Broken detailed balance and entropy production in the human brain

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...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 118; no. 47; pp. 1 - 7
Main Authors Lynn, Christopher W., Cornblath, Eli J., Papadopoulos, Lia, Bertolero, Maxwell A., Bassett, Danielle S.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 23.11.2021
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Summary: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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Author contributions: C.W.L. and D.S.B. designed research; C.W.L. performed research; C.W.L., E.J.C., and L.P. contributed new reagents/analytic tools; C.W.L. and M.A.B. analyzed data; and C.W.L. and D.S.B. wrote the paper.
Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved October 11, 2021 (received for review May 28, 2021)
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2109889118