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      Treatment of Gravitational Pulling Sensation in Patients With Mal de Debarquement Syndrome (MdDS): A Model-Based Approach

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          Abstract

          Perception of the spatial vertical is important for maintaining and stabilizing vertical posture during body motion. The velocity storage pathway of vestibulo-ocular reflex (VOR), which integrates vestibular, optokinetic, and proprioception in the vestibular nuclei vestibular-only (VO) neurons, has spatio-temporal properties that are defined by eigenvalues and eigenvectors of its system matrix. The yaw, pitch and roll eigenvectors are normally aligned with the spatial vertical and corresponding head axes. Misalignment of the roll eigenvector with the head axes was hypothesized to be an important contributor to the oscillating vertigo during MdDS. Based on this, a treatment protocol was developed using simultaneous horizontal opto-kinetic stimulation and head roll (OKS-VOR). This protocol was not effective in alleviating the MdDS pulling sensations. A model was developed, which shows how maladaptation of the yaw eigenvector relative to the head yaw, either forward, back, or side down, could be responsible for the pulling sensation that subjects experience. The model predicted the sometimes counter-intuitive OKS directions that would be most effective in re-adapting the yaw eigenvector to alleviate the pulling sensation in MdDS. Model predictions were consistent with the treatment of 50 patients with a gravitational pulling sensation as the dominant feature. Overall, pulling symptoms in 72% of patients were immediately alleviated after the treatment and lasted for 3 years after the treatment in 58% of patients. The treatment also alleviated the pulling sensation in patients where pulling was not the dominant feature. Thus, the OKS method has a long-lasting effect comparable to that of OKS-VOR readaptation. The study elucidates how the spatio-temporal organization of velocity storage stabilizes upright posture and how maladaptation of the yaw eigenvector generates MdDS pulling sensations. Thus, this study introduces a new way to treat gravitational pull which could be used alone or in combination with previously proposed VOR readaptation techniques.

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          Most cited references72

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          A technique for the measturement of attittudes

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            Sensorimotor integration in human postural control.

            It is generally accepted that human bipedal upright stance is achieved by feedback mechanisms that generate an appropriate corrective torque based on body-sway motion detected primarily by visual, vestibular, and proprioceptive sensory systems. Because orientation information from the various senses is not always available (eyes closed) or accurate (compliant support surface), the postural control system must somehow adjust to maintain stance in a wide variety of environmental conditions. This is the sensorimotor integration problem that we investigated by evoking anterior-posterior (AP) body sway using pseudorandom rotation of the visual surround and/or support surface (amplitudes 0.5-8 degrees ) in both normal subjects and subjects with severe bilateral vestibular loss (VL). AP rotation of body center-of-mass (COM) was measured in response to six conditions offering different combinations of available sensory information. Stimulus-response data were analyzed using spectral analysis to compute transfer functions and coherence functions over a frequency range from 0.017 to 2.23 Hz. Stimulus-response data were quite linear for any given condition and amplitude. However, overall behavior in normal subjects was nonlinear because gain decreased and phase functions sometimes changed with increasing stimulus amplitude. "Sensory channel reweighting" could account for this nonlinear behavior with subjects showing increasing reliance on vestibular cues as stimulus amplitudes increased. VL subjects could not perform this reweighting, and their stimulus-response behavior remained quite linear. Transfer function curve fits based on a simple feedback control model provided estimates of postural stiffness, damping, and feedback time delay. There were only small changes in these parameters with increasing visual stimulus amplitude. However, stiffness increased as much as 60% with increasing support surface amplitude. To maintain postural stability and avoid resonant behavior, an increase in stiffness should be accompanied by a corresponding increase in damping. Increased damping was achieved primarily by decreasing the apparent time delay of feedback control rather than by changing the damping coefficient (i.e., corrective torque related to body-sway velocity). In normal subjects, stiffness and damping were highly correlated with body mass and moment of inertia, with stiffness always about 1/3 larger than necessary to resist the destabilizing torque due to gravity. The stiffness parameter in some VL subjects was larger compared with normal subjects, suggesting that they may use increased stiffness to help compensate for their loss. Overall results show that the simple act of standing quietly depends on a remarkably complex sensorimotor control system.
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              A new interpretation of spontaneous sway measures based on a simple model of human postural control.

              This study shows that center-of-pressure (COP) traces that closely resemble physiologically measured COP functions can be produced by an appropriate selection of model parameters in a simple feedback model of the human postural control system. Variations in the values of stiffness, damping, time delay, and noise level determine the values of 15 sway measures commonly used to characterize spontaneous sway. Results from model simulations indicate that there is a high degree of correlation among these sway measures, and the measures cluster into three different groups. Only two principal components accounted for about 92% of the variation among the different sway measures analyzed. This model can be used to formulate hypotheses regarding the cause of postural control deficits reported in the literature. This is accomplished using a multidimensional optimization procedure to estimate model parameters from a diverse set of spontaneous sway measures. These model parameters describe physiologically meaningful features of the postural control system as opposed to conventional sway measures that provide only a parametric description of sway. To show the application of this method, we applied it to published data of spontaneous sway from elderly subjects and contrasted it to the data of young healthy subjects. We found that modest increases in stiffness and damping and a fairly large increase in noise level with aging could account for the variety of sway measures reported in the literature for elderly subjects.
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                Author and article information

                Contributors
                Journal
                Front Integr Neurosci
                Front Integr Neurosci
                Front. Integr. Neurosci.
                Frontiers in Integrative Neuroscience
                Frontiers Media S.A.
                1662-5145
                23 May 2022
                2022
                : 16
                : 801817
                Affiliations
                [1] 1Department of Neurology, Icahn School of Medicine at Mount Sinai , New York, NY, United States
                [2] 2Institute for Neural and Intelligent Systems, Department of Computer and Information Science, Brooklyn College of the City University of New York , Brooklyn, NY, United States
                [3] 3Department of Computer Science, Graduate Center of CUNY , New York, NY, United States
                [4] 4Ph.D Program in Psychology and Neuroscience, Graduate Center of CUNY , New York, NY, United States
                [5] 5Department Neurology and Otolaryngology, NYU Robert I. Grossman School of Medicine , New York, NY, United States
                Author notes

                Edited by: Laurence Roy Harris, York University, Canada

                Reviewed by: Floris L. Wuyts, University of Antwerp, Belgium; Hong-bing Xiang, Huazhong University of Science and Technology, China

                *Correspondence: Theodore Raphan, raphan@ 123456nsi.brooklyn.cuny.edu
                Article
                10.3389/fnint.2022.801817
                9168314
                35676926
                1fd49380-4a33-405b-a6e9-d761c5647dc0
                Copyright © 2022 Yakushin, Raphan and Cho.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 25 October 2021
                : 06 April 2022
                Page count
                Figures: 9, Tables: 2, Equations: 0, References: 72, Pages: 17, Words: 13149
                Categories
                Neuroscience
                Original Research

                Neurosciences
                mdds,velocity storage,orientation-vector,gravitational pull,rocking,swaying,bobbing,vestibular only (vo) neurons

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