Habituation of vestibular-evoked balance responses after repeated exposure to a postural threat

IF 4.4 2区 医学 Q1 NEUROSCIENCES Journal of Physiology-London Pub Date : 2025-02-21 DOI:10.1113/JP287391
Martin Zaback, Solenne Villemer, Kyle J. Missen, J. Timothy Inglis, Mark G. Carpenter
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Abstract

Vestibular-evoked balance responses are facilitated when faced with threats to stability. However, the extent to which these sensorimotor adaptations covary with changes in emotional and autonomic state remains unclear. This study repeatedly exposed individuals to the same postural threat while vestibular-motor responses were probed using stochastic vestibular stimulation (SVS; 2–25 Hz). This allowed emotional and autonomic state to be manipulated within the same threat environment to determine if vestibular-evoked balance responses are coupled with the emotional/autonomic changes induced by the threat or are facilitated in a strictly context-dependent manner. Twenty-three young adults stood with their head turned 90° while receiving SVS at LOW (0.8 m above ground, away from edge) and HIGH (3.2 m above ground, at edge) conditions. LOW trials were completed before and after a block of 10 HIGH trials. Ground reaction forces (GRFs) and plantar flexor (soleus and medial gastrocnemius (MG)) EMG were recorded. Vestibular-evoked responses recorded from GRFs and EMG were quantified in terms of signal coupling (coherence and cumulant density) and gain, and emotional and autonomic state were assessed from self-reports and electrodermal activity. Vestibular-evoked balance responses were facilitated with initial threat exposure. After repeated exposure, there was significant habituation of the emotional response to threat, which was accompanied by reductions in vestibular-evoked balance responses, most notably for GRFs and MG-EMG. This suggests that threat-related changes in vestibular-motor function are tightly coupled with the emotional and autonomic changes induced by the threat, and not an invariant response to context-specific features of the threat.

Key points

  • Balance corrective responses mediated through vestibular-motor pathways are facilitated when stability is threatened; however, the extent to which these sensorimotor adaptations covary with changes in emotional state remains unclear.
  • By having young adults repeatedly stand at the edge of an elevated surface, this study examined how vestibular-evoked balance responses, probed using stochastic vestibular stimulation and recorded from ground reaction forces and plantar flexor EMG, changed alongside estimates of emotional state.
  • Vestibular-evoked responses were facilitated when individuals were first exposed to the postural threat, but demonstrated marked habituation alongside estimates of emotional state after repeated exposure.
  • This suggests that threat-related changes in vestibular-motor function are coupled to the emotional response to threat, and are not an invariant response to context-specific features of the threat.
  • These changes in vestibular-motor function are likely part of a multisensory adaptation process that primes the nervous system to respond to sudden destabilizing forces when fearful of falling.

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反复暴露于姿势威胁后前庭诱发平衡反应的习惯化。
当面对稳定性的威胁时,前庭诱发的平衡反应会得到促进。然而,这些感觉运动适应在多大程度上随情绪和自主状态的变化而变化仍不清楚。本研究反复暴露个体于相同的姿势威胁,同时使用随机前庭刺激(SVS;2-25赫兹)。这允许在相同的威胁环境中操纵情绪和自主状态,以确定前庭诱发的平衡反应是否与威胁引起的情绪/自主变化相结合,还是以严格依赖于上下文的方式促进。23名年轻人在低(离地面0.8米,远离边缘)和高(离地面3.2米,在边缘)条件下接受SVS时,头部转向90°。LOW试验在10个HIGH试验之前和之后完成。记录地面反作用力(GRFs)和足底屈肌(比目鱼肌和腓肠肌内侧肌)肌电图。根据grf和EMG记录的前庭诱发反应的信号耦合(相干性和累积密度)和增益进行量化,并根据自我报告和皮电活动评估情绪和自主状态。前庭诱发平衡反应在初始威胁暴露下得到促进。反复暴露后,对威胁的情绪反应出现了明显的习惯化,这伴随着前庭诱发的平衡反应的减少,尤其是grf和MG-EMG。这表明,与威胁相关的前庭运动功能变化与威胁引起的情绪和自主神经变化紧密相关,而不是对威胁的特定环境特征的不变反应。重点:当稳定性受到威胁时,通过前庭-运动通路介导的平衡纠正反应得到促进;然而,这些感觉运动适应在多大程度上随情绪状态的变化而变化仍不清楚。通过让年轻人反复站在高表面的边缘,本研究通过随机前庭刺激来探测前庭诱发的平衡反应,并记录地面反力和足底屈肌肌电图,研究了前庭诱发的平衡反应如何随着情绪状态的估计而变化。当个体第一次暴露于姿势威胁时,前庭诱发反应得到促进,但在重复暴露后表现出明显的习惯化和情绪状态估计。这表明,前庭运动功能中与威胁相关的变化与对威胁的情绪反应相关联,而不是对威胁的情境特定特征的不变反应。前庭运动功能的这些变化很可能是多感觉适应过程的一部分,该过程使神经系统在害怕跌倒时对突然的不稳定力量作出反应。
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来源期刊
Journal of Physiology-London
Journal of Physiology-London 医学-神经科学
CiteScore
9.70
自引率
7.30%
发文量
817
审稿时长
2 months
期刊介绍: The Journal of Physiology publishes full-length original Research Papers and Techniques for Physiology, which are short papers aimed at disseminating new techniques for physiological research. Articles solicited by the Editorial Board include Perspectives, Symposium Reports and Topical Reviews, which highlight areas of special physiological interest. CrossTalk articles are short editorial-style invited articles framing a debate between experts in the field on controversial topics. Letters to the Editor and Journal Club articles are also published. All categories of papers are subjected to peer reivew. The Journal of Physiology welcomes submitted research papers in all areas of physiology. Authors should present original work that illustrates new physiological principles or mechanisms. Papers on work at the molecular level, at the level of the cell membrane, single cells, tissues or organs and on systems physiology are all acceptable. Theoretical papers and papers that use computational models to further our understanding of physiological processes will be considered if based on experimentally derived data and if the hypothesis advanced is directly amenable to experimental testing. While emphasis is on human and mammalian physiology, work on lower vertebrate or invertebrate preparations may be suitable if it furthers the understanding of the functioning of other organisms including mammals.
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