Bogard Alysha T, Hemmerle Makenna R, Smith Andrew C, Tan Andrew Q
Sensorimotor Recovery and Neuroplasticity Lab at the University of Colorado, Boulder, CO, USA.
Dept. of Physical Medicine and Rehabilitation, University of Colorado School of Medicine, Aurora, CO, USA.
J Physiol. 2024 Nov;602(21):5879-5899. doi: 10.1113/JP285425. Epub 2023 Nov 20.
Breathing mild bouts of low oxygen air (i.e. acute intermittent hypoxia, AIH) has been shown to improve locomotor function in humans after a spinal cord injury. How AIH-induced gains in motor performance are achieved remains unclear. We examined the hypothesis that AIH augments motor learning and motor retention during a locomotor adaptation task. We further hypothesized that gains in motor learning and retention will be associated with reductions in net metabolic power, consistent with the acquisition of energetically favourable mechanics. Thirty healthy individuals were randomly allocated into either a control group or an AIH group. We utilized a split-belt treadmill to characterize adaptations to an unexpected belt speed perturbation of equal magnitude during an initial exposure and a second exposure. Adaptation was characterized by changes in spatiotemporal step asymmetry, anterior-posterior force asymmetry, and net metabolic power. While both groups adapted by reducing spatial asymmetry, only the AIH group achieved significant reductions in double support time asymmetry and propulsive force asymmetry during both the initial and the second exposures to the belt speed perturbation. Net metabolic power was also significantly lower in the AIH group, with significant reductions from the initial perturbation exposure to the second. These results provide the first evidence that AIH mediates improvements in both motor learning and retention. Further, our results suggest that reductions in net metabolic power continue to be optimized upon subsequent learning and are driven by more energetically favourable temporal coordination strategies. Our observation that AIH facilitates motor learning and retention can be leveraged to design rehabilitation interventions that promote functional recovery. KEY POINTS: Brief exposures to low oxygen air, known as acute intermittent hypoxia (AIH), improves locomotor function in humans after a spinal cord injury, but it remains unclear how gains in motor performance are achieved. In this study, we tested the hypothesis that AIH induces enhancements in motor learning and retention by quantifying changes in interlimb coordination, anterior-posterior force symmetry and metabolic cost during a locomotor adaptation task. We show the first evidence that AIH improves both motor learning and savings of newly learned temporal interlimb coordination strategies and force asymmetry compared to untreated individuals. We further demonstrate that AIH elicits greater reductions in metabolic cost during motor learning that continues to be optimized upon subsequent learning. Our findings suggest that AIH-induced gains in locomotor performance are facilitated by enhancements in motor learning and retention of more energetically favourable coordination strategies.
已证明,呼吸轻度间歇性低氧空气(即急性间歇性缺氧,AIH)可改善脊髓损伤后人的运动功能。目前尚不清楚AIH是如何实现运动表现提升的。我们检验了这样一种假设,即AIH在运动适应任务中增强运动学习和运动记忆。我们进一步假设,运动学习和记忆的提升将与净代谢功率的降低相关,这与获得能量上有利的力学机制一致。30名健康个体被随机分为对照组或AIH组。我们使用分带跑步机来表征在初次暴露和再次暴露期间对同等幅度的意外带速扰动的适应情况。适应情况通过时空步长不对称性、前后力不对称性和净代谢功率的变化来表征。虽然两组都通过减少空间不对称性来适应,但只有AIH组在初次和再次暴露于带速扰动期间,双支撑时间不对称性和推进力不对称性都有显著降低。AIH组的净代谢功率也显著更低,从初次扰动暴露到再次暴露有显著降低。这些结果首次证明AIH介导了运动学习和记忆的改善。此外,我们的结果表明,净代谢功率在后续学习中持续优化,并由更有利于能量利用的时间协调策略驱动。我们观察到AIH促进运动学习和记忆,这可用于设计促进功能恢复的康复干预措施。要点:短暂暴露于低氧空气,即急性间歇性缺氧(AIH),可改善脊髓损伤后人的运动功能,但尚不清楚如何实现运动表现的提升。在本研究中,我们通过量化运动适应任务期间肢体间协调性、前后力对称性和代谢成本的变化,检验了AIH诱导运动学习和记忆增强的假设。我们首次证明,与未治疗个体相比,AIH改善了运动学习以及新习得的肢体间时间协调性策略和力不对称性的保留。我们进一步证明,AIH在运动学习期间引起更大的代谢成本降低,并且在后续学习中持续优化。我们的研究结果表明,运动学习的增强和保留更有利于能量利用的协调策略促进了AIH诱导的运动表现提升。