [3 ,4 ]
Kringelbach, Morten L. [2 ,5 ]
Deco, Gustavo [1 ,6 ]
机构
[1] Univ Pompeu Fabra, Ctr Brain & Cognit, Theoret & Computat Neurosci Grp, Barcelona 08018, Spain
[2] Univ Oxford, Dept Psychiat, Oxford OX3 7JX, England
[3] Univ Oxford, Oxford Ctr Human Brain Act, Oxford OX3 7JX, England
[4] Univ Oxford, Dept Engn Sci, Inst Biomed Engn, Ctr Doctoral Training Healthcare Innovat, Oxford OX1 3PJ, England
[5] Aarhus Univ, CFIN MindLab, DK-8000 Aarhus, Denmark
[6] Inst Catalana Recerca & Estudis Avancats, Barcelona 08010, Spain
关键词
Resting state; MEG; Oscillations; Network; Kuramoto; Modeling; Structural connectivity; Functional connectivity; RESTING-STATE NETWORKS; KURAMOTO MODEL; BRAIN ACTIVITY; ALPHA-RHYTHM; DYNAMICS; FMRI; SYNCHRONIZATION; FLUCTUATIONS; CORTEX; EEG;
D O I
10.1016/j.neuroimage.2013.11.047
中图分类号
Q189 [神经科学];
学科分类号
071006 [神经生物学];
摘要
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. (C) 2013 The Authors. Published by Elsevier Inc. All rights reserved.
引用
收藏
页码:423 / 435
页数:13
相关论文
共 72 条
[1]
The Kuramoto model:: A simple paradigm for synchronization phenomena [J].
Acebrón, JA ;
Bonilla, LL ;
Vicente, CJP ;
Ritort, F ;
Spigler, R .
REVIEWS OF MODERN PHYSICS, 2005, 77 (01) :137-185
[2]
[Anonymous], 1998, Recent Advances in Biomagnetism
[3]
HOW DELAYS AFFECT NEURAL DYNAMICS AND LEARNING [J].
BALDI, P ;
ATIYA, AF .
IEEE TRANSACTIONS ON NEURAL NETWORKS, 1994, 5 (04) :612-621
[4]
Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks [J].
Bartos, Marlene ;
Vida, Imre ;
Jonas, Peter .
NATURE REVIEWS NEUROSCIENCE, 2007, 8 (01) :45-56
[5]
Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? [J].
Behrens, T. E. J. ;
Berg, H. Johansen ;
Jbabdi, S. ;
Rushworth, M. F. S. ;
Woolrich, M. W. .
NEUROIMAGE, 2007, 34 (01) :144-155
[6]
Characterization and propagation of uncertainty in diffusion-weighted MR imaging [J].
Behrens, TEJ ;
Woolrich, MW ;
Jenkinson, M ;
Johansen-Berg, H ;
Nunes, RG ;
Clare, S ;
Matthews, PM ;
Brady, JM ;
Smith, SM .
MAGNETIC RESONANCE IN MEDICINE, 2003, 50 (05) :1077-1088
[7]
FUNCTIONAL CONNECTIVITY IN THE MOTOR CORTEX OF RESTING HUMAN BRAIN USING ECHO-PLANAR MRI [J].
BISWAL, B ;
YETKIN, FZ ;
HAUGHTON, VM ;
HYDE, JS .
MAGNETIC RESONANCE IN MEDICINE, 1995, 34 (04) :537-541
[8]
Toward discovery science of human brain function [J].
Biswal, Bharat B. ;
Mennes, Maarten ;
Zuo, Xi-Nian ;
Gohel, Suril ;
Kelly, Clare ;
Smith, Steve M. ;
Beckmann, Christian F. ;
Adelstein, Jonathan S. ;
Buckner, Randy L. ;
Colcombe, Stan ;
Dogonowski, Anne-Marie ;
Ernst, Monique ;
Fair, Damien ;
Hampson, Michelle ;
Hoptman, Matthew J. ;
Hyde, James S. ;
Kiviniemi, Vesa J. ;
Kotter, Rolf ;
Li, Shi-Jiang ;
Lin, Ching-Po ;
Lowe, Mark J. ;
Mackay, Clare ;
Madden, David J. ;
Madsen, Kristoffer H. ;
Margulies, Daniel S. ;
Mayberg, Helen S. ;
McMahon, Katie ;
Monk, Christopher S. ;
Mostofsky, Stewart H. ;
Nagel, Bonnie J. ;
Pekar, James J. ;
Peltier, Scott J. ;
Petersen, Steven E. ;
Riedl, Valentin ;
Rombouts, Serge A. R. B. ;
Rypma, Bart ;
Schlaggar, Bradley L. ;
Schmidt, Sein ;
Seidler, Rachael D. ;
Siegle, Greg J. ;
Sorg, Christian ;
Teng, Gao-Jun ;
Veijola, Juha ;
Villringer, Arno ;
Walter, Martin ;
Wang, Lihong ;
Weng, Xu-Chu ;
Whitfield-Gabrieli, Susan ;
Williamson, Peter ;
Windischberger, Christian .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2010, 107 (10) :4734-4739
[9]
Synchronization in networks of excitatory and inhibitory neurons with sparse, random connectivity [J].
Börgers, C ;
Kopell, N .
NEURAL COMPUTATION, 2003, 15 (03) :509-538
[10]
Generative models of cortical oscillations: neurobiological implications of the Kuramoto model [J].
Breakspear, Michael ;
Heitmann, Stewart ;
Daffertshofer, Andreas .
FRONTIERS IN HUMAN NEUROSCIENCE, 2010, 4