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Vascular origins of low-frequency oscillations in the cerebrospinal fluid signal in resting-state fMRI: Interpretation using photoplethysmography.

ABSTRACT: In vivo mapping of cerebrovascular oscillations in the 0.05-0.15 Hz remains difficult. Oscillations in the cerebrospinal fluid (CSF) represent a possible avenue for noninvasively tracking these oscillations using resting-state functional MRI (rs-fMRI), and have been used to correct for vascular oscillations in rs-fMRI functional connectivity. However, the relationship between low-frequency CSF and vascular oscillations remains unclear. In this study, we investigate this relationship using fast simultaneous rs-fMRI and photoplethysmogram (PPG), examining the 0.1 Hz PPG signal, heart-rate variability (HRV), pulse-intensity ratio (PIR), and the second derivative of the PPG (SDPPG). The main findings of this study are: (a) signals in different CSF regions are not equivalent in their associations with vascular and tissue rs-fMRI signals; (b) the PPG signal is maximally coherent with the arterial and CSF signals at the cardiac frequency, but coherent with brain tissue at ~0.2 Hz; (c) PIR is maximally coherent with the CSF signal near 0.03 Hz; and (d) PPG-related vascular oscillations only contribute to ~15% of the CSF (and arterial) signal in rs-fMRI. These findings caution against averaging all CSF regions when extracting physiological nuisance regressors in rs-fMRI applications, and indicate the drivers of the CSF signal are more than simply cardiac. Our study is an initial attempt at the refinement and standardization of how the CSF signal in rs-fMRI can be used and interpreted. It also paves the way for using rs-fMRI in the CSF as a potential tool for tracking cerebrovascular health through, for instance, the potential relationship between PIR and the CSF signal.

SUBMITTER: Attarpour A

PROVIDER: S-EPMC8090775 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Resting-state functional magnetic resonance imaging (rs-fMRI) is a widely used technique for mapping the brain's functional architecture, so delineating the main sources of variance comprising the signal is crucial. Low frequency oscillations (LFO) that are not of neural origin, but which are driven by mechanisms related to cerebral autoregulation (CA), are present in the blood-oxygenation-level-dependent (BOLD) signal within the rs-fMRI frequency band. In this study we use a MR compatible device (Caretaker, Biopac) to obtain a non-invasive estimate of beat-to-beat mean arterial pressure (MAP) fluctuations concurrently with rs-fMRI at 3T. Healthy adult subjects (n = 9; 5 male) completed two 20-min rs-fMRI scans. MAP fluctuations were decomposed into different frequency scales using a discrete wavelet transform, and oscillations at approximately 0.1 Hz show a high degree of spatially structured correlations with matched frequency fMRI fluctuations. On average across subjects, MAP fluctuations at this scale of the wavelet decomposition explain ∼2.2% of matched frequency fMRI signal variance. Additionally, a simultaneous multi-slice multi-echo acquisition was used to collect 10-min rs-fMRI at three echo times at 7T in a separate group of healthy adults (n = 5; 5 male). Multiple echo times were used to estimate the R2 ∗ decay at every time point, and MAP was shown to strongly correlate with this signal, which suggests a purely BOLD (i.e., blood flow related) origin. This study demonstrates that there is a significant component of the BOLD signal that has a systemic physiological origin, and highlights the fact that not all localized BOLD signal changes necessarily reflect blood flow supporting local neural activity. Instead, these data show that a proportion of BOLD signal fluctuations in rs-fMRI are due to localized control of blood flow that is independent of local neural activity, most likely reflecting more general systemic autoregulatory processes. Thus, fMRI is a promising tool for studying flow changes associated with cerebral autoregulation with high spatial resolution.

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Vascular origins of low-frequency oscillations in the cerebrospinal fluid signal in resting-state fMRI: Interpretation using photoplethysmography.

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