Dynamic changes in network synchrony reveal resting-state functional networks.

Experimental functional magnetic resonance imaging studies have shown that spontaneous brain activity, i.e., in the absence of any external input, exhibit complex spatial and temporal patterns of co-activity between segregated brain regions. These so-called large-scale resting-state functional connectivity networks represent dynamically organized neural assemblies interacting with each other in a complex way. It has been suggested that looking at the dynamical properties of complex patterns of brain functional co-activity may reveal neural mechanisms underlying the dynamic changes in functional interactions. Here, we examine how global network dynamics is shaped by different network configurations, derived from realistic brain functional interactions. We focus on two main dynamics measures: synchrony and variations in synchrony. Neural activity and the inferred hemodynamic response of the network nodes are simulated using a system of 90 FitzHugh-Nagumo neural models subject to system noise and time-delayed interactions. These models are embedded into the topology of the complex brain functional interactions, whose architecture is additionally reduced to its main structural pathways. In the simulated functional networks, patterns of correlated regional activity clearly arise from dynamical properties that maximize synchrony and variations in synchrony. Our results on the fast changes of the level of the network synchrony also show how flexible changes in the large-scale network dynamics could be.

[1]  G. Deco,et al.  Ongoing Cortical Activity at Rest: Criticality, Multistability, and Ghost Attractors , 2012, The Journal of Neuroscience.

[2]  M. Shanahan Metastable chimera states in community-structured oscillator networks. , 2009, Chaos.

[3]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

[4]  L. Shampine,et al.  Solving DDEs in MATLAB , 2001 .

[5]  Andreas Daffertshofer,et al.  Generative Models of Cortical Oscillations: Neurobiological Implications of the Kuramoto Model , 2010, Front. Hum. Neurosci..

[6]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[7]  O. Sporns,et al.  The economy of brain network organization , 2012, Nature Reviews Neuroscience.

[8]  Gustavo Deco,et al.  Structural connectivity in schizophrenia and its impact on the dynamics of spontaneous functional networks. , 2013, Chaos.

[9]  Vito Latora,et al.  Remote synchronization reveals network symmetries and functional modules. , 2012, Physical review letters.

[10]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[11]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[12]  S. Strogatz From Kuramoto to Crawford: exploring the onset of synchronization in populations of coupled oscillators , 2000 .

[13]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[14]  Lester Melie-García,et al.  Studying the human brain anatomical network via diffusion-weighted MRI and Graph Theory , 2008, NeuroImage.

[15]  R. Kötter,et al.  Cortical network dynamics with time delays reveals functional connectivity in the resting brain , 2008, Cognitive Neurodynamics.

[16]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[17]  Daniel S. Margulies,et al.  Mapping the functional connectivity of anterior cingulate cortex , 2007, NeuroImage.

[18]  E. Izhikevich Weakly Coupled Oscillators , 2006 .

[19]  Peter J Hellyer,et al.  The Control of Global Brain Dynamics: Opposing Actions of Frontoparietal Control and Default Mode Networks on Attention , 2014, The Journal of Neuroscience.

[20]  Gustavo Deco,et al.  Using the Virtual Brain to Reveal the Role of Oscillations and Plasticity in Shaping Brain's Dynamical Landscape , 2014, Brain Connect..

[21]  L. Shampine,et al.  A 3(2) pair of Runge - Kutta formulas , 1989 .

[22]  Anil K. Seth,et al.  Granger causality analysis of fMRI BOLD signals is invariant to hemodynamic convolution but not downsampling , 2013, NeuroImage.

[23]  V. Flunkert,et al.  Pydelay - a python tool for solving delay differential equations , 2009 .

[24]  Le Hoa Nguyen,et al.  Synchronization of coupled chaotic FitzHugh-Nagumo neurons via Lyapunov functions , 2011, Math. Comput. Simul..

[25]  O. Sporns,et al.  Key role of coupling, delay, and noise in resting brain fluctuations , 2009, Proceedings of the National Academy of Sciences.

[26]  Jürgen Kurths,et al.  Synchronization: Phase locking and frequency entrainment , 2001 .

[27]  J. Kelso,et al.  The Metastable Brain , 2014, Neuron.

[28]  Karl J. Friston,et al.  Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics , 2000, NeuroImage.

[29]  Gustavo Deco,et al.  How anatomy shapes dynamics: a semi-analytical study of the brain at rest by a simple spin model , 2012, Front. Comput. Neurosci..

[30]  Andreas Daffertshofer,et al.  Comparing Brain Networks of Different Size and Connectivity Density Using Graph Theory , 2010, PloS one.

[31]  Danielle S Bassett,et al.  Cross-linked structure of network evolution. , 2013, Chaos.

[32]  Philipp Hövel,et al.  Functional connectivity of distant cortical regions: Role of remote synchronization and symmetry in interactions , 2014, NeuroImage.

[33]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[34]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[35]  David K Campbell,et al.  Editorial: The pre-history of Chaos-An Interdisciplinary Journal of Nonlinear Science. , 2015, Chaos.

[36]  Viktor K. Jirsa,et al.  Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire , 2008, PLoS Comput. Biol..

[37]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[38]  Murray Shanahan,et al.  Metastability and chimera states in modular delay and pulse-coupled oscillator networks. , 2012, Chaos.

[39]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[40]  Philipp Hövel,et al.  Synchronization of Coupled Neural oscillators with Heterogeneous delays , 2012, Int. J. Bifurc. Chaos.

[41]  Philipp Hövel,et al.  When nonlocal coupling between oscillators becomes stronger: patched synchrony or multichimera states. , 2012, Physical review letters.

[42]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[43]  Morten L. Kringelbach,et al.  Exploring the network dynamics underlying brain activity during rest , 2014, Progress in Neurobiology.

[44]  Morten L. Kringelbach,et al.  Modeling the outcome of structural disconnection on resting-state functional connectivity , 2012, NeuroImage.

[45]  Valentin Flunkert,et al.  Pydelay: A Simulation Package , 2011 .

[46]  Gustavo Deco,et al.  Role of local network oscillations in resting-state functional connectivity , 2011, NeuroImage.