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Brain-wide functional connectivity artifactually inflates throughout fMRI scans: a problem and solution

The fMRI blood oxygen level-dependent (BOLD) signal is a mainstay of neuroimaging assessment of neuronal activity and functional connectivity in vivo. Thus, a chief priority is maximizing this signal’s reliability and validity. To this end, the fMRI community has invested considerable effort into op...

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Autores principales: Korponay, Cole, Janes, Amy C., Frederick, Blaise B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10515781/
https://www.ncbi.nlm.nih.gov/pubmed/37745340
http://dx.doi.org/10.1101/2023.09.08.556939
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author Korponay, Cole
Janes, Amy C.
Frederick, Blaise B.
author_facet Korponay, Cole
Janes, Amy C.
Frederick, Blaise B.
author_sort Korponay, Cole
collection PubMed
description The fMRI blood oxygen level-dependent (BOLD) signal is a mainstay of neuroimaging assessment of neuronal activity and functional connectivity in vivo. Thus, a chief priority is maximizing this signal’s reliability and validity. To this end, the fMRI community has invested considerable effort into optimizing both experimental designs and physiological denoising procedures to improve the accuracy, across-scan reproducibility, and subject discriminability of BOLD-derived metrics like functional connectivity. Despite these advances, we discover that a substantial and ubiquitous defect remains in fMRI datasets: functional connectivity throughout the brain artifactually inflates during the course of fMRI scans – by an average of more than 70% in 15 minutes of scan time - at spatially heterogeneous rates, producing both spatial and temporal distortion of brain connectivity maps. We provide evidence that this inflation is driven by a previously unrecognized time-dependent increase of non-neuronal, systemic low-frequency oscillation (sLFO) blood flow signal during fMRI scanning. This signal is not removed by standard denoising procedures such as independent component analysis (ICA). However, we demonstrate that a specialized sLFO denoising procedure - Regressor Interpolation at Progressive Time Delays (RIPTiDe) - can be added to standard denoising pipelines to significantly attenuate functional connectivity inflation. We confirm the presence of sLFO-driven functional connectivity inflation in multiple independent fMRI datasets – including the Human Connectome Project – as well as across resting-state, task, and sleep-state conditions, and demonstrate its potential to produce false positive findings. Collectively, we present evidence for a previously unknown physiological phenomenon that spatiotemporally distorts estimates of brain connectivity in human fMRI datasets, and present a solution for mitigating this artifact.
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spelling pubmed-105157812023-09-23 Brain-wide functional connectivity artifactually inflates throughout fMRI scans: a problem and solution Korponay, Cole Janes, Amy C. Frederick, Blaise B. bioRxiv Article The fMRI blood oxygen level-dependent (BOLD) signal is a mainstay of neuroimaging assessment of neuronal activity and functional connectivity in vivo. Thus, a chief priority is maximizing this signal’s reliability and validity. To this end, the fMRI community has invested considerable effort into optimizing both experimental designs and physiological denoising procedures to improve the accuracy, across-scan reproducibility, and subject discriminability of BOLD-derived metrics like functional connectivity. Despite these advances, we discover that a substantial and ubiquitous defect remains in fMRI datasets: functional connectivity throughout the brain artifactually inflates during the course of fMRI scans – by an average of more than 70% in 15 minutes of scan time - at spatially heterogeneous rates, producing both spatial and temporal distortion of brain connectivity maps. We provide evidence that this inflation is driven by a previously unrecognized time-dependent increase of non-neuronal, systemic low-frequency oscillation (sLFO) blood flow signal during fMRI scanning. This signal is not removed by standard denoising procedures such as independent component analysis (ICA). However, we demonstrate that a specialized sLFO denoising procedure - Regressor Interpolation at Progressive Time Delays (RIPTiDe) - can be added to standard denoising pipelines to significantly attenuate functional connectivity inflation. We confirm the presence of sLFO-driven functional connectivity inflation in multiple independent fMRI datasets – including the Human Connectome Project – as well as across resting-state, task, and sleep-state conditions, and demonstrate its potential to produce false positive findings. Collectively, we present evidence for a previously unknown physiological phenomenon that spatiotemporally distorts estimates of brain connectivity in human fMRI datasets, and present a solution for mitigating this artifact. Cold Spring Harbor Laboratory 2023-09-15 /pmc/articles/PMC10515781/ /pubmed/37745340 http://dx.doi.org/10.1101/2023.09.08.556939 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Korponay, Cole
Janes, Amy C.
Frederick, Blaise B.
Brain-wide functional connectivity artifactually inflates throughout fMRI scans: a problem and solution
title Brain-wide functional connectivity artifactually inflates throughout fMRI scans: a problem and solution
title_full Brain-wide functional connectivity artifactually inflates throughout fMRI scans: a problem and solution
title_fullStr Brain-wide functional connectivity artifactually inflates throughout fMRI scans: a problem and solution
title_full_unstemmed Brain-wide functional connectivity artifactually inflates throughout fMRI scans: a problem and solution
title_short Brain-wide functional connectivity artifactually inflates throughout fMRI scans: a problem and solution
title_sort brain-wide functional connectivity artifactually inflates throughout fmri scans: a problem and solution
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10515781/
https://www.ncbi.nlm.nih.gov/pubmed/37745340
http://dx.doi.org/10.1101/2023.09.08.556939
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