Effects of Thresholding on Voxel-Wise Correspondence of Breath-Hold and Resting-State Maps of Cerebrovascular Reactivity.

Nooshin J Fesharaki,James L Reuss,Edgar A Deyoe,Wendy E Huddleston,Amy B Mathew,Jay J Pillai,Jedidiah R Mathis

doi:10.3389/fnins.2021.654957

Abstract

Functional magnetic resonance imaging for presurgical brain mapping enables neurosurgeons to identify viable tissue near a site of operable pathology which might be at risk of surgery-induced damage. However, focal brain pathology (e.g., tumors) may selectively disrupt neurovascular coupling while leaving the underlying neurons functionally intact. Such neurovascular uncoupling can result in false negatives on brain activation maps thereby compromising their use for surgical planning. One way to detect potential neurovascular uncoupling is to map cerebrovascular reactivity using either an active breath-hold challenge or a passive resting-state scan. The equivalence of these two methods has yet to be fully established, especially at a voxel level of resolution. To quantitatively compare breath-hold and resting-state maps of cerebrovascular reactivity, we first identified threshold settings that optimized coverage of gray matter while minimizing false responses in white matter. When so optimized, the resting-state metric had moderately better gray matter coverage and specificity. We then assessed the spatial correspondence between the two metrics within cortical gray matter, again, across a wide range of thresholds. Optimal spatial correspondence was strongly dependent on threshold settings which if improperly set tended to produce statistically biased maps. When optimized, the two CVR maps did have moderately good correspondence with each other (mean accuracy of 73.6%). Our results show that while the breath-hold and resting-state maps may appear qualitatively similar they are not quantitatively identical at a voxel level of resolution.

Highlights

The use of blood oxygenation level dependent (BOLD) functional MRI for presurgical brain mapping permits safer, more effective, surgery by allowing neurosurgeons to identify functional cortex close to a site of operable pathology (Hart, 2007; Pillai, 2010; Jenkinson et al, 2018; Vysotski et al, 2018)
In accordance with the structure of our data analysis, we discuss the results in two main sections: (1) The association of CVRresponsive voxels with gray vs. white matter and (2) a voxel-wise comparison of the breath-hold cerebrovascular reactivity (CVR) and resting-state CVRe maps with each other
The accuracy was calculated as the summation of CVR-responsive voxels in gray matter and non-responsive voxels in white matter relative to the total number of voxels (Equation 3 above)

Summary

Introduction

The use of blood oxygenation level dependent (BOLD) functional MRI (fMRI) for presurgical brain mapping permits safer, more effective, surgery by allowing neurosurgeons to identify functional (eloquent) cortex close to a site of operable pathology (Hart, 2007; Pillai, 2010; Jenkinson et al, 2018; Vysotski et al, 2018). The neurovascular coupling mechanism that underlies task-evoked BOLD responses can be disrupted by focal brain pathology (e.g., tumor), causing reduced or absent fMRI signals despite the presence of functionally intact neurons (Holodny et al, 2000; Ulmer et al, 2004; Burke and Buhrle, 2006; Hou et al, 2006; Pak et al, 2017; Silva et al, 2017; Voss et al, 2019) Such “neurovascular uncoupling” (NVU) thereby causes false negatives on the fMRI task-activation maps (Ulmer et al, 2003; Pillai and Mikulis, 2014; Zaca et al, 2014; Para et al, 2017). If NVU is undetected, aggressive surgery could result in resection of eloquent cortex, thereby causing severe post-treatment neurological deficits and a diminished quality of life for the patient (Zaca et al, 2011; Rahman et al, 2016)

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