Understanding the origin, nature and functional significance of complex patterns of neural activity, as recorded by diverse electrophysiological and neuroimaging techniques, is a central challenge in Neuroscience. Such patterns include collective oscillations, emerging out of neural synchronization, as well as highly-heterogeneous outbursts of activity interspersed by periods of quiescence, called "neuronal avalanches". Much debate has been generated about the possible scale-invariance or criticality of such avalanches, and its relevance for brain function. Aimed at shedding light onto this, here we analyze the large-scale collective properties of the cortex by using a mesoscopic approach, following the principle of parsimony of Landau-Ginzburg. Our model is similar to that of Wilson-Cowan for neural dynamics but, crucially, including stochasticity and space; synaptic plasticity and inhibition are considered as possible regulatory mechanisms. Detailed analyses uncover a phase diagram including down-states, synchronous, asynchronous, and up-state phases, and reveal that empirical findings for neuronal avalanches are consistently reproduced by tuning our model to the edge of synchronization. This reveals that the putative criticality of cortical dynamics does not correspond to a quiescent-to-active phase transition, as usually assumed in theoretical approaches, but to a synchronization phase transition, at which incipient oscillations and scalefree avalanches coexist. Furthermore, our model also accounts for up and down states as they occur, e.g. during deep sleep. The present approach constitutes a framework to rationalize the possible collective phases and phase transitions of cortical networks in simple terms, thus helping shed light into basic aspects of brain functioning from a very broad perspective.Cortical dynamics | Neuronal avalanches | Criticality | Synaptic plasticity T he cerebral cortex exhibits spontaneous activity even in the absence of any task or external stimuli (1-3). A salient aspect of this, so-called, resting-state dynamics, as revealed by in vivo and in vitro measurements, is that it exhibits outbursts of electrochemical activity, characterized by brief episodes of coherence -during which many neurons fire within a narrow time window-interspaced by periods of relative quiescence, giving rise to collective oscillatory rhythms (4, 5). Shedding light on the origin, nature, and functional meaning of such an intricate dynamics is a fundamental challenge in Neuroscience (6).Upon experimentally enhancing the spatio-temporal resolution of activity recordings, Beggs and Plenz made the remarkable finding that, actually, synchronized outbursts of neural activity could be decomposed into complex spatio-temporal patterns, thereon named "neuronal avalanches" (7). The sizes and durations of such avalanches were reported to be distributed as power-laws, i.e. to be organized in a scale-free way, limited only by network size (7). Furthermore, they obey finite-size scaling (8), a trademark of scale invariance...
The spontaneous emergence of coherent behavior through synchronization plays a key role in neural function, and its anomalies often lie at the basis of pathologies. Here we employ a parsimonious (mesoscopic) approach to study analytically and computationally the synchronization (Kuramoto) dynamics on the actual human-brain connectome network. We elucidate the existence of a so-far-uncovered intermediate phase, placed between the standard synchronous and asynchronous phases, i.e. between order and disorder. This novel phase stems from the hierarchical modular organization of the connectome. Where one would expect a hierarchical synchronization process, we show that the interplay between structural bottlenecks and quenched intrinsic frequency heterogeneities at many different scales, gives rise to frustrated synchronization, metastability, and chimera-like states, resulting in a very rich and complex phenomenology. We uncover the origin of the dynamic freezing behind these features by using spectral graph theory and discuss how the emerging complex synchronization patterns relate to the need for the brain to access –in a robust though flexible way– a large variety of functional attractors and dynamical repertoires without ad hoc fine-tuning to a critical point.
We revisit the problem of deriving the mean-field values of avalanche exponents in systems with absorbing states. These are well known to coincide with those of unbiased branching processes. Here we show that for at least four different universality classes (directed percolation, dynamical percolation, the voter model or compact directed percolation class, and the Manna class of stochastic sandpiles) this common result can be obtained by mapping the corresponding Langevin equations describing each of them into a random walker confined to the origin by a logarithmic potential. We report on the emergence of nonuniversal continuously varying exponent values stemming from the presence of small external driving - that might induce avalanche merging - that, to the best of our knowledge, has not been noticed in the past. Many of the other results derived here appear in the literature as independently derived for individual universality classes or for the branching process itself. Still, we believe that a simple and unified perspective as the one presented here can help (1) clarify the overall picture, (2) underline the superuniversality of the behavior as well as the dependence on external driving, and (3) avoid the common existing confusion between unbiased branching processes (equivalent to a random walker in a balanced logarithmic potential) and standard (unconfined) random walkers.
Avalanches whose sizes and durations are distributed as power laws appear in many contexts, from physics to geophysics and biology. Here, we show that there is a hidden peril in thresholding continuous times series -either from empirical or synthetic data-for the identification of avalanches. In particular, we consider two possible alternative definitions of avalanche size used e.g. in the empirical determination of avalanche exponents in the analysis of neural-activity data. By performing analytical and computational studies of an Ornstein-Uhlenbeck process (taken as a guiding example) we show that (i) if relatively large threshold values are employed to determine the beginning and ending of avalanches and (ii) if -as sometimes done in the literature-avalanche sizes are defined as the total area (above zero) of the avalanche, then true asymptotic scaling behavior is not seen, instead the observations are dominated by transient effects. This problem -that we have detected in some recent works-leads to misinterpretations of the resulting scaling regimes.
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