Non-equilibrium whole-brain dynamics arise from pairwise interactions

Sebastian M. Geli; Christopher W. Lynn; Morten L. Kringelbach; Gustavo Deco; Yonatan Sanz Perl

doi:10.1016/j.xcrp.2025.102464

Non-equilibrium whole-brain dynamics arise from pairwise interactions

Sebastian M. Geli^*, Christopher W. Lynn, Morten L. Kringelbach, Gustavo Deco, Yonatan Sanz Perl^*

^*Corresponding author for this work

Department of Clinical Medicine - Center for Music In the Brain

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

The human brain is a complex system of multiple neural elements that interact at different orders (pairwise, triplets, etc.), displaying non-equilibrium processes from the neuronal scale to the whole-brain scale. Here, we study how non-equilibrium dynamics of large-scale brain activity is driven by the interaction of its constituent elements at different orders. We hypothesize that the interactions generating non-equilibrium dynamics at the macroscopic brain scale are typically pairwise, with higher-order dependences playing a diminishing role. By expanding the entropy production into a sequence of orders of interactions, we find that pairwise interactions contribute dominantly. In light of this finding, we demonstrate that it is possible to characterize non-equilibrium brain dynamics using the interactions of pairs of macroscopic brain regions rather than complex interactions involving three or more regions. Furthermore, we propose that the entropy production of pairs of brain regions is a sensitive indicator for characterizing task-induced brain states.

Original language	English
Article number	102464
Journal	Cell Reports Physical Science
Volume	6
Issue	3
ISSN	2666-3864
DOIs	https://doi.org/10.1016/j.xcrp.2025.102464
Publication status	Published - Mar 2025

Keywords

brain
entropy production
high-order interactions
non-equilibrium
thermodynamics

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title = "Non-equilibrium whole-brain dynamics arise from pairwise interactions",

abstract = "The human brain is a complex system of multiple neural elements that interact at different orders (pairwise, triplets, etc.), displaying non-equilibrium processes from the neuronal scale to the whole-brain scale. Here, we study how non-equilibrium dynamics of large-scale brain activity is driven by the interaction of its constituent elements at different orders. We hypothesize that the interactions generating non-equilibrium dynamics at the macroscopic brain scale are typically pairwise, with higher-order dependences playing a diminishing role. By expanding the entropy production into a sequence of orders of interactions, we find that pairwise interactions contribute dominantly. In light of this finding, we demonstrate that it is possible to characterize non-equilibrium brain dynamics using the interactions of pairs of macroscopic brain regions rather than complex interactions involving three or more regions. Furthermore, we propose that the entropy production of pairs of brain regions is a sensitive indicator for characterizing task-induced brain states.",

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author = "Geli, {Sebastian M.} and Lynn, {Christopher W.} and Kringelbach, {Morten L.} and Gustavo Deco and {Sanz Perl}, Yonatan",

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AU - Lynn, Christopher W.

AU - Kringelbach, Morten L.

AU - Deco, Gustavo

AU - Sanz Perl, Yonatan

PY - 2025/3

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N2 - The human brain is a complex system of multiple neural elements that interact at different orders (pairwise, triplets, etc.), displaying non-equilibrium processes from the neuronal scale to the whole-brain scale. Here, we study how non-equilibrium dynamics of large-scale brain activity is driven by the interaction of its constituent elements at different orders. We hypothesize that the interactions generating non-equilibrium dynamics at the macroscopic brain scale are typically pairwise, with higher-order dependences playing a diminishing role. By expanding the entropy production into a sequence of orders of interactions, we find that pairwise interactions contribute dominantly. In light of this finding, we demonstrate that it is possible to characterize non-equilibrium brain dynamics using the interactions of pairs of macroscopic brain regions rather than complex interactions involving three or more regions. Furthermore, we propose that the entropy production of pairs of brain regions is a sensitive indicator for characterizing task-induced brain states.

AB - The human brain is a complex system of multiple neural elements that interact at different orders (pairwise, triplets, etc.), displaying non-equilibrium processes from the neuronal scale to the whole-brain scale. Here, we study how non-equilibrium dynamics of large-scale brain activity is driven by the interaction of its constituent elements at different orders. We hypothesize that the interactions generating non-equilibrium dynamics at the macroscopic brain scale are typically pairwise, with higher-order dependences playing a diminishing role. By expanding the entropy production into a sequence of orders of interactions, we find that pairwise interactions contribute dominantly. In light of this finding, we demonstrate that it is possible to characterize non-equilibrium brain dynamics using the interactions of pairs of macroscopic brain regions rather than complex interactions involving three or more regions. Furthermore, we propose that the entropy production of pairs of brain regions is a sensitive indicator for characterizing task-induced brain states.

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Non-equilibrium whole-brain dynamics arise from pairwise interactions

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Keywords

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