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Artificial intelligence velocimetry reveals in vivo flow rates, pressure gradients, and shear stresses in murine perivascular flows

Quantifying the flow of cerebrospinal fluid (CSF) is crucial for understanding brain waste clearance and nutrient delivery, as well as edema in pathological conditions such as stroke. However, existing in vivo techniques are limited to sparse velocity measurements in pial perivascular spaces (PVSs)...

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Autores principales: Boster, Kimberly A. S., Cai, Shengze, Ladrón-de-Guevara, Antonio, Sun, Jiatong, Zheng, Xiaoning, Du, Ting, Thomas, John H., Nedergaard, Maiken, Karniadakis, George Em, Kelley, Douglas H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10083563/
https://www.ncbi.nlm.nih.gov/pubmed/36989300
http://dx.doi.org/10.1073/pnas.2217744120
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author Boster, Kimberly A. S.
Cai, Shengze
Ladrón-de-Guevara, Antonio
Sun, Jiatong
Zheng, Xiaoning
Du, Ting
Thomas, John H.
Nedergaard, Maiken
Karniadakis, George Em
Kelley, Douglas H.
author_facet Boster, Kimberly A. S.
Cai, Shengze
Ladrón-de-Guevara, Antonio
Sun, Jiatong
Zheng, Xiaoning
Du, Ting
Thomas, John H.
Nedergaard, Maiken
Karniadakis, George Em
Kelley, Douglas H.
author_sort Boster, Kimberly A. S.
collection PubMed
description Quantifying the flow of cerebrospinal fluid (CSF) is crucial for understanding brain waste clearance and nutrient delivery, as well as edema in pathological conditions such as stroke. However, existing in vivo techniques are limited to sparse velocity measurements in pial perivascular spaces (PVSs) or low-resolution measurements from brain-wide imaging. Additionally, volume flow rate, pressure, and shear stress variation in PVSs are essentially impossible to measure in vivo. Here, we show that artificial intelligence velocimetry (AIV) can integrate sparse velocity measurements with physics-informed neural networks to quantify CSF flow in PVSs. With AIV, we infer three-dimensional (3D), high-resolution velocity, pressure, and shear stress. Validation comes from training with 70% of PTV measurements and demonstrating close agreement with the remaining 30%. A sensitivity analysis on the AIV inputs shows that the uncertainty in AIV inferred quantities due to uncertainties in the PVS boundary locations inherent to in vivo imaging is less than 30%, and the uncertainty from the neural net initialization is less than 1%. In PVSs of N = 4 wild-type mice we find mean flow speed 16.33 ± 11.09 µm/s, volume flow rate 2.22 ± 1.983 × 10(3) µm(3)/s, axial pressure gradient ( − 2.75 ± 2.01)×10(−4) Pa/µm (−2.07 ± 1.51 mmHg/m), and wall shear stress (3.00 ± 1.45)×10(−3) Pa (all mean ± SE). Pressure gradients, flow rates, and resistances agree with prior predictions. AIV infers in vivo PVS flows in remarkable detail, which will improve fluid dynamic models and potentially clarify how CSF flow changes with aging, Alzheimer’s disease, and small vessel disease.
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spelling pubmed-100835632023-09-29 Artificial intelligence velocimetry reveals in vivo flow rates, pressure gradients, and shear stresses in murine perivascular flows Boster, Kimberly A. S. Cai, Shengze Ladrón-de-Guevara, Antonio Sun, Jiatong Zheng, Xiaoning Du, Ting Thomas, John H. Nedergaard, Maiken Karniadakis, George Em Kelley, Douglas H. Proc Natl Acad Sci U S A Physical Sciences Quantifying the flow of cerebrospinal fluid (CSF) is crucial for understanding brain waste clearance and nutrient delivery, as well as edema in pathological conditions such as stroke. However, existing in vivo techniques are limited to sparse velocity measurements in pial perivascular spaces (PVSs) or low-resolution measurements from brain-wide imaging. Additionally, volume flow rate, pressure, and shear stress variation in PVSs are essentially impossible to measure in vivo. Here, we show that artificial intelligence velocimetry (AIV) can integrate sparse velocity measurements with physics-informed neural networks to quantify CSF flow in PVSs. With AIV, we infer three-dimensional (3D), high-resolution velocity, pressure, and shear stress. Validation comes from training with 70% of PTV measurements and demonstrating close agreement with the remaining 30%. A sensitivity analysis on the AIV inputs shows that the uncertainty in AIV inferred quantities due to uncertainties in the PVS boundary locations inherent to in vivo imaging is less than 30%, and the uncertainty from the neural net initialization is less than 1%. In PVSs of N = 4 wild-type mice we find mean flow speed 16.33 ± 11.09 µm/s, volume flow rate 2.22 ± 1.983 × 10(3) µm(3)/s, axial pressure gradient ( − 2.75 ± 2.01)×10(−4) Pa/µm (−2.07 ± 1.51 mmHg/m), and wall shear stress (3.00 ± 1.45)×10(−3) Pa (all mean ± SE). Pressure gradients, flow rates, and resistances agree with prior predictions. AIV infers in vivo PVS flows in remarkable detail, which will improve fluid dynamic models and potentially clarify how CSF flow changes with aging, Alzheimer’s disease, and small vessel disease. National Academy of Sciences 2023-03-29 2023-04-04 /pmc/articles/PMC10083563/ /pubmed/36989300 http://dx.doi.org/10.1073/pnas.2217744120 Text en Copyright © 2023 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
Boster, Kimberly A. S.
Cai, Shengze
Ladrón-de-Guevara, Antonio
Sun, Jiatong
Zheng, Xiaoning
Du, Ting
Thomas, John H.
Nedergaard, Maiken
Karniadakis, George Em
Kelley, Douglas H.
Artificial intelligence velocimetry reveals in vivo flow rates, pressure gradients, and shear stresses in murine perivascular flows
title Artificial intelligence velocimetry reveals in vivo flow rates, pressure gradients, and shear stresses in murine perivascular flows
title_full Artificial intelligence velocimetry reveals in vivo flow rates, pressure gradients, and shear stresses in murine perivascular flows
title_fullStr Artificial intelligence velocimetry reveals in vivo flow rates, pressure gradients, and shear stresses in murine perivascular flows
title_full_unstemmed Artificial intelligence velocimetry reveals in vivo flow rates, pressure gradients, and shear stresses in murine perivascular flows
title_short Artificial intelligence velocimetry reveals in vivo flow rates, pressure gradients, and shear stresses in murine perivascular flows
title_sort artificial intelligence velocimetry reveals in vivo flow rates, pressure gradients, and shear stresses in murine perivascular flows
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10083563/
https://www.ncbi.nlm.nih.gov/pubmed/36989300
http://dx.doi.org/10.1073/pnas.2217744120
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