Motor control or the art of betting

IF 4.4 2区 医学 Q1 NEUROSCIENCES Journal of Physiology-London Pub Date : 2025-03-25 DOI:10.1113/JP288801
Pierre-Paul Vidal
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Secondary vestibular neurons in the brainstem take their name from the fact that they receive primary vestibular afferents. However, as we later realized, these neurons also receive proprioceptive inputs, mainly from the neuromuscular spindles of the 48 neck muscles, and visual inputs via the accessory optic system. This explains why, when you are sitting on a train and the train next to you leaves, you feel your own train moving. As a result, second-order vestibular neurons actually develop an internal multimodal representation of head and body movement in space. This representation is used to stabilize gaze and posture, to generate an awareness of movement and to allow separation between one's own movement and externally generated movement. In this context, can we still talk about vestibular neurons? Should we ask ourselves whether the central nervous system preserves ‘vestibular, visual and proprioceptive’ information or whether it mixes these inputs in the service of a multimodal representation of the world for frequency tuned channel? In the light of electrophysiological work on animal models, several types of multimodal representation of our own movement probably coexist in the vestibular nucleus, with variable weighting for visual and proprioceptive vestibular afferents.</p><p>And that's not all. The so-called ‘vestibular’ neurons also receive cerebellar and cortical inputs, and their activity is modulated by several neuromodulators involved in vigilance, emotional and autonomic changes. This partly explains the results obtained by Zaback et al. (<span>2025</span>) and Cullen (<span>2023</span>), which show that we are a long way from a 19th century conception of postural control as the result of the sum of elementary reflexes. We are confronted with ultra-rapid representations elaborated by the CNS on the basis of a cocktail of sensory inputs, the actual level of vigilance, and the affective and probably social context. In around 200 ms, these are used to develop coherent representations of a fluctuating world, which are necessary to stabilize our gaze, control our posture, distinguish between someone pushing us and a movement we have initiated; in short, to avoid motor disasters.</p><p>In such critical situations, we might expect everyone's control of their gaze and posture to be relatively uniform in identical circumstances. This is not the case, as Zaback et al. (<span>2025</span>) and others have shown. All neurophysiologists who work on sensory-motor transformations, whether in animal models or in humans, learn that the more ecological the context in which they work and the more precise their measurements of behaviour, the greater the differences between individuals. In other words, the question is not just to understand how, on the basis of multimodal representations influenced by context, we reconstruct a reality that enables us to act. It is also about understanding how different people reach different conclusions when it comes to regulating their motor control. In other words, each of us has our own perceptual-motor style (for a review, see Vidal et al., <span>2021</span>) and even more so in pathological states. The consequence is that the average of behaviours in a cohort can be misleading. Each person, when the control of gaze and posture is challenged, takes a different view of the risks to which she/he is exposed and therefore adopts different solutions to resolve the problem. This is why individual longitudinal monitoring is becoming a key element in the study of motor control.</p><p>Also, being a permanent biped is a risky game. Uncertain prediction and/or the adoption of poor muscular synergies lead to a fall to the ground 500 ms later, around 700 ms after the start of a postural perturbation. Furthermore, falls are the second leading cause of death by unintentional trauma in the world, not to mention the various injuries they cause and the loss of independence of the elderly. The study by Zaback et al. (<span>2025</span>) and previous others and previous studies show that control of gaze and posture, far from being a series of reflexes, is a question of ultra-rapid bets, not predictions, to assess the risks, and the optimal motor programs aiming to avoid them. These strategies have communalities between individuals (we rarely bet at random). They also define different styles for different individuals and unreasonable betting leads to neuroses (acrophobia, fear of falling). These considerations are probably even truer when pathological processes and their rehabilitation are involved. 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引用次数: 0

Abstract

The study by Zaback et al. (2025) in the present issue of The Journal of Physiology involved repeatedly exposing individuals to the same postural threat at the same time as probing vestibular and motor responses using stochastic vestibular stimulation. This made it possible to manipulate the emotional and autonomic state in the context of the same threat. Their results suggest that threat-related changes in vestibular and motor function are closely related to threat-induced emotional and autonomic changes, and are not an invariant response to specific contextual features of the threat. This study, which is very interesting in itself, raises some fascinating questions about sensorimotor transformations.

One of these concerns the status of sensory information in the CNS. Secondary vestibular neurons in the brainstem take their name from the fact that they receive primary vestibular afferents. However, as we later realized, these neurons also receive proprioceptive inputs, mainly from the neuromuscular spindles of the 48 neck muscles, and visual inputs via the accessory optic system. This explains why, when you are sitting on a train and the train next to you leaves, you feel your own train moving. As a result, second-order vestibular neurons actually develop an internal multimodal representation of head and body movement in space. This representation is used to stabilize gaze and posture, to generate an awareness of movement and to allow separation between one's own movement and externally generated movement. In this context, can we still talk about vestibular neurons? Should we ask ourselves whether the central nervous system preserves ‘vestibular, visual and proprioceptive’ information or whether it mixes these inputs in the service of a multimodal representation of the world for frequency tuned channel? In the light of electrophysiological work on animal models, several types of multimodal representation of our own movement probably coexist in the vestibular nucleus, with variable weighting for visual and proprioceptive vestibular afferents.

And that's not all. The so-called ‘vestibular’ neurons also receive cerebellar and cortical inputs, and their activity is modulated by several neuromodulators involved in vigilance, emotional and autonomic changes. This partly explains the results obtained by Zaback et al. (2025) and Cullen (2023), which show that we are a long way from a 19th century conception of postural control as the result of the sum of elementary reflexes. We are confronted with ultra-rapid representations elaborated by the CNS on the basis of a cocktail of sensory inputs, the actual level of vigilance, and the affective and probably social context. In around 200 ms, these are used to develop coherent representations of a fluctuating world, which are necessary to stabilize our gaze, control our posture, distinguish between someone pushing us and a movement we have initiated; in short, to avoid motor disasters.

In such critical situations, we might expect everyone's control of their gaze and posture to be relatively uniform in identical circumstances. This is not the case, as Zaback et al. (2025) and others have shown. All neurophysiologists who work on sensory-motor transformations, whether in animal models or in humans, learn that the more ecological the context in which they work and the more precise their measurements of behaviour, the greater the differences between individuals. In other words, the question is not just to understand how, on the basis of multimodal representations influenced by context, we reconstruct a reality that enables us to act. It is also about understanding how different people reach different conclusions when it comes to regulating their motor control. In other words, each of us has our own perceptual-motor style (for a review, see Vidal et al., 2021) and even more so in pathological states. The consequence is that the average of behaviours in a cohort can be misleading. Each person, when the control of gaze and posture is challenged, takes a different view of the risks to which she/he is exposed and therefore adopts different solutions to resolve the problem. This is why individual longitudinal monitoring is becoming a key element in the study of motor control.

Also, being a permanent biped is a risky game. Uncertain prediction and/or the adoption of poor muscular synergies lead to a fall to the ground 500 ms later, around 700 ms after the start of a postural perturbation. Furthermore, falls are the second leading cause of death by unintentional trauma in the world, not to mention the various injuries they cause and the loss of independence of the elderly. The study by Zaback et al. (2025) and previous others and previous studies show that control of gaze and posture, far from being a series of reflexes, is a question of ultra-rapid bets, not predictions, to assess the risks, and the optimal motor programs aiming to avoid them. These strategies have communalities between individuals (we rarely bet at random). They also define different styles for different individuals and unreasonable betting leads to neuroses (acrophobia, fear of falling). These considerations are probably even truer when pathological processes and their rehabilitation are involved. Again, individual longitudinal monitoring should become the rule.

Two final comments to conclude this editorial. First, to meet the challenge of gambling, various studies of the vestibular system have highlighted two constituent elements that could be instrumental at the neuronal level: vestibular habituation and vestibular adaptation. Second, the ubiquitous artificial intelligence does not seem to be able to answer the questions raised here: if there's one thing large language models (LLMs) do not do, it's bet and be anxious about it. Perhaps these two typically human behaviours explain why gaze and postural control became so effective in the permanent bipeds we have become, and why they ultimately failed with age.

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运动控制或赌博的艺术。
Zaback等人(2025)发表在本期《生理学杂志》上的这项研究涉及在使用随机前庭刺激探查前庭和运动反应的同时,反复将个体暴露于相同的姿势威胁中。这使得在相同威胁的背景下操纵情绪和自主状态成为可能。他们的研究结果表明,前庭和运动功能的威胁相关变化与威胁引起的情绪和自主神经变化密切相关,并不是对威胁的特定背景特征的不变反应。这项研究本身就很有趣,它提出了一些关于感觉运动转换的有趣问题。其中之一是关于感觉信息在中枢神经系统中的地位。脑干中的次级前庭神经元因接受初级前庭传入信号而得名。然而,正如我们后来意识到的那样,这些神经元也接受本体感觉输入,主要来自48个颈部肌肉的神经肌肉纺锤波,并通过副视系统接收视觉输入。这就解释了为什么当你坐在火车上,旁边的火车离开时,你会感到自己的火车在移动。因此,二级前庭神经元实际上发展出了一种内部的多模态表征,即头部和身体在空间中的运动。这种表现被用来稳定凝视和姿势,产生运动的意识,并允许自己的运动和外部产生的运动之间的分离。在这种情况下,我们还能讨论前庭神经元吗?我们是否应该问问自己,中枢神经系统是否保留了“前庭、视觉和本体感受”的信息,或者它是否将这些输入混合在一起,为频率调谐频道提供对世界的多模态表征?根据动物模型的电生理工作,我们自身运动的几种多模态表征可能在前庭核中共存,视觉和本体感觉前庭传入神经的权重不同。这还不是全部。所谓的“前庭”神经元也接受小脑和皮层的输入,它们的活动受到几种涉及警觉、情绪和自主神经变化的神经调节剂的调节。这在一定程度上解释了Zaback等人(2025)和Cullen(2023)获得的结果,这些结果表明,我们距离19世纪将姿势控制作为基本反射总和的结果的概念还有很长的路要走。我们面对的是由中枢神经系统在一系列感官输入、实际警惕性水平、情感和可能的社会背景的基础上精心制作的超快速表征。在大约200毫秒的时间里,这些神经元被用来形成对波动世界的连贯表征,这对于稳定我们的目光、控制我们的姿势、区分有人在推我们和我们发起的运动是必要的;简而言之,避免汽车灾难。在这种关键的情况下,我们可能会期望每个人对他们的目光和姿势的控制在相同的情况下相对一致。正如Zaback等人(2025)和其他人所表明的那样,情况并非如此。所有研究感觉-运动转换的神经生理学家,无论是动物模型还是人类,都知道他们工作的环境越生态,他们对行为的测量越精确,个体之间的差异就越大。换句话说,问题不仅仅是要理解,在受环境影响的多模态表征的基础上,我们如何重建一个使我们能够采取行动的现实。这也是关于理解不同的人在调节运动控制时如何得出不同的结论。换句话说,我们每个人都有自己的感知运动风格(回顾,见Vidal et al., 2021),在病理状态下更是如此。其结果是,一个群体的平均行为可能具有误导性。每个人在对目光和姿势的控制受到挑战时,对自己所面临的风险会有不同的看法,因此会采取不同的解决方案。这就是为什么个人纵向监测成为电机控制研究的关键因素。此外,成为永久的两足动物是一项冒险的游戏。不确定的预测和/或采用较差的肌肉协同作用导致在姿势扰动开始后约700毫秒,即500毫秒后摔倒在地。此外,跌倒是世界上因意外创伤而死亡的第二大原因,更不用说它们造成的各种伤害和老年人丧失独立性。Zaback等人(2025)的研究以及之前的其他人和先前的研究表明,对凝视和姿势的控制,远非一系列的反射,而是一个超快速下注的问题,而不是预测,以评估风险,以及旨在避免风险的最佳运动程序。 这些策略在个体之间具有共性(我们很少随机下注)。他们还为不同的人定义了不同的风格,不合理的赌博会导致神经症(恐高症、害怕摔倒)。当涉及到病理过程及其康复时,这些考虑可能更加真实。同样,个人纵向监测应该成为规则。这篇社论的最后两点评论。首先,为了应对赌博的挑战,前庭系统的各种研究都强调了两个可能在神经元水平上起作用的组成要素:前庭习惯化和前庭适应。其次,无处不在的人工智能似乎无法回答这里提出的问题:如果有一件事是大型语言模型(llm)做不到的,那就是打赌和焦虑。也许这两种典型的人类行为解释了为什么凝视和姿势控制在我们成为永久的两足动物时变得如此有效,以及为什么它们最终会随着年龄的增长而失效。
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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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