Department of Biomedical Engineering, McGill University, Montreal, Quebec, Canada.
Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University, Baltimore, Maryland, USA.
J Physiol. 2021 Apr;599(8):2239-2254. doi: 10.1113/JP281183. Epub 2021 Mar 10.
Sensory systems are adapted to the statistical structure of natural stimuli, thereby optimizing neural coding. Head motion during natural activities is first sensed and then processed by central vestibulo-motor pathways to influence subsequent behaviour, thereby establishing a feedback loop. To investigate the role of this vestibular feedback on the statistical structure of the head movements, we compared head movements in patients with unilateral vestibular loss and healthy controls. We show that the loss of vestibular feedback substantially alters the statistical structure of head motion for activities that require rapid online feedback control and predict this change by modelling the effects of increased movement variability. Our findings suggest that, following peripheral vestibular loss, changes in the reliability of the sensory input to central pathways impact the statistical structure of head motion during voluntary behaviours.
It is widely believed that sensory systems are adapted to optimize neural coding of their natural stimuli. Recent evidence suggests that this is the case for the vestibular system, which senses head movement and contributes to essential functions ranging from the most automatic reflexes to voluntary motor control. During everyday behaviours, head motion is sensed by the vestibular system. In turn, this sensory feedback influences subsequent behaviour, raising the questions of whether and how real-time feedback provided by the vestibular system alters the statistical structure of head movements. We predicted that a reduction in vestibular feedback would alter head movement statistics, particularly for tasks reliant on rapid vestibular feedback. To test this proposal, we recorded six-dimensional head motion in patients with variable degrees of unilateral vestibular loss during standard balance and gait tasks, as well as dynamic self-paced activities. While distributions of linear accelerations and rotational velocities were comparable for patients and age-matched healthy controls, comparison of power spectra revealed significant differences during more dynamic and challenging activities. Specifically, consistent with our prediction, head movement power spectra were significantly altered in patients during two tasks that required rapid online vestibular feedback: active repetitive jumping and walking on foam. Using computational methods, we analysed concurrently measured torso motion and identified increases in head-torso movement variability. Taken together, our results demonstrate that vestibular loss significantly alters head movement statistics and further suggest that increased variability and impaired feedback to internal models required for accurate motor control contribute to the observed changes.
感觉系统适应自然刺激的统计结构，从而优化神经编码。在自然活动期间，头部运动首先被感知，然后被中央前庭运动通路处理，以影响随后的行为，从而建立一个反馈回路。为了研究这种前庭反馈对头部运动统计结构的作用，我们比较了单侧前庭损失患者和健康对照者的头部运动。我们表明，前庭反馈的丧失会极大地改变需要快速在线反馈控制的活动的头部运动的统计结构，并通过建模增加运动可变性的影响来预测这种变化。我们的发现表明，在周围性前庭损失后，传入中央通路的感觉输入的可靠性变化会影响自愿行为期间头部运动的统计结构。
人们普遍认为，感觉系统适应于优化其自然刺激的神经编码。最近的证据表明，这种情况适用于前庭系统，它感知头部运动，并有助于从最自动的反射到自愿运动控制的基本功能。在日常行为中，头部运动被前庭系统感知。反过来，这种感觉反馈会影响随后的行为，提出了这样一个问题，即前庭系统提供的实时反馈是否以及如何改变头部运动的统计结构。我们预测，前庭反馈的减少会改变头部运动的统计数据，特别是对于依赖快速前庭反馈的任务。为了验证这一假设，我们在有不同程度单侧前庭损失的患者中记录了标准平衡和步态任务以及动态自我调节活动期间的六维头部运动。虽然患者和年龄匹配的健康对照组的线性加速度和旋转速度分布相似，但对功率谱的比较显示，在更动态和更具挑战性的活动中存在显著差异。具体而言，与我们的预测一致，在需要快速在线前庭反馈的两项任务中，患者的头部运动功率谱发生了显著变化：主动重复跳跃和在泡沫上行走。使用计算方法，我们分析了同时测量的躯干运动，并确定头部-躯干运动的可变性增加。总的来说，我们的结果表明，前庭损失显著改变了头部运动的统计数据，并进一步表明，增加的可变性和受损的反馈到内部模型，以实现准确的运动控制，有助于观察到的变化。
