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Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality

Dendritic spines change their size and shape spontaneously, but the function of this remains unclear. Here, we address this in a biophysical model of spine fluctuations, which reproduces experimentally measured spine fluctuations. For this, we characterize size- and shape fluctuations from confocal...

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Autores principales: Bonilla-Quintana, Mayte, Wörgötter, Florentin, D’Este, Elisa, Tetzlaff, Christian, Fauth, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7889935/
https://www.ncbi.nlm.nih.gov/pubmed/33597561
http://dx.doi.org/10.1038/s41598-021-83331-9
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author Bonilla-Quintana, Mayte
Wörgötter, Florentin
D’Este, Elisa
Tetzlaff, Christian
Fauth, Michael
author_facet Bonilla-Quintana, Mayte
Wörgötter, Florentin
D’Este, Elisa
Tetzlaff, Christian
Fauth, Michael
author_sort Bonilla-Quintana, Mayte
collection PubMed
description Dendritic spines change their size and shape spontaneously, but the function of this remains unclear. Here, we address this in a biophysical model of spine fluctuations, which reproduces experimentally measured spine fluctuations. For this, we characterize size- and shape fluctuations from confocal microscopy image sequences using autoregressive models and a new set of shape descriptors derived from circular statistics. Using the biophysical model, we extrapolate into longer temporal intervals and find the presence of 1/f noise. When investigating its origins, the model predicts that the actin dynamics underlying shape fluctuations self-organizes into a critical state, which creates a fine balance between static actin filaments and free monomers. In a comparison against a non-critical model, we show that this state facilitates spine enlargement, which happens after LTP induction. Thus, ongoing spine shape fluctuations might be necessary to react quickly to plasticity events.
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spelling pubmed-78899352021-02-22 Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality Bonilla-Quintana, Mayte Wörgötter, Florentin D’Este, Elisa Tetzlaff, Christian Fauth, Michael Sci Rep Article Dendritic spines change their size and shape spontaneously, but the function of this remains unclear. Here, we address this in a biophysical model of spine fluctuations, which reproduces experimentally measured spine fluctuations. For this, we characterize size- and shape fluctuations from confocal microscopy image sequences using autoregressive models and a new set of shape descriptors derived from circular statistics. Using the biophysical model, we extrapolate into longer temporal intervals and find the presence of 1/f noise. When investigating its origins, the model predicts that the actin dynamics underlying shape fluctuations self-organizes into a critical state, which creates a fine balance between static actin filaments and free monomers. In a comparison against a non-critical model, we show that this state facilitates spine enlargement, which happens after LTP induction. Thus, ongoing spine shape fluctuations might be necessary to react quickly to plasticity events. Nature Publishing Group UK 2021-02-17 /pmc/articles/PMC7889935/ /pubmed/33597561 http://dx.doi.org/10.1038/s41598-021-83331-9 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Bonilla-Quintana, Mayte
Wörgötter, Florentin
D’Este, Elisa
Tetzlaff, Christian
Fauth, Michael
Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality
title Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality
title_full Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality
title_fullStr Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality
title_full_unstemmed Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality
title_short Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality
title_sort reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7889935/
https://www.ncbi.nlm.nih.gov/pubmed/33597561
http://dx.doi.org/10.1038/s41598-021-83331-9
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