Abstract
We present the first evidence for vascular regulation driving fMRI signals in specific functional brain networks. Using concurrent neuronal and vascular stimuli, we collected 30 BOLD fMRI datasets in 10 healthy individuals: a working memory task, flashing checkerboard stimulus, and CO2 inhalation challenge were delivered in concurrent but orthogonal paradigms. The resulting imaging data were averaged together and decomposed using independent component analysis, and three “neuronal networks” were identified as demonstrating maximum temporal correlation with the neuronal stimulus paradigms: Default Mode Network, Task Positive Network, and Visual Network. For each of these, we observed a second network component with high spatial overlap. Using dual regression in the original 30 datasets, we extracted the time-series associated with these network pairs and calculated the percent of variance explained by the neuronal or vascular stimuli using a normalized R2 parameter. In each pairing, one network was dominated by the appropriate neuronal stimulus, and the other was dominated by the vascular stimulus as represented by the end-tidal CO2 time-series recorded in each scan. We acquired a second dataset in 8 of the original participants, where no CO2 challenge was delivered and CO2 levels fluctuated naturally with breathing variations. Although splitting of functional networks was not robust in these data, performing dual regression with the network maps from the original analysis in this new dataset successfully replicated our observations. Thus, in addition to responding to localized metabolic changes, the brain’s vasculature may be regulated in a coordinated manner that mimics (and potentially supports) specific functional brain networks. Multi-modal imaging and advances in fMRI acquisition and analysis could facilitate further study of the dual nature of functional brain networks. It will be critical to understand network-specific vascular function, and the behavior of a coupled vascular-neural network, in future studies of brain pathology.
Highlights
Imaging neuroscience has advanced a new theory of brain function based on the interconnectedness of neuronal activity in multiple brain regions(Friston, 2011)
We observed that all three functional brain networks probed in our study were composed of spatially similar pairs of components where one was significantly more associated with the appropriate neuronal stimulus and the other significantly more associated with the vascular stimulus
The inhaled carbon dioxide challenge used as a vascular stimulus in this study is known to induce systemic vasodilation and Blood Oxygenation Level Dependent (BOLD) signal increases (Liu, B De Vis, & Lu, 2018), our results suggest that the vasodilatory effects show regional variation and that may drive BOLD signal changes in specific functional brain networks or sub-networks
Summary
Imaging neuroscience has advanced a new theory of brain function based on the interconnectedness of neuronal activity in multiple brain regions(Friston, 2011) These regions form structural and functional networks that are consistent across individuals(Damoiseaux et al., 2006) and intrinsic to brain activity during active processing or in the resting state(Friston, 2011; Smith et al, 2009). It is well established that local blood flow is tightly coupled to local neuronal activity to protect brain metabolism (Damoiseaux et al, 2006; Karbowski, 2014) This coupling is what underpins the Blood Oxygenation Level Dependent (BOLD) contrast mechanism in functional magnetic resonance imaging (fMRI) of brain activity, and this technique has been used to characterize functional networks in thousands of neuroimaging studies of the human brain (Power, Schlaggar, & Petersen, 2014). Several functional brain networks are robustly identified in human subjects, in both task-activation and resting-state datasets (Cole, Bassett, Power, Braver, & Petersen, 2014; Damoiseaux et al, 2006; Smith et al, 2009), and are frequently characterized in patient cohorts to better understand the mechanisms of pathology
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