Landau–Ginzburg theory of cortex dynamics: Scale-free avalanches emerge at the edge of synchronization

Abstract

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, includes stochasticity and space; synaptic plasticity and inhibition are considered as possible regulatory mechanisms. Detailed analyses uncover a phase diagram including down-state, 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 scale-free avalanches coexist. Furthermore, our model also accounts for up and down states as they occur (e.g., during deep sleep). This approach constitutes a framework to rationalize the possible collective phases and phase transitions of cortical networks in simple terms, thus helping to shed light on basic aspects of brain functioning from a very broad perspective.