Prevalent and sex-biased breathing patterns modify functional connectivity MRI in young adults

Lynch, Charles J.; Silver, Benjamin M.; Dubin, Marc G.; Martin, Alex; Voss, Henning U.; Jones, Rebecca M.; Power, Jonathan D.

doi:10.1038/s41467-020-18974-9

Cited by 35 publications

(31 citation statements)

References 57 publications

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“…3A ). Importantly, the amplitude of these natural fluctuations during resting-state will vary across subjects, and potentially across study populations ( Lynch et al, 2020 ). If the BOLD fluctuations related to P ET CO 2 changes are small in amplitude, it can be hard to distinguish them from other physiological, artefactual or neuronally-driven fluctuations that occur at (or aliased into) the same low-frequencies ( Murphy et al, 2013 , Liu, 2016 , Caballero-Gaudes and Reynolds, 2017 , Tong et al, 2019 , Whittaker et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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Cerebrovascular reactivity (CVR), defined here as the Blood Oxygenation Level Dependent (BOLD) response to a CO 2 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 2–3 minute breathing task to the start of a resting-state segment. Two different breathing tasks were used to induce fluctuations in arterial CO 2 pressure: a breath-hold task to induce hypercapnia (CO 2 increase) and a cued deep breathing task to induce hypocapnia (CO 2 decrease). Our analysis produced voxel-wise estimates of the amplitude (CVR) and timing (lag) of the BOLD-fMRI response to CO 2 by systematically shifting the CO 2 regressor in time to optimize the model fit. This optimization inherently increases gray 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 CO 2 and BOLD-fMRI signals, and improves our confidence in the plausibility of voxel-wise 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: Discussionmentioning

confidence: 99%

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

et al. 2021

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“…One reason that including breathing tasks benefits CVR mapping is simply that the induced variation in P ET CO 2 amplitude is large compared to the smaller fluctuations during undirected free breathing (see Figure 2). Importantly, the amplitude of these natural fluctuations during resting-state will vary across subjects, and potentially across study populations [91]. If the BOLD fluctuations related to P ET CO 2 changes are small in amplitude, it can be hard to distinguish them from other physiological, artefactual or neuronally-driven fluctuations that occur at (or aliased into) the same low-frequencies [45]–[49].…”

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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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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“…Both studies did agree on males having larger SC-FC coupling in right supramarginal gyrus, but the rest of the results diverge. We hypothesize this may be due to differences in sample size/characteristics or imaging acquisition/preprocessing strategies; particularly important when investigating sex differences in FC is the use of global signal regression which can remove non-neuronal signals like motion 39 and respiration that are known to have sex-specific effects 40 . Our GLM framework additionally controlled for covariates like in-scanner motion and intracranial volume which have known sex differences and a complex relationship with BOLD signals 41, 42 .…”

Section: Discussionmentioning

confidence: 99%

Regional structural-functional connectome coupling is heritable and associated with age, sex and cognitive scores in adults

Jamison

Sabuncu

et al. 2020

Preprint

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Large scale white matter brain connections quantified via the structural connectome (SC) act as the backbone for the flow of functional activation, which can be represented via the functional connectome (FC). Many studies have used statistical analysis or computational modeling techniques to relate SC and FC at a global, whole-brain level. However, relatively few studies have investigated the relationship between individual cortical and subcortical regions’ structural and functional connectivity profiles, here called SC-FC coupling, or how this SC-FC coupling may be heritable or related to age, sex and cognitive abilities. Here, we quantify regional SC-FC coupling in a large group of healthy young adults (22 to 37 years) using diffusion-weighted MRI and resting-state functional MRI data from the Human Connectome Project. We find that while regional SC-FC coupling strengths vary widely across cortical, subcortical and cerebellar regions, they were strongest in highly myelinated visual and somatomotor areas. Additionally, SC-FC coupling displayed a broadly negative association with age and, depending on the region, varied across sexes and with cognitive scores. Specifically, males had higher coupling strength in right supramarginal gyrus and left cerebellar regions while females had higher coupling strength in right visual, right limbic and right cerebellar regions. Furthermore, increased SC-FC coupling in the right lingual gyrus was associated with worse cognitive scores. Finally, we found SC-FC coupling to be highly heritable, particularly in the visual, dorsal attention, and fronto-parietal networks, and, interestingly, more heritable than FC or SC alone. Taken together, these results suggest regional structure-function coupling in young adults decreases with age, varies across sexes in a non-systematic way, is somewhat associated with cognition and is highly heritable.

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Prevalent and sex-biased breathing patterns modify functional connectivity MRI in young adults

Cited by 35 publications

References 57 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

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

Regional structural-functional connectome coupling is heritable and associated with age, sex and cognitive scores in adults

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