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      The vestibulospinal nucleus is a locus of balance development

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          Abstract

          Mature vertebrates maintain posture using vestibulospinal neurons that transform sensed instability into reflexive commands to spinal motor circuits. Postural stability improves across development. However, due to the complexity of terrestrial locomotion, vestibulospinal contributions to postural refinement in early life remain unexplored. Here we leveraged the relative simplicity of underwater locomotion to quantify the postural consequences of losing vestibulospinal neurons during development in larval zebrafish. By comparing posture at two timepoints, we discovered that later lesions of vestibulospinal neurons led to greater instability. Analysis of thousands of individual swim bouts revealed that lesions disrupted movement timing and corrective reflexes without impacting swim kinematics, particularly in older larvae. Using a generative model of swimming, we showed how these disruptions could account for the increased postural variability at both timepoints. Finally, late lesions disrupted the fin/trunk coordination observed in older larvae, linking vestibulospinal neurons to postural control schemes used to navigate in depth. Since later lesions were considerably more disruptive to postural stability, we conclude that vestibulospinal contributions to balance increase as larvae mature. Vestibulospinal neurons are highly conserved across vertebrates; we therefore propose that they are a substrate for developmental improvements to postural control.

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          Most cited references71

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          How animals move: an integrative view.

          Recent advances in integrative studies of locomotion have revealed several general principles. Energy storage and exchange mechanisms discovered in walking and running bipeds apply to multilegged locomotion and even to flying and swimming. Nonpropulsive lateral forces can be sizable, but they may benefit stability, maneuverability, or other criteria that become apparent in natural environments. Locomotor control systems combine rapid mechanical preflexes with multimodal sensory feedback and feedforward commands. Muscles have a surprising variety of functions in locomotion, serving as motors, brakes, springs, and struts. Integrative approaches reveal not only how each component within a locomotor system operates but how they function as a collective whole.
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            The how and why of arm swing during human walking.

            Humans walk bipedally, and thus, it is unclear why they swing their arms. In this paper, we will review the mechanisms and functions of arm swinging in human gait. First, we discuss the potential advantages of having swinging arms. Second, we go into the detail on the debate whether arm swing is arising actively or passively, where we will conclude that while a large part of arm swinging is mechanically passive, there is an active contribution of muscles (i.e. an activity that is not merely caused by stretch reflexes). Third, we describe the possible function of the active muscular contribution to arm swinging in normal gait, and discuss the possibility that a Central Pattern Generator (CPG) generates this activity. Fourth, we discuss examples from pathological cases, in which arm swinging is affected. Moreover, using the ideas presented, we suggest ways in which arm swing may be used as a therapeutic aid. We conclude that (1) arm swing should be seen as an integral part of human bipedal gait, arising mostly from passive movements, which are stabilized by active muscle control, which mostly originates from locomotor circuits in the central nervous system (2) arm swinging during normal bipedal gait most likely serves to reduce energy expenditure and (3) arm swinging may be of therapeutic value. Copyright © 2013 Elsevier B.V. All rights reserved.
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              Load-regulating mechanisms in gait and posture: comparative aspects.

              How is load sensed by receptors, and how is this sensory information used to guide locomotion? Many insights in this domain have evolved from comparative studies since it has been realized that basic principles concerning load sensing and regulation can be found in a wide variety of animals, both vertebrate and invertebrate. Feedback about load is not only derived from specific load receptors but also from other types of receptors that previously were thought to have other functions. In the central nervous system of many species, a convergence is found between specific and nonspecific load receptors. Furthermore, feedback from load receptors onto central circuits involved in the generation of rhythmic locomotor output is commonly found. During the stance phase, afferent activity from various load detectors can activate the extensor part in such circuits, thereby providing reinforcing force feedback. At the same time, the flexion is suppressed. The functional role of this arrangement is that activity in antigravity muscles is promoted while the onset of the next flexion is delayed as long as the limb is loaded. This type of reinforcing force feedback is present during gait but absent in the immoble resting animal.
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                Author and article information

                Journal
                bioRxiv
                BIORXIV
                bioRxiv
                Cold Spring Harbor Laboratory
                07 December 2023
                : 2023.12.06.570482
                Affiliations
                [1 ]Departments of Otolaryngology, Neuroscience & Physiology, and the Neuroscience Institute, New York University Grossman School of Medicine
                [2 ]National Institutes of Natural Sciences, Exploratory Research Center on Life and Living Systems (ExCELLS), National Institute for Basic Biology, Okazaki 444-8787, Aichi, Japan
                Author notes

                AUTHOR CONTRIBUTIONS

                Conceptualization: KRH and DS, Methodology: KRH and DS, Investigation: KRH and KH, Resources: YK and SH, Visualization: KRH, Writing: KRH, Editing: DS, Funding Acquisition: KRH and DS, Supervision: DS.

                Author information
                http://orcid.org/0000-0001-5408-9256
                http://orcid.org/0000-0002-2754-6834
                http://orcid.org/0000-0001-8381-8622
                http://orcid.org/0000-0001-6350-4992
                http://orcid.org/0000-0001-7969-9632
                Article
                10.1101/2023.12.06.570482
                10723429
                38105966
                aaac1087-c343-45f2-b8e5-d08884161ae5

                This work is licensed under a Creative Commons Attribution 4.0 International License, which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.

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