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      Down regulation of vestibular balance stabilizing mechanisms to enable transition between motor states

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          Abstract

          The neural control of transition between posture and movement encompasses the regulation of reflex-stabilizing mechanisms to enable motion. Optimal feedback theory suggests that such transitions require the disengagement of one motor control policy before the implementation of another. To test this possibility, we investigated the continuity of the vestibular control of balance during transitions between quiet standing and locomotion and between two standing postures. Healthy subjects initiated and terminated locomotion or shifted the distribution of their weight between their feet, while exposed to electrical vestibular stimuli (EVS). The relationship between EVS and ground reaction forces was quantified using time-frequency analyses. Discontinuities corresponding to null coherence periods were observed preceding the onset of movement initiation and during the step preceding locomotion termination. These results show humans interrupt the vestibular balance stabilizing mechanisms to transition between motor states, suggesting a discrete change between motor control policies, as predicted by optimal feedback theory.

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          Crossing Abbey Road is something of a paradox in neuroscientific terms. As you stand waiting to cross, tiny movements of your body – such as those due to breathing – cause you to sway by small amounts. To prevent you from falling over, your brain makes active corrections to your posture. These posture-correcting mechanisms oppose movements such as sway and keep you standing upright. But what happens when you want to cross the road?

          To get you moving, your brain has two options. It could temporarily suppress the posture-correcting mechanisms. Or it could reconfigure them so that they work in a different way. The posture-correcting mechanisms rely upon sensory input from various sources. These include the vestibular system of the inner ear. The vestibular system tells the brain about the position and movement of the head in space and relative to gravity. Monitoring vestibular system activity as a person starts to move should thus reveal what is happening to the posture-correcting mechanisms.

          Tisserand et al. asked healthy volunteers to transition between standing still and walking, or to shift their weight from one foot to the other. At the same time, small non-painful electric currents were applied to the bones behind the volunteers' ears. These currents induced small changes in vestibular system activity. Sensors in the floor measured the forces the volunteers generated while standing or walking, thereby revealing how they adjusted their balance. The results showed that the brain suppresses its posture-correcting mechanisms before people start or stop moving.

          These findings have implications for robotics. They could make it easier to program robots to show smooth transitions into and out of movement. The findings are also relevant to movement disorders such as Parkinson's disease. One common symptom of this disorder is freezing of gait, in which patients suddenly feel as though their feet are glued to the ground. Understanding how the brain controls movement transitions may reveal how such symptoms arise.

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          Most cited references45

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          Optimal feedback control and the neural basis of volitional motor control.

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            Vestibular system: the many facets of a multimodal sense.

            Elegant sensory structures in the inner ear have evolved to measure head motion. These vestibular receptors consist of highly conserved semicircular canals and otolith organs. Unlike other senses, vestibular information in the central nervous system becomes immediately multisensory and multimodal. There is no overt, readily recognizable conscious sensation from these organs, yet vestibular signals contribute to a surprising range of brain functions, from the most automatic reflexes to spatial perception and motor coordination. Critical to these diverse, multimodal functions are multiple computationally intriguing levels of processing. For example, the need for multisensory integration necessitates vestibular representations in multiple reference frames. Proprioceptive-vestibular interactions, coupled with corollary discharge of a motor plan, allow the brain to distinguish actively generated from passive head movements. Finally, nonlinear interactions between otolith and canal signals allow the vestibular system to function as an inertial sensor and contribute critically to both navigation and spatial orientation.
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              Active control of lateral balance in human walking.

              We measured variability of foot placement during gait to test whether lateral balance must be actively controlled against dynamic instability. The hypothesis was developed using a simple dynamical model that can walk down a slight incline with a periodic gait resembling that of humans. This gait is entirely passive except that it requires active control for a single unstable mode, confined mainly to lateral motion. An especially efficient means of controlling this instability is to adjust lateral foot placement. We hypothesized that similar active feedback control is performed by humans, with fore-aft dynamics stabilized either passively or by very low-level control. The model predicts that uncertainty within the active feedback loop should result in variability in foot placement that is larger laterally than fore-aft. In addition, loss of sensory information such as by closing the eyes should result in larger increases in lateral variability. The control model also predicts a slight coupling between step width and length. We tested 15 young normal human subjects and found that lateral variability was 79% larger than fore-aft variability with eyes open, and a larger increase in lateral variability (53% vs. 21%) with eyes closed, consistent with the model's predictions. We also found that the coupling between lateral and fore-aft foot placements was consistent with a value of 0.13 predicted by the control model. Our results imply that humans may harness passive dynamic properties of the limbs in the sagittal plane, but must provide significant active control in order to stabilize lateral motion.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                10 July 2018
                2018
                : 7
                : e36123
                Affiliations
                [1 ]deptSchool of Kinesiology University of British Columbia VancouverCanada
                [2 ]deptDepartment of Kinesiology and Health Science Utah State University LoganUnited States
                [3 ]deptDepartment of Mechanical Engineering University of British Columbia VancouverCanada
                [4 ]deptInstitute for Computing, Information and Cognitive Systems University of British Columbia VancouverCanada
                [5 ]deptDepartment of Engineering Monash University ClaytonAustralia
                [6 ]deptInternational Collaboration on Repair Discoveries University of British Columbia VancouverCanada
                [7 ]deptDjavad Mowafaghian Centre for Brain Health University of British Columbia VancouverCanada
                University of Waterloo United States
                University of California, Berkeley United States
                University of Waterloo United States
                Author information
                https://orcid.org/0000-0002-6857-9886
                http://orcid.org/0000-0002-6781-0281
                Article
                36123
                10.7554/eLife.36123
                6056236
                29989550
                aed3cbab-49d7-4d42-9354-37a20fc9e363
                © 2018, Tisserand et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 22 February 2018
                : 30 June 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000038, Natural Sciences and Engineering Research Council of Canada;
                Award ID: 356026–13
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Human Biology and Medicine
                Neuroscience
                Custom metadata
                Down regulation of the gain from the vestibular sensory sources prior to the initiation of movement is a motor control solution to overcome the reflex-stabilizing mechanisms to enable motion from a postural orientation.

                Life sciences
                vestibular signal,motor control policy,transition,locomotion,posture,human
                Life sciences
                vestibular signal, motor control policy, transition, locomotion, posture, human

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