Cerebrovascular reactivity mapping using intermittent breath modulation

Liu, Peiying; Xu, Cuimei; Lin, Zixuan; Sur, Sandeepa; Li, Yang; Yaşar, Sevil; Rosenberg, Paul B.; Albert, Marilyn; Lu, Hanzhang

doi:10.1016/j.neuroimage.2020.116787

Cited by 28 publications

(37 citation statements)

References 48 publications

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“…Therefore, we chose to display CVR values resulting from multiple analysis options in Figure 8 and Supplementary Figure 7. With no statistical thresholding, the positive GM CVR amplitudes for No-Opt and Lag-Opt (Figure 8 and Supplementary Table 2) agree with the range seen in previous literature modelling CVR with breathing tasks or resting-state, when expressed in units of %BOLD/mmHg [34], [42], [54], [58], [63], [93], [94]. Unexpectedly, the REST segments showed higher GM CVR values than the task segments after lag optimization and following the strictest thresholding, particularly for RESTCDB ( Figure 8, Supplementary Figure 7).…”

Section: Discussionsupporting

confidence: 87%

“…We have shown that the inclusion of breathing task data further increases the number of voxels in the brain that have a significant relationship between PETCO2 and BOLD-fMRI signals, and improves our confidence in the plausibility of voxel-wise hemodynamic lag estimates. A recent study [34] followed a very similar rationale to ours: to develop a practical non-gas inhalation method that is largely based in a resting-state scan but introduces breathing modulations to enhance fluctuations in PETCO2. They compared CVR maps from resting-state scans, scans with intermittent breathing modulations throughout the scan period (for a duration of 12 seconds after 30-60 s of free breathing), a breath-holding scan, and a CO2 gas inhalation scan.…”

Section: Discussionmentioning

confidence: 99%

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A practical modification to a resting state fMRI protocol for improved characterization of cerebrovascular function

Stickland

Zvolanek

Moia

et al. 2021

Preprint

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Cerebrovascular reactivity (CVR), defined here as the Blood Oxygenation Level Dependent (BOLD) response to a CO2 pressure change, is a useful metric of cerebrovascular function. Both the amplitude and the timing (hemodynamic lag) of the CVR response can bring insight into the nature of a cerebrovascular pathology and aid in understanding noise confounds when using functional Magnetic Resonance Imaging (fMRI) to study neural activity. This research assessed a practical modification to a typical resting state fMRI protocol, to improve the characterization of cerebrovascular function. In 9 healthy subjects, we modelled CVR and lag in three resting state data segments, and in data segments which added a 2 to 3 minute breathing task to the start of a resting state segment. Two different breathing tasks were used to induce fluctuations in arterial CO2 pressure: a breath hold task to induce hypercapnia (CO2 increase) and a cued deep breathing task to induce hypocapnia (CO2 decrease). Our analysis produced voxelwise estimates of the amplitude (CVR) and timing (lag) of the BOLD fMRI response to CO2 by systematically shifting the CO2 regressor in time to optimize the model fit. This optimization inherently increases grey matter CVR values and fit statistics. The inclusion of a simple breathing task, compared to a resting state scan only, increases the number of voxels in the brain that have a significant relationship between CO2 and BOLD fMRI signals, and improves our confidence in the plausibility of voxelwise CVR and hemodynamic lag estimates. We demonstrate the clinical utility and feasibility of this protocol in an incidental finding of Moyamoya disease, and explore the possibilities and challenges of using this protocol in younger populations. This hybrid protocol has direct applications for CVR mapping in both research and clinical settings and wider applications for fMRI denoising and interpretation.

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Section: Discussionsupporting

confidence: 87%

Section: Discussionmentioning

confidence: 99%

A practical modification to a resting state fMRI protocol for improved characterization of cerebrovascular function

Stickland

Zvolanek

Moia

et al. 2021

Preprint

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“…Another possibility would be to assess CVR in resting state fMRI, either measuring resting fluctuations in exhaled CO2 levels (Golestani, Wei, & Chen, 2016;Lipp et al, 2015), or by using a band of the power spectrum of the global signal as a regressor of interest (P. Liu et al, 2017Liu et al, , 2020.…”

Section: Discussionmentioning

confidence: 99%

ICA-based Denoising Strategies in Breath-Hold Induced Cerebrovascular Reactivity Mapping with Multi Echo BOLD fMRI

Moia

Termenon

Uruñuela

et al. 2020

Preprint

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Performing a BOLD functional MRI (fMRI) acquisition during breath-hold (BH) tasks is a non-invasive, robust method to estimate cerebrovascular reactivity (CVR). However, movement and breathing-related artefacts caused by the BH can substantially hinder CVR estimates due to their high temporal collinearity with the effect of interest, and attention has to be paid when choosing which analysis model should be applied to the data. In this study, we evaluate the performance of multiple analysis strategies based on lagged general linear models applied on multi-echo BOLD fMRI data, acquired in ten subjects performing a BH task during ten sessions, to obtain subject-specific CVR and haemodynamic lag estimates. The evaluated approaches range from conventional regression models including drifts and motion timecourses as nuisance regressors applied on single-echo or optimally-combined data, to more complex models including regressors obtained from multi-echo independent component analysis with different grades of orthogonalization in order to preserve the effect of interest, i.e. the CVR. We compare these models in terms of their ability to make signal intensity changes independent from motion, as well as the reliability as measured by voxelwise intraclass correlation coefficients of both CVR and lag maps over time. Our results reveal that a conservative independent component analysis model applied on the optimally-combined multi-echo fMRI signal offers the largest reduction of motion-related effects in the signal, while yielding reliable CVR amplitude and lag estimates, although a conventional regression model applied on the optimally-combined data results in similar estimates. This work demonstrate the usefulness of multi-echo based fMRI acquisitions and independent component analysis denoising for precision mapping of CVR in single subjects based on BH paradigms, fostering its potential as a clinically-viable neuroimaging tool for individual patients. It also proves that the way in which data-driven regressors should be incorporated in the analysis model is not straight-forward due to their complex interaction with the BH-induced BOLD response.

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“…Task instructions are usually provided using visual cues, although auditory cues can also be used ( Riecker et al, 2003 ; Chang et al, 2008 ; Kannurpatti and Biswal, 2008 ; Tancredi and Hoge, 2013 ; Wu et al, 2019 ). Visual cues have ranged from simple written instructions displayed on a screen ( Bright and Murphy, 2013 ; Haight et al, 2015 ; Lipp et al, 2015 ; Pinto et al, 2016 ; Liu et al, 2020 ), to color-coded or symbolic cues ( Friedman et al, 2008 ; Thomason and Glover, 2008 ; Kannurpatti et al, 2010 ; Gonzales et al, 2014 ; Prilipko et al, 2014 ). In order to control for the potentially strong neuronal activation induced by visual instructions, brightness levels should remain similar across task and baseline periods ( Kastrup et al, 1999a , b ).…”

Section: Task-based Methodsmentioning

confidence: 99%

“…Combined breathing protocols should also be explored. In fact, a newly proposed breathing protocol based on rs-fMRI combined with intermittent breath modulation was indicated as another option for less cooperative participants ( Liu et al, 2020 ). This strategy combines the large dynamic range of changes induced by breathing tasks with the easiness of resting-state methods.…”

Section: Future Workmentioning

confidence: 99%

Cerebrovascular Reactivity Mapping Without Gas Challenges: A Methodological Guide

et al. 2021

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Cerebrovascular reactivity (CVR) is defined as the ability of vessels to alter their caliber in response to vasoactive factors, by means of dilating or constricting, in order to increase or decrease regional cerebral blood flow (CBF). Importantly, CVR may provide a sensitive biomarker for pathologies where vasculature is compromised. Furthermore, the spatiotemporal dynamics of CVR observed in healthy subjects, reflecting regional differences in cerebral vascular tone and response, may also be important in functional MRI studies based on neurovascular coupling mechanisms. Assessment of CVR is usually based on the use of a vasoactive stimulus combined with a CBF measurement technique. Although transcranial Doppler ultrasound has been frequently used to obtain global flow velocity measurements, MRI techniques are being increasingly employed for obtaining CBF maps. For the vasoactive stimulus, vasodilatory hypercapnia is usually induced through the manipulation of respiratory gases, including the inhalation of increased concentrations of carbon dioxide. However, most of these methods require an additional apparatus and complex setups, which not only may not be well-tolerated by some populations but are also not widely available. For these reasons, strategies based on voluntary breathing fluctuations without the need for external gas challenges have been proposed. These include the task-based methodologies of breath holding and paced deep breathing, as well as a new generation of methods based on spontaneous breathing fluctuations during resting-state. Despite the multitude of alternatives to gas challenges, existing literature lacks definitive conclusions regarding the best practices for the vasoactive modulation and associated analysis protocols. In this work, we perform an extensive review of CVR mapping techniques based on MRI and CO2 variations without gas challenges, focusing on the methodological aspects of the breathing protocols and corresponding data analysis. Finally, we outline a set of practical guidelines based on generally accepted practices and available data, extending previous reports and encouraging the wider application of CVR mapping methodologies in both clinical and academic MRI settings.

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Cerebrovascular reactivity mapping using intermittent breath modulation

Cited by 28 publications

References 48 publications

A practical modification to a resting state fMRI protocol for improved characterization of cerebrovascular function

A practical modification to a resting state fMRI protocol for improved characterization of cerebrovascular function

ICA-based Denoising Strategies in Breath-Hold Induced Cerebrovascular Reactivity Mapping with Multi Echo BOLD fMRI

Cerebrovascular Reactivity Mapping Without Gas Challenges: A Methodological Guide

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