Multicellular sensing at a feedback-induced critical point

Michael Vennettilli, Amir Erez, Andrew Mugler*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Feedback in sensory biochemical networks can give rise to bifurcations in cells' behavioral response. These bifurcations share many properties with thermodynamic critical points. Evidence suggests that biological systems may operate near these critical points, but the functional benefit of doing so remains poorly understood. Here we investigate a simple biochemical model with nonlinear feedback and multicellular communication to determine if criticality provides a functional benefit in terms of the ability to gain information about a stochastic chemical signal. We find that when signal fluctuations are slow, the mutual information between the signal and the intracellular readout is maximized at criticality, because the benefit of high signal susceptibility outweighs the detriment of high readout noise. When cells communicate, criticality gives rise to long-range correlations in readout molecule number among cells. Consequently, we find that communication increases the mutual information between a given cell's readout and the spatial average of the signal across the population. Finally, we find that both with and without communication, the sensory benefits of criticality compete with critical slowing down, such that the information rate, as opposed to the information itself, is minimized at the critical point. Our results reveal the costs and benefits of feedback-induced criticality for multicellular sensing.

Original languageAmerican English
Article number052411
JournalPhysical Review E
Volume102
Issue number5
DOIs
StatePublished - 23 Nov 2020

Bibliographical note

Funding Information:
M.V. thanks Farshid Jafarpour and Terrence Edmonds for helpful discussions. M.V. and A.M. were supported by the Simons Foundation (376198) and the National Science Foundation (MCB-1936761, PHY-1945018). A.E. was supported by the National Science Foundation through the Center for the Physics of Biological Function (PHY-1734030) and by the National Institutes of Health (R01 GM082938).

Publisher Copyright:
© 2020 American Physical Society.

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