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The dynamics of resting fluctuations in the brain: metastability and its dynamical cortical core

Abstract : In the human brain, spontaneous activity during resting state consists of rapid transitions between functional network states over time but the underlying mechanisms are not understood. We use connectome based computational brain network modeling to reveal fundamental principles of how the human brain generates large-scale activity observable by noninvasive neuroimaging. We used structural and functional neuroimaging data to construct whole-brain models. With this novel approach, we reveal that the human brain during resting state operates at maximum metastability, i.e. in a state of maximum network switching. In addition, we investigate cortical heterogeneity across areas. Optimization of the spectral characteristics of each local brain region revealed the dynamical cortical core of the human brain, which is driving the activity of the rest of the whole brain. Brain network modelling goes beyond correlational neuroimaging analysis and reveals non-trivial network mechanisms underlying non-invasive observations. Our novel findings significantly pertain to the important role of computational connectomics in understanding principles of brain function. "When we take a general view of the wonderful stream of our consciousness, what strikes us first is the different pace of its parts. Like a bird's life, it seems to be made of an alternation of flights and perchings. " William James 1 Survival remains the perhaps most important problem faced by brains and a key challenge is how to segregate and integrate relevant information over different timescales when faced with hostile, often constantly changing environments 2. Reconciling different speeds of information processing, from fast to slow, is especially important, and could be key to the relative evolutionary success of mammals whose sophisticated brains are able to combine prior information from past memories with current stimuli to predict the future and to adapt behaviour accordingly 3-5. This was recognized well over a century ago by William James, generally acknowledged as one of the fathers of modern cognitive psychology 1. Speaking of this problem using the apt metaphor of the stream of consciousness, James noted that there is a different pace to its parts, comparing it to the life of a bird whose journey consists of an "alternation of flights and perchings". In the language of today's dynamical systems, the flights are akin to fast, segregative tendencies and the perchings to slower, integrative tendencies of the dynamic brain in action 2, 6, 7. In addition, motivated by recent experimental and modelling work of other labs 8, 9 , we investigate cortical heterogeneity across areas. By optimizing the spectral characteristics of each local brain node (in the coupled network),
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Gustavo Deco, Morten Kringelbach, Viktor Jirsa, Petra Ritter. The dynamics of resting fluctuations in the brain: metastability and its dynamical cortical core. Scientific Reports, Nature Publishing Group, 2017, 7, ⟨10.1038/s41598-017-03073-5⟩. ⟨hal-03246113⟩

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