Motor control requires a coordinated ensemble of spatiotemporally precise neural oscillations across a distributed motor network, particularly in the beta range (15 to 30 Hz) to successfully plan and execute volitional actions. While substantial evidence implicates beta activity as critical to motor control, the molecular processes supporting these microcircuits and their inherent oscillatory dynamics remain poorly understood. Among these processes are mitochondrial integrity and the associated redox environments, although their direct impact on human neurophysiological function is unknown. Herein, 40 healthy adults completed a motor sequence paradigm during magnetoencephalography (MEG). MEG data were imaged in the time–frequency domain using a beamformer to evaluate beta oscillatory profiles during distinct phases of motor control (i.e., planning and execution) and subsequent behavior. To comprehensively quantify features of the mitochondrial redox environment, we used state-of-the-art systems biology approaches including Seahorse Analyzer to assess mitochondrial respiration and electron paramagnetic resonance spectroscopy to measure superoxide levels in whole blood as well as antioxidant activity assays. Using structural equation modeling, we tested the relationship between mitochondrial function and sensorimotor brain-behavior dynamics through alterations in the redox environment (e.g., generation of superoxide and alteration in antioxidant defenses). Our results indicated that superoxide-sensitive but not hydrogen peroxide–sensitive features of the redox environment had direct and mediating effects on the bioenergetic–neural pathways serving motor performance in healthy adults. Importantly, our results suggest that alterations in the redox environment may directly impact behavior above and beyond mitochondrial respiratory capacities alone and further may be effective targets for age- and disease-related declines in cognitive–motor function.

运动控制需要跨分布式运动网络的时空精确神经振荡的协调合奏，特别是在 beta 范围（15 到 30 Hz）中，以成功计划和执行意志行动。虽然大量证据表明 beta 活动对运动控制至关重要，但支持这些微电路的分子过程及其固有的振荡动力学仍然知之甚少。这些过程包括线粒体完整性和相关的氧化还原环境，尽管它们对人类神经生理功能的直接影响尚不清楚。在此，40 名健康成年人在脑磁图 (MEG) 期间完成了运动序列范例。MEG 数据使用波束形成器在时频域成像，以评估电机控制不同阶段的 β 振荡曲线（即，计划和执行）以及随后的行为。为了全面量化线粒体氧化还原环境的特征，我们使用了最先进的系统生物学方法，包括海马分析仪来评估线粒体呼吸和电子顺磁共振光谱来测量全血中的超氧化物水平以及抗氧化活性测定。我们使用结构方程模型，通过氧化还原环境的改变（例如，超氧化物的产生和抗氧化防御的改变）测试了线粒体功能与感觉运动大脑行为动力学之间的关系。我们的研究结果表明，氧化还原环境的超氧化物敏感而非过氧化氢敏感特征对健康成人的运动表现的生物能神经通路具有直接和中介作用。