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

Abstract 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. Howeve...

Full description

Bibliographic Details
Main Authors: Federico Tesler, Marja-Leena Linne, Alain Destexhe
Format: Article
Language:English
Published: Nature Portfolio 2023-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-32618-0
_version_ 1797841001411248128
author Federico Tesler
Marja-Leena Linne
Alain Destexhe
author_facet Federico Tesler
Marja-Leena Linne
Alain Destexhe
author_sort Federico Tesler
collection DOAJ
description Abstract 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.
first_indexed 2024-04-09T16:23:50Z
format Article
id doaj.art-53af6238695d495ca62f9ae3b36146f6
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-04-09T16:23:50Z
publishDate 2023-04-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-53af6238695d495ca62f9ae3b36146f62023-04-23T11:17:33ZengNature PortfolioScientific Reports2045-23222023-04-0113111710.1038/s41598-023-32618-0Modeling the relationship between neuronal activity and the BOLD signal: contributions from astrocyte calcium dynamicsFederico Tesler0Marja-Leena Linne1Alain Destexhe2CNRS, Paris-Saclay Institute of Neuroscience (NeuroPSI), Paris-Saclay UniversityFaculty of Medicine and Health Technology, Tampere UniversityCNRS, Paris-Saclay Institute of Neuroscience (NeuroPSI), Paris-Saclay UniversityAbstract 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.https://doi.org/10.1038/s41598-023-32618-0
spellingShingle Federico Tesler
Marja-Leena Linne
Alain Destexhe
Modeling the relationship between neuronal activity and the BOLD signal: contributions from astrocyte calcium dynamics
Scientific Reports
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
url https://doi.org/10.1038/s41598-023-32618-0
work_keys_str_mv AT federicotesler modelingtherelationshipbetweenneuronalactivityandtheboldsignalcontributionsfromastrocytecalciumdynamics
AT marjaleenalinne modelingtherelationshipbetweenneuronalactivityandtheboldsignalcontributionsfromastrocytecalciumdynamics
AT alaindestexhe modelingtherelationshipbetweenneuronalactivityandtheboldsignalcontributionsfromastrocytecalciumdynamics