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Broken detailed balance and entropy production in the human brain

Christopher W. Lynn,E. Cornblath,Lia Papadopoulos,Maxwell A. Bertolero,D. Bassett

Published 2020 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance To perform biological functions, living systems must break detailed balance by consuming energy and producing entropy. At microscopic scales, broken detailed balance enables a suite of molecular and cellular functions, including computations, kinetic proofreading, sensing, adaptation, and transportation. But do macroscopic violations of detailed balance enable higher-order biological functions, such as cognition and movement? To answer this question, we adapt tools from nonequilibrium statistical mechanics to quantify broken detailed balance in complex living systems. Analyzing neural recordings from hundreds of human subjects, we find that the brain violates detailed balance at large scales and that these violations increase with physical and cognitive exertion. Generally, we provide a flexible framework for investigating broken detailed balance at large scales in complex systems. Living systems break detailed balance at small scales, consuming energy and producing entropy in the environment to perform molecular and cellular functions. However, it remains unclear how broken detailed balance manifests at macroscopic scales and how such dynamics support higher-order biological functions. Here we present a framework to quantify broken detailed balance by measuring entropy production in macroscopic systems. We apply our method to the human brain, an organ whose immense metabolic consumption drives a diverse range of cognitive functions. Using whole-brain imaging data, we demonstrate that the brain nearly obeys detailed balance when at rest, but strongly breaks detailed balance when performing physically and cognitively demanding tasks. Using a dynamic Ising model, we show that these large-scale violations of detailed balance can emerge from fine-scale asymmetries in the interactions between elements, a known feature of neural systems. Together, these results suggest that violations of detailed balance are vital for cognition and provide a general tool for quantifying entropy production in macroscopic systems.

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