Self-Organized Criticality in the Brain

Abstract

Self-organized criticality (SOC) refers to the ability of complex systems to evolve toward a second-order phase transition at which interactions between system components lead to scale-invariant events that are beneficial for system performance. For the last two decades, considerable experimental evidence has accumulated that the mammalian cortex with its diversity in cell types, interconnectivity, and plasticity might exhibit SOC. Here, we review the experimental findings of isolated, layered cortex preparations to self-organize toward four dynamical motifs presently identified in the intact cortex in vivo: up-states, oscillations, neuronal avalanches, and coherence potentials. During up-states, the synchronization observed for nested theta/gamma oscillations embeds scale-invariant neuronal avalanches, which can be identified by robust power law scaling in avalanche sizes with a slope of −3/2 and a critical branching parameter of 1. This precise dynamical coordination, tracked in the negative transients of the local field potential (nLFP) and spiking activity of pyramidal neurons using two-photon imaging, emerges autonomously in superficial layers of organotypic cortex cultures and acute cortex slices, is homeostatically regulated, exhibits separation of time scales, and reveals unique size vs. quiet time dependencies. A subclass of avalanches, the coherence potentials, exhibits precise maintenance of the time course in propagated local synchrony. Avalanches emerge in superficial layers of the cortex under conditions of strong external drive. The balance of excitation and inhibition (E/I), as well as neuromodulators such as dopamine, establishes powerful control parameters for avalanche dynamics. This rich dynamical repertoire is not observed in dissociated cortex cultures, which lack the differentiation into cortical layers and exhibit a dynamical phenotype expected for a first-order phase transition. The precise interactions between up-states, nested oscillations, and avalanches in superficial layers of the cortex provide compelling evidence for SOC in the brain.

Studying the developing brain in real-world contexts: moving from castles in the air to castles on the ground.

“…Research with adults has also examined the differences in the energetic state of the brain between a resting and an attentive state. Generally, the resting state is associated with nearcritical dynamics, in which a high dynamic range and a large repertoire of brain states may be advantageous; whereas, a task-active (attentive) state induces subcritical dynamics, which is associated with a lower dynamic range, which in turn may reduce elements of interference affecting task performance (Fagerholm et al, 2015;Hellyer et al, 2014;Lynn et al, 2021;Plenz et al, 2021). According to the free energy minimisation principle, biological systems must resist the second law of thermodynamics (i.e., a tendency to disorder), so that they do not decay to equilibrium (K. Friston, 2010; K. J.…”

Self-Organised Critical Dynamics as a Key to Fundamental Features of Complexity in Physical, Biological, and Social Networks

“…The role of such complex topologies in brain dynamics was pointed out [64]. Even though the brain data increasingly confirm the evidence of SOC, understanding the precise role of brain criticality remains a challenging question [65,66]. The underlying dilemma, as pointed out in a recent perspective paper [65], is whether the primary cause for the brain criticality lies in the demand of its robustness or improved functionality, both of which are compatible with SOC states.…”

Toward a Unified Analysis of the Brain Criticality Hypothesis: Reviewing Several Available Tools

“…There are quite a few excellent reviews regarding the subject of brain criticality by now (see e.g., Wilting et al, 2018 ; Wilting and Priesemann, 2019a ; Plenz et al, 2021 ; Zeraati et al, 2021 ). But the field is full of controversies and clearly lacks a standardization.…”