Universal organization of resting brain activity at the thermodynamic critical point

Shan Yu,Hongdian Yang,Oren Shriki,Dietmar Plenz

doi:10.3389/fnsys.2013.00042

Abstract

Thermodynamic criticality describes emergent phenomena in a wide variety of complex systems. In the mammalian cortex, one type of complex dynamics that spontaneously emerges from neuronal interactions has been characterized as neuronal avalanches. Several aspects of neuronal avalanches such as their size and life time distributions are described by power laws with unique exponents, indicating an underlying critical branching process that governs avalanche formation. Here, we show that neuronal avalanches also reflect an organization of brain dynamics close to a thermodynamic critical point. We recorded spontaneous cortical activity in monkeys and humans at rest using high-density intracranial microelectrode arrays and magnetoencephalography, respectively. By numerically changing a control parameter equivalent to thermodynamic temperature, we observed typical critical behavior in cortical activities near the actual physiological condition, including the phase transition of an order parameter, as well as the divergence of susceptibility and specific heat. Finite-size scaling of these quantities allowed us to derive robust critical exponents highly consistent across monkey and humans that uncover a distinct, yet universal organization of brain dynamics. Our results demonstrate that normal brain dynamics at rest resides near or at criticality, which maximizes several aspects of information processing such as input sensitivity and dynamic range.

Highlights

Thermodynamic criticality describes emergent phenomena in a wide variety of complex systems
Significant negative local field potential deflections, which indicate synchronized activity of local neuronal populations (Petermann et al, 2009; Yu et al, 2011), were detected using an amplitude threshold of –2.5 SDs of the LOCAL FIELD POTENTIAL (LFP) calculated for each electrode (Figure 1B)
This power-law demonstrates that ongoing cortical activity at rest in awake monkeys organizes as neuronal avalanches (Beggs and Plenz, 2003; Petermann et al, 2009)

Summary

Introduction

Thermodynamic criticality describes emergent phenomena in a wide variety of complex systems. Such balanced interactions poise the system at a transition between two contrasting phases (quantified by the order parameter, M) and give rise to a number of non-trivial emergent properties, including the divergence of the sensitivity to external perturbations (quantified by the susceptibility, χ), and internal complexity/diversity (quantified by the specific heat, C; Stanley, 1987; Binney et al, 1992; Sornette, 2006) For the cortex, these quantities have intuitive meanings in terms of neuronal information processing. Recent studies of neuronal avalanches strongly suggest that neuronal interactions, both at the mesoscopic scale

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Discussion

Conclusion