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Modeling the relationship between neuronal activity and the BOLD signal: contributions from astrocyte calcium dynamics

Functional magnetic resonance imaging relies on the coupling between neuronal and vascular activity, but the mechanisms behind this coupling are still under discussion. Recent experimental evidence suggests that calcium signaling may play a significant role in neurovascular coupling. However, it is...

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Autores principales: Tesler, Federico, Linne, Marja-Leena, Destexhe, Alain
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10119111/
https://www.ncbi.nlm.nih.gov/pubmed/37081004
http://dx.doi.org/10.1038/s41598-023-32618-0
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author Tesler, Federico
Linne, Marja-Leena
Destexhe, Alain
author_facet Tesler, Federico
Linne, Marja-Leena
Destexhe, Alain
author_sort Tesler, Federico
collection PubMed
description Functional magnetic resonance imaging relies on the coupling between neuronal and vascular activity, but the mechanisms behind this coupling are still under discussion. Recent experimental evidence suggests that calcium signaling may play a significant role in neurovascular coupling. However, it is still controversial where this calcium signal is located (in neurons or elsewhere), how it operates and how relevant is its role. In this paper we introduce a biologically plausible model of the neurovascular coupling and we show that calcium signaling in astrocytes can explain main aspects of the dynamics of the coupling. We find that calcium signaling can explain so-far unrelated features such as the linear and non-linear regimes, the negative vascular response (undershoot) and the emergence of a (calcium-driven) Hemodynamic Response Function. These features are reproduced here for the first time by a single model of the detailed neuronal-astrocyte-vascular pathway. Furthermore, we analyze how information is coded and transmitted from the neuronal to the vascular system and we predict that frequency modulation of astrocytic calcium dynamics plays a key role in this process. Finally, our work provides a framework to link neuronal activity to the BOLD signal, and vice-versa, where neuronal activity can be inferred from the BOLD signal. This opens new ways to link known alterations of astrocytic calcium signaling in neurodegenerative diseases (e.g. Alzheimer’s and Parkinson’s diseases) with detectable changes in the neurovascular coupling.
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spelling pubmed-101191112023-04-22 Modeling the relationship between neuronal activity and the BOLD signal: contributions from astrocyte calcium dynamics Tesler, Federico Linne, Marja-Leena Destexhe, Alain Sci Rep Article Functional magnetic resonance imaging relies on the coupling between neuronal and vascular activity, but the mechanisms behind this coupling are still under discussion. Recent experimental evidence suggests that calcium signaling may play a significant role in neurovascular coupling. However, it is still controversial where this calcium signal is located (in neurons or elsewhere), how it operates and how relevant is its role. In this paper we introduce a biologically plausible model of the neurovascular coupling and we show that calcium signaling in astrocytes can explain main aspects of the dynamics of the coupling. We find that calcium signaling can explain so-far unrelated features such as the linear and non-linear regimes, the negative vascular response (undershoot) and the emergence of a (calcium-driven) Hemodynamic Response Function. These features are reproduced here for the first time by a single model of the detailed neuronal-astrocyte-vascular pathway. Furthermore, we analyze how information is coded and transmitted from the neuronal to the vascular system and we predict that frequency modulation of astrocytic calcium dynamics plays a key role in this process. Finally, our work provides a framework to link neuronal activity to the BOLD signal, and vice-versa, where neuronal activity can be inferred from the BOLD signal. This opens new ways to link known alterations of astrocytic calcium signaling in neurodegenerative diseases (e.g. Alzheimer’s and Parkinson’s diseases) with detectable changes in the neurovascular coupling. Nature Publishing Group UK 2023-04-20 /pmc/articles/PMC10119111/ /pubmed/37081004 http://dx.doi.org/10.1038/s41598-023-32618-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Tesler, Federico
Linne, Marja-Leena
Destexhe, Alain
Modeling the relationship between neuronal activity and the BOLD signal: contributions from astrocyte calcium dynamics
title Modeling the relationship between neuronal activity and the BOLD signal: contributions from astrocyte calcium dynamics
title_full Modeling the relationship between neuronal activity and the BOLD signal: contributions from astrocyte calcium dynamics
title_fullStr Modeling the relationship between neuronal activity and the BOLD signal: contributions from astrocyte calcium dynamics
title_full_unstemmed Modeling the relationship between neuronal activity and the BOLD signal: contributions from astrocyte calcium dynamics
title_short Modeling the relationship between neuronal activity and the BOLD signal: contributions from astrocyte calcium dynamics
title_sort modeling the relationship between neuronal activity and the bold signal: contributions from astrocyte calcium dynamics
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10119111/
https://www.ncbi.nlm.nih.gov/pubmed/37081004
http://dx.doi.org/10.1038/s41598-023-32618-0
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