Neurovascular and cortical responses to hyperoxia: enhanced cognition and electroencephalographic activity despite reduced perfusion

• Published in: The Journal of physiology 2020-09, Vol.598 (18), p.3941-3956
• Main Authors: Damato, Elizabeth G., Flak, Tod A., Mayes, Ryan S., Strohl, Kingman P., Ziganti, Aemilee M., Abdollahifar, Alireza, Flask, Chris A., LaManna, Joseph C., Decker, Michael J.
• Format: Article
• Language: English
• Subjects: Arousal; Carbon dioxide; Cerebral blood flow; cerebral perfusion; Cerebrovascular Circulation; Cognition; Cognition & reasoning; Cognitive ability; Decompression; EEG; EEG (electroencephalography); Electroencephalography; Female; Gases; Humans; Hyperoxia; Hypoxia; Information processing; Magnetic resonance imaging; Male; MRI (magnetic resonance imaging); Neuroprotection; Oxygen; Perfusion; Physiology; pulsed arterial spin labelling; Spin labeling; Synchronization
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/JP279453

Key points Extreme aviation is accompanied by ever‐present risks of hypobaric hypoxia and decompression sickness. Neuroprotection against those hazards is conferred through fractional inspired oxygen (FI,O2) concentrations of 60–100% (hyperoxia). Hyperoxia reduces global cerebral perfusion (gCBF), increases reactive oxygen species within the brain and leads to cell death within the hippocampus. However, an understanding of hyperoxia's effect on cortical activity and concomitant levels of cognitive performance is lacking. This limits our understanding of whether hyperoxia could lower the brain's threshold of tolerance to physiological stressors inherent to extreme aviation, such as high gravitational forces. This study aimed to quantify the impact of hyperoxia upon global cerebral perfusion (gCBF), cognitive performance and cortical electroencephalography (EEG). Hyperoxia evoked a rapid reduction in gCBF, yet cognitive performance and vigilance were enhanced. EEG measurements revealed enhanced alpha power, suggesting less desynchrony, within the cortical temporal regions. Collectively, this work suggests hyperoxia‐induced brain hypoperfusion is accompanied by enhanced cognitive processing and cortical arousal. Extreme aviators continually inspire hyperoxic gas to mitigate risk of hypoxia and decompression injury. This neuroprotection carries a physiological cost: reduced cerebral perfusion (CBF). As reduced CBF may increase vulnerability to ever‐present physiological challenges during extreme aviation, we defined the magnitude and duration of hyperoxia‐induced changes in CBF, cortical electrical activity and cognition in 30 healthy males and females. Magnetic resonance imaging with pulsed arterial spin labelling provided serial measurements of global CBF (gCBF), first during exposure to 21% inspired oxygen (FI,O2) followed by a 30‐min exposure to 100% FI,O2. High‐density EEG facilitated characterization of cortical activity during assessment of cognitive performance, also measured during exposure to 21% and 100% FI,O2. Acid‐base physiology was measured with arterial blood gases. We found that exposure to 100% FI,O2 reduced gCBF to 63% of baseline values across all participants. Cognitive performance testing at 21% FI,O2 was accompanied by increased theta and beta power with decreased alpha power across multiple cortical areas. During cognitive testing at 100% FI,O2, alpha activity was less desynchronized within the temporal regions than at 21% FI,O2. The co