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      Postural Ataxia in Cerebellar Downbeat Nystagmus: Its Relation to Visual, Proprioceptive and Vestibular Signals and Cerebellar Atrophy

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          Abstract

          Background

          The cerebellum integrates proprioceptive, vestibular and visual signals for postural control. Cerebellar patients with downbeat nystagmus (DBN) complain of unsteadiness of stance and gait as well as blurred vision and oscillopsia.

          Objectives

          The aim of this study was to elucidate the differential role of visual input, gaze eccentricity, vestibular and proprioceptive input on the postural stability in a large cohort of cerebellar patients with DBN, in comparison to healthy age-matched control subjects.

          Methods

          Oculomotor (nystagmus, smooth pursuit eye movements) and postural (postural sway speed) parameters were recorded and related to each other and volumetric changes of the cerebellum (voxel-based morphometry, SPM).

          Results

          Twenty-seven patients showed larger postural instability in all experimental conditions. Postural sway increased with nystagmus in the eyes closed condition but not with the eyes open. Romberg’s ratio remained stable and was not different from healthy controls. Postural sway did not change with gaze position or graviceptive input. It increased with attenuated proprioceptive input and on tandem stance in both groups but Romberg’s ratio also did not differ. Cerebellar atrophy (vermal lobule VI, VIII) correlated with the severity of impaired smooth pursuit eye movements of DBN patients.

          Conclusions

          Postural ataxia of cerebellar patients with DBN cannot be explained by impaired visual feedback. Despite oscillopsia visual feedback control on cerebellar postural control seems to be preserved as postural sway was strongest on visual deprivation. The increase in postural ataxia is neither related to modulations of single components characterizing nystagmus nor to deprivation of single sensory (visual, proprioceptive) inputs usually stabilizing stance. Re-weighting of multisensory signals and/or inappropriate cerebellar motor commands might account for this postural ataxia.

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          Most cited references 36

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          Regularity of center-of-pressure trajectories depends on the amount of attention invested in postural control

          The influence of attention on the dynamical structure of postural sway was examined in 30 healthy young adults by manipulating the focus of attention. In line with the proposed direct relation between the amount of attention invested in postural control and regularity of center-of-pressure (COP) time series, we hypothesized that: (1) increasing cognitive involvement in postural control (i.e., creating an internal focus by increasing task difficulty through visual deprivation) increases COP regularity, and (2) withdrawing attention from postural control (i.e., creating an external focus by performing a cognitive dual task) decreases COP regularity. We quantified COP dynamics in terms of sample entropy (regularity), standard deviation (variability), sway-path length of the normalized posturogram (curviness), largest Lyapunov exponent (local stability), correlation dimension (dimensionality) and scaling exponent (scaling behavior). Consistent with hypothesis 1, standing with eyes closed significantly increased COP regularity. Furthermore, variability increased and local stability decreased, implying ineffective postural control. Conversely, and in line with hypothesis 2, performing a cognitive dual task while standing with eyes closed led to greater irregularity and smaller variability, suggesting an increase in the “efficiency, or “automaticity” of postural control”. In conclusion, these findings not only indicate that regularity of COP trajectories is positively related to the amount of attention invested in postural control, but also substantiate that in certain situations an increased internal focus may in fact be detrimental to postural control.
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            Visual stabilization of posture. Physiological stimulus characteristics and clinical aspects.

            Visual stabilization of posture is critically dependent on stimulus characteristics as well as on the performance of the visual system. The purpose of the present investigation was to obtain quantitative data in man by means of posturography of fore-aft and lateral body sway in relation to different visual stimulus characteristics. Visual acuity, when decreased logarithmically, causes a linearly increasing postural instability, twice as prominent for fore-aft than for lateral sway. Any measurable visual contribution for fore-aft sway ceases with an acuity lower than 0.03 and for lateral sway with an acuity lower than 0.01. The central area of the visual field as compared with the peripheral retina dominates postural control. The foveal region exhibits a powerful contribution, in particular for lateral sway. A partial but significant visual stabilization is preserved with a visual input rate between 1 to 4 Hz flicker frequency. As soon as continuous motion perception becomes involved with frequencies higher than 4 Hz, visual stabilization gradually improves with a saturation at frequencies higher than 16 Hz. Lateral body sway activity and eye-object distance are linearly related: body sway decreases with increasing distance corresponding to the linear decrease of net retinal displacement with increasing eye-object distance. Aspects of 'afferent' and 'efferent' visual motion perception, which involve fore-aft and lateral body sway differently, are evaluated. The clinical relevance is demonstrated in patients with oculomotor disturbances. The results are discussed with respect to the variety of related clinical disorders, which involve reduction in visual acuity, field defects, accommodation disturbances and ocular oscillations.
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              Vertical nystagmus: clinical facts and hypotheses.

              The pathophysiology of spontaneous upbeat (UBN) and downbeat (DBN) nystagmus is reviewed in the light of several instructive clinical findings and experimental data. UBN due to pontine lesions could result from damage to the ventral tegmental tract (VTT), originating in the superior vestibular nucleus (SVN), coursing through the ventral pons and transmitting excitatory upward vestibular signals to the third nerve nucleus. A VTT lesion probably leads to relative hypoactivity of the drive to the motoneurons of the elevator muscles with, consequently, an imbalance between the downward and upward systems, resulting in a downward slow phase. The results observed in internuclear ophthalmoplegia suggest that the medial longitudinal fasciculus (MLF) is involved in the transmission of both upward and downward vestibular signals. Since no clinical cases of DBN due to focal brainstem damage have been reported, it may be assumed that the transmission of downward vestibular signals depends only upon the MLF, whereas that of upward vestibular signals involves both the MLF and the VTT. The main focal lesions resulting in DBN affect the cerebellar flocculus and/or paraflocculus. Apparently, this structure tonically inhibits the SVN and its excitatory efferent tract (i.e. the VTT) but not the downward vestibular system. Therefore, a floccular lesion could result in a disinhibition of the SVN-VTT pathway with, consequently, relative hyperactivity of the drive to the motoneurons of the elevator muscles, resulting in an upward slow phase. UBN also results from lesions affecting the caudal medulla. An area in this region could form part of a feedback loop involved in upward gaze-holding, originating in a collateral branch of the VTT and comprising the caudal medulla, the flocculus and the SVN, successively. Therefore, it is suggested that the main types of spontaneous vertical nystagmus due to focal central lesions result from a primary dysfunction of the SVN-VTT pathway, which becomes hypoactive after pontine or caudal medullary lesions, thereby eliciting UBN, and hyperactive after floccular lesions, thereby eliciting DBN. Lastly, since gravity influences UBN and DBN and may facilitate the downward vestibular system and restrain the upward vestibular system, it is hypothesized that the excitatory SVN-VTT pathway, along with its specific floccular inhibition, has developed to counteract the gravity pull. This anatomical hyperdevelopment is apparently associated with a physiological upward velocity bias, since the gain of all upward slow eye movements is greater than that of downward slow eye movements in normal human subjects and in monkeys.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                5 January 2017
                2017
                : 12
                : 1
                Affiliations
                [1 ]Department of Neurology, University of Lübeck, Lubeck, Germany
                [2 ]Institute of Psychology II, University of Lübeck, Lubeck, Germany
                Tokai University, JAPAN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: CH AS JK MG.

                • Data curation: CH AS JK MG.

                • Formal analysis: CH AS JK MG.

                • Funding acquisition: CH.

                • Investigation: CH AS JK MG.

                • Methodology: CH AS JK MG.

                • Project administration: CH.

                • Resources: CH AS MG.

                • Software: CH AS MG.

                • Supervision: CH AS MG.

                • Validation: CH AS JK MG.

                • Visualization: CH AS JK MG.

                • Writing – original draft: CH AS.

                • Writing – review & editing: CH AS JK MG.

                Article
                PONE-D-16-34807
                10.1371/journal.pone.0168808
                5215796
                28056109
                © 2017 Helmchen et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 5, Tables: 0, Pages: 16
                Product
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Biology and Life Sciences
                Neuroscience
                Cognitive Science
                Cognitive Neuroscience
                Motor Reactions
                Postural Control
                Biology and Life Sciences
                Neuroscience
                Cognitive Neuroscience
                Motor Reactions
                Postural Control
                Biology and Life Sciences
                Anatomy
                Head
                Eyes
                Medicine and Health Sciences
                Anatomy
                Head
                Eyes
                Biology and Life Sciences
                Anatomy
                Ocular System
                Eyes
                Medicine and Health Sciences
                Anatomy
                Ocular System
                Eyes
                Medicine and Health Sciences
                Neurology
                Neurodegenerative Diseases
                Movement Disorders
                Ataxia
                Biology and Life Sciences
                Physiology
                Sensory Physiology
                Visual System
                Eye Movements
                Medicine and Health Sciences
                Physiology
                Sensory Physiology
                Visual System
                Eye Movements
                Biology and Life Sciences
                Neuroscience
                Sensory Systems
                Visual System
                Eye Movements
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Vision
                Social Sciences
                Psychology
                Sensory Perception
                Vision
                Physical Sciences
                Materials Science
                Materials by Structure
                Foam
                Medicine and Health Sciences
                Ophthalmology
                Visual Impairments
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Atrophy
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Atrophy
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