Prefrontal executive function enhanced by prior acute inhalation of low-dose hypoxic gas: Modulation via cardiac vagal activity

IF 4.7 2区医学 Q1 NEUROIMAGING

NeuroImage Pub Date : 2025-03-17 DOI:10.1016/j.neuroimage.2025.121139

Dongmin Lee , Yudai Yamazaki , Ryuta Kuwamizu , Masahiro Okamoto , Hideaki Soya

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Abstract

Today, diverse psychophysiological stresses, such as severe time constraints and busy lifestyles, contribute to cardiac parasympathetic dysfunction, potentially leading to mental health issues and declines in critical executive functions. It is essential to develop accessible methods of enhancing cardiac vagal activity (CVA) to mitigate these adverse effects. We previously demonstrated that inhaling low-dose hypoxic gas (FIO₂: 13.5 %) for 10 min acts as a hormetic stressor, inducing a supercompensation effect in CVA post-hypoxia. Since CVA is a key mediator of brain-heart communication in that it influences executive functions by interacting with the left dorsolateral prefrontal cortex (L-DLPFC), increasing CVA may enhance cognitive ability. We hypothesized that acute low-dose hypoxia leads to enhanced executive function via CVA modulation. Twenty-six individuals participated in both normobaric hypoxia (NH; FIO₂: 13.5 %) and normoxia (NN; ambient air) conditions. CVA, measured through heart rate variability, was analyzed three times: pre-hypoxia/normoxia, hypoxia/normoxia, and post-hypoxia/normoxia. Executive function was assessed using the Stroop task before and after exposure, and prefrontal cortex activity during the task was monitored using multichannel functional near-infrared spectroscopy. A supercompensation of CVA occurred concomitantly with a reduction in heart rate following hypoxic gas inhalation. Stroop performance improved with increased task-related activation of the L-DLPFC in the NH condition. Causal mediation analysis revealed that the post-hypoxia enhancement of CVA mediated improvements in Stroop performance and increased L-DLPFC activation. These findings strongly support our hypothesis that the enhancement of CVA following hormetic hypoxic stress contributes to improved executive function, broadening the scope of neurocognitive approaches for effectively enhancing executive function.

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先前急性吸入低剂量低氧气体增强前额叶执行功能：通过心脏迷走神经活动调节

今天，各种心理生理压力，如严重的时间限制和繁忙的生活方式，导致心脏副交感神经功能障碍，可能导致心理健康问题和关键执行功能下降。因此，有必要开发易于使用的方法来增强心脏迷走神经活动（CVA），以减轻这些不利影响。我们之前证明，吸入低剂量缺氧气体（fio2: 13.5%） 10分钟可作为应激源，诱导缺氧后CVA的超补偿效应。由于CVA通过与左背外侧前额叶皮质（L-DLPFC）相互作用而影响执行功能，因此CVA是脑心通讯的关键中介，增加CVA可能会增强认知能力。我们假设急性低剂量缺氧通过CVA调节导致执行功能增强。26个个体分别参加了常压缺氧(NH；FIO₂：13.5%)和常氧(NN；环境空气条件。通过心率变异性测量CVA，分析三次：缺氧前/正常缺氧，缺氧/正常缺氧和缺氧后/正常缺氧。在暴露前后使用Stroop任务评估执行功能，并使用多通道功能近红外光谱监测任务期间前额叶皮层的活动。低氧气体吸入后，CVA的超代偿与心率降低同时发生。在NH条件下，随着L-DLPFC任务相关激活的增加，Stroop的表现也有所改善。因果中介分析显示，缺氧后CVA的增强介导Stroop表现的改善和L-DLPFC激活的增加。这些发现有力地支持了我们的假设，即有氧缺氧应激后CVA的增强有助于改善执行功能，拓宽了有效增强执行功能的神经认知方法的范围。

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来源期刊

NeuroImage 医学-核医学

CiteScore

11.30

自引率

10.50%

发文量

809

审稿时长

63 days

期刊介绍： NeuroImage, a Journal of Brain Function provides a vehicle for communicating important advances in acquiring, analyzing, and modelling neuroimaging data and in applying these techniques to the study of structure-function and brain-behavior relationships. Though the emphasis is on the macroscopic level of human brain organization, meso-and microscopic neuroimaging across all species will be considered if informative for understanding the aforementioned relationships.