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Temporal signals drive the emergence of multicellular information networks
Coordinated responses to environmental stimuli are critical for multicellular organisms. To overcome the obstacles of cell-to-cell heterogeneity and noisy signaling dynamics within individual cells, cells must effectively exchange information with peers. However, the dynamics and mechanisms of colle...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9477235/ https://www.ncbi.nlm.nih.gov/pubmed/36067282 http://dx.doi.org/10.1073/pnas.2202204119 |
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author | Li, Guanyu LeFebre, Ryan Starman, Alia Chappell, Patrick Mugler, Andrew Sun, Bo |
author_facet | Li, Guanyu LeFebre, Ryan Starman, Alia Chappell, Patrick Mugler, Andrew Sun, Bo |
author_sort | Li, Guanyu |
collection | PubMed |
description | Coordinated responses to environmental stimuli are critical for multicellular organisms. To overcome the obstacles of cell-to-cell heterogeneity and noisy signaling dynamics within individual cells, cells must effectively exchange information with peers. However, the dynamics and mechanisms of collective information transfer driven by external signals are poorly understood. Here we investigate the calcium dynamics of neuronal cells that form confluent monolayers and respond to cyclic ATP stimuli in microfluidic devices. Using Granger inference to reconstruct the underlying causal relations between the cells, we find that the cells self-organize into spatially decentralized and temporally stationary networks to support information transfer via gap junction channels. The connectivity of the causal networks depends on the temporal profile of the external stimuli, where short periods, or long periods with small duty fractions, lead to reduced connectivity and fractured network topology. We build a theoretical model based on communicating excitable units that reproduces our observations. The model further predicts that connectivity of the causal network is maximal at an optimal communication strength, which is confirmed by the experiments. Together, our results show that information transfer between neuronal cells is externally regulated by the temporal profile of the stimuli and internally regulated by cell–cell communication. |
format | Online Article Text |
id | pubmed-9477235 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-94772352023-03-06 Temporal signals drive the emergence of multicellular information networks Li, Guanyu LeFebre, Ryan Starman, Alia Chappell, Patrick Mugler, Andrew Sun, Bo Proc Natl Acad Sci U S A Physical Sciences Coordinated responses to environmental stimuli are critical for multicellular organisms. To overcome the obstacles of cell-to-cell heterogeneity and noisy signaling dynamics within individual cells, cells must effectively exchange information with peers. However, the dynamics and mechanisms of collective information transfer driven by external signals are poorly understood. Here we investigate the calcium dynamics of neuronal cells that form confluent monolayers and respond to cyclic ATP stimuli in microfluidic devices. Using Granger inference to reconstruct the underlying causal relations between the cells, we find that the cells self-organize into spatially decentralized and temporally stationary networks to support information transfer via gap junction channels. The connectivity of the causal networks depends on the temporal profile of the external stimuli, where short periods, or long periods with small duty fractions, lead to reduced connectivity and fractured network topology. We build a theoretical model based on communicating excitable units that reproduces our observations. The model further predicts that connectivity of the causal network is maximal at an optimal communication strength, which is confirmed by the experiments. Together, our results show that information transfer between neuronal cells is externally regulated by the temporal profile of the stimuli and internally regulated by cell–cell communication. National Academy of Sciences 2022-09-06 2022-09-13 /pmc/articles/PMC9477235/ /pubmed/36067282 http://dx.doi.org/10.1073/pnas.2202204119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Physical Sciences Li, Guanyu LeFebre, Ryan Starman, Alia Chappell, Patrick Mugler, Andrew Sun, Bo Temporal signals drive the emergence of multicellular information networks |
title | Temporal signals drive the emergence of multicellular information networks |
title_full | Temporal signals drive the emergence of multicellular information networks |
title_fullStr | Temporal signals drive the emergence of multicellular information networks |
title_full_unstemmed | Temporal signals drive the emergence of multicellular information networks |
title_short | Temporal signals drive the emergence of multicellular information networks |
title_sort | temporal signals drive the emergence of multicellular information networks |
topic | Physical Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9477235/ https://www.ncbi.nlm.nih.gov/pubmed/36067282 http://dx.doi.org/10.1073/pnas.2202204119 |
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