Normalized Connectomes Show Increased Synchronizability with Age through Their Second Largest Eigenvalue

The synchronization of different brain regions is widely observed under both normal and pathological conditions such as epilepsy. However, the relationship between the dynamics of these brain regions, the connectivity between them, and the ability to synchronize remains an open question. We investigated the problem of inter-region synchronization in networks of Wilson-Cowan/Neural field equations with homeostatic plasticity, each of which acts as a model for an isolated brain region. We considered arbitrary connection profiles with only one constraint: the rows of the connection matrices are all identically normalized. We found that these systems often synchronize to the solution obtained from a single, self-coupled neural region. We analyze the stability of this solution through a straightforward modification of the Master Stability Function (MSF) approach and found that synchronized solutions lose stability for connectivity matrices when the second largest positive eigenvalue is sufficiently large, for values of the global coupling parameter that are not too large. This result was numerically confirmed for ring systems and lattices and was also robust to small amounts of heterogeneity in the homeostatic set points in each node. Finally, we tested this result on connectomes obtained from 196 subjects over a broad age range (4-85 years) from the Human Connectome Project. We found that the second largest eigenvalue tended to decrease with age, indicating an increase in synchronizability that may be related to the increased prevalence of epilepsy with old age.

[1]  M. Breakspear Dynamic models of large-scale brain activity , 2017, Nature Neuroscience.

[2]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[3]  J. M. Buldú,et al.  Brain synchronizability, a false friend , 2018, NeuroImage.

[4]  Bard Ermentrout,et al.  Bifurcations of Stationary Solutions in an Interacting Pair of E-I Neural Fields , 2012, SIAM J. Appl. Dyn. Syst..

[5]  Mauricio Barahona,et al.  Emergence of Slow-Switching Assemblies in Structured Neuronal Networks , 2015, PLoS Comput. Biol..

[6]  Stephen Coombes,et al.  Large-scale neural dynamics: Simple and complex , 2010, NeuroImage.

[7]  A. Wolf,et al.  Determining Lyapunov exponents from a time series , 1985 .

[8]  Menahem Segal,et al.  Dendritic spines shaped by synaptic activity , 2000, Current Opinion in Neurobiology.

[9]  Danielle S Bassett,et al.  Developmental increases in white matter network controllability support a growing diversity of brain dynamics , 2016, Nature Communications.

[10]  Adilson E Motter,et al.  Network synchronization landscape reveals compensatory structures, quantization, and the positive effect of negative interactions , 2009, Proceedings of the National Academy of Sciences.

[11]  Timothy E. J. Behrens,et al.  Human connectomics , 2012, Current Opinion in Neurobiology.

[12]  Rafael Yuste,et al.  Spine Motility Phenomenology, Mechanisms, and Function , 2002, Neuron.

[13]  B. Ermentrout Neural networks as spatio-temporal pattern-forming systems , 1998 .

[14]  Anita E. Bandrowski,et al.  The UCLA multimodal connectivity database: a web-based platform for brain connectivity matrix sharing and analysis , 2012, Front. Neuroinform..

[15]  E. Beghi,et al.  Aging and the Epidemiology of Epilepsy , 2018, Neuroepidemiology.

[16]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[17]  Wilten Nicola,et al.  Chaos in homeostatically regulated neural systems. , 2018, Chaos.

[18]  Joshua C. Brumberg,et al.  A quantitative population model of whisker barrels: Re-examining the Wilson-Cowan equations , 1996, Journal of Computational Neuroscience.

[19]  Claudia Clopath,et al.  Local inhibitory plasticity tunes macroscopic brain dynamics and allows the emergence of functional brain networks , 2016, NeuroImage.

[20]  Youngmin Park,et al.  Scalar Reduction of a Neural Field Model with Spike Frequency Adaptation , 2018, SIAM J. Appl. Dyn. Syst..

[21]  T. Carroll,et al.  Master Stability Functions for Synchronized Coupled Systems , 1998 .

[22]  Elwood S. Buffa,et al.  Graph Theory with Applications , 1977 .

[23]  Zachary P. Kilpatrick,et al.  Wandering Bumps in Stochastic Neural Fields , 2012, SIAM J. Appl. Dyn. Syst..

[24]  Henning Sprekeler,et al.  Inhibitory Plasticity Balances Excitation and Inhibition in Sensory Pathways and Memory Networks , 2011, Science.

[25]  Gary W. Mathern,et al.  Basic research in epilepsy and aging , 2006, Epilepsy Research.

[26]  Paul C Bressloff,et al.  Stochastic neural field model of stimulus-dependent variability in cortical neurons , 2019, bioRxiv.

[27]  Olaf Sporns,et al.  Comparative Connectomics , 2016, Trends in Cognitive Sciences.