Heterogeneous motor BOLD-fMRI responses in brain areas exhibiting negative BOLD cerebrovascular reactivity indicate that steal phenomenon does not always result from exhausted cerebrovascular reserve capacity

Christiaan Hendrik Bas van Niftrik; Aimée Hiller; Martina Sebök; Matthias Halter; James Duffin; Joseph A Fisher; David J Mikulis; Luca Regli; Marco Piccirelli; Jorn Fierstra

doi:10.1016/j.mri.2023.07.010

Heterogeneous motor BOLD-fMRI responses in brain areas exhibiting negative BOLD cerebrovascular reactivity indicate that steal phenomenon does not always result from exhausted cerebrovascular reserve capacity

Magn Reson Imaging. 2023 Nov:103:124-130. doi: 10.1016/j.mri.2023.07.010. Epub 2023 Jul 21.

Affiliations

¹ Department of Neurosurgery, University Hospital Zurich, University of Zurich, Switzerland; Clinical Neuroscience Center, University Hospital Zurich, Switzerland. Electronic address: bas.vanniftrik@usz.ch.
² Department of Neurosurgery, University Hospital Zurich, University of Zurich, Switzerland; Clinical Neuroscience Center, University Hospital Zurich, Switzerland; Department of Abdominal and Transplant Surgery, University Hospital Zurich, University of Zurich. Switzerland.
³ Department of Neurosurgery, University Hospital Zurich, University of Zurich, Switzerland; Clinical Neuroscience Center, University Hospital Zurich, Switzerland.
⁴ Department of Physiology, University of Toronto, Toronto, ON, Canada.
⁵ Department of Anesthesia and Pain Management, University Health Network, Toronto, ON, Canada.; Institute of Medical Science, University of Toronto, Toronto, ON, Canada.
⁶ Joint Department of Medical Imaging and the Functional Neuroimaging Laboratory, University Health Network, Toronto, ON, Canada.
⁷ Clinical Neuroscience Center, University Hospital Zurich, Switzerland; Department of Neuroradiology, University Hospital Zurich, University of Zurich, Switzerland.

PMID: 37481092
DOI: 10.1016/j.mri.2023.07.010

Abstract

Introduction: Brain areas exhibiting negative blood oxygenation-level dependent cerebrovascular reactivity (BOLD-CVR) responses to carbon dioxide (CO₂) are thought to suffer from a completely exhausted autoregulatory cerebrovascular reserve capacity and exhibit vascular steal phenomenon. If this assumption is correct, the presence of vascular steal phenomenon should subsequently result in an equal negative fMRI signal response during a motor-task based BOLD-fMRI study (increase in metabolism without an increase in cerebral blood flow due to exhausted reserve capacity) in otherwise functional brain tissue. To investigate this premise, the aim of this study was to further investigate motor-task based BOLD-fMRI signal responses in brain areas exhibiting negative BOLD-CVR.

Material and methods: Seventy-one datasets of patients with cerebrovascular steno-occlusive disease without motor defects, who underwent a CO₂-calibrated motor task-based BOLD-fMRI study with a fingertapping paradigm and a subsequent BOLD-CVR study with a precisely controlled CO₂-challenge during the same MRI examination, were included. We compared BOLD-fMRI signal responses in the bilateral pre- and postcentral gyri - i.e. Region of Interest (ROI) with the corresponding BOLD-CVR in this ROI. The ROI was determined using a second level group analysis of the BOLD-fMRI task study of 42 healthy individuals undergoing the same study protocol.

Results: An overall decrease in BOLD-CVR was associated with a decrease in BOLD-fMRI signal response within the ROI. For patients exhibiting negative BOLD-CVR, we found both positive and negative motor-task based BOLD-fMRI signal responses.

Conclusion: We show that the presence of negative BOLD-CVR responses to CO₂ is associated with heterogeneous motor task-based BOLD-fMRI signal responses, where some patients show -more presumed- negative BOLD-fMRI signal responses, while other patient showed positive BOLD-fMRI signal responses. This finding may indicate that the autoregulatory vasodilatory reserve capacity does not always need to be completely exhausted for vascular steal phenomenon to occur.

Keywords: BOLD; Cerebrovascular reactivity; Task-based BOLD-fMRI; Vascular steal phenomenon.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brain / blood supply
Brain / diagnostic imaging
Carbon Dioxide
Cerebrovascular Circulation / physiology
Cerebrovascular Disorders*
Humans
Magnetic Resonance Imaging* / methods

Substances

Carbon Dioxide