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      Amplification of vibration induced nystagmus in patients with peripheral vestibular loss by head tilt

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          Abstract

          Introduction

          In patients with unilateral loss of vestibular function (UVL) vibration of the skull leads to a response of the vestibulo-ocular reflex (VOR) called vibration-induced nystagmus (VIN), with slow phases usually directed toward the paretic ear. This response is thought to result from the difference between the neural discharge in semicircular canal afferents from the healthy and the affected labyrinth. The brain interprets this difference as a sustained imbalance in angular (rotational) vestibular tone, which in natural circumstances would only occur when the head was rotating at a constant acceleration.

          Methods

          To study this effect, we used a contemporary model of the neural network that combines sensory information about head rotation, translation, and tilt relative to gravity to estimate head orientation and motion. Based on the model we hypothesize that in patients with UVL, the brain may estimate not only a “virtual” rotation from the induced canal imbalance but also a subsequent “virtual” translation from the incorrect computation of the orientation of the head relative to gravity. If this is the case, the pattern of vibration-induced nystagmus will depend on the orientation of the head relative to gravity during the stimulation. This model predicts that this “virtual” translation will alter the baseline VIN elicited with the head upright; augmenting it when the affected ear is down and diminishing it when the affected ear is up.

          Results

          Confirming this hypothesis, we recorded VIN in 3 patients with UVL (due to vestibular neuritis) in upright, right ear-down, and left ear-down positions and each showed the expected pattern.

          Discussion

          From a practical, clinical view, our results and modeling suggest that positional VIN might reveal a hidden imbalance in angular vestibular tone in patients with UVL, when patients have equivocal signs of a vestibular imbalance, such as a minute amount of spontaneous or vibration-induced nystagmus with the head upright. This research provides insights into the underlying mechanisms of vestibular processing, the analysis of nystagmus in patients with UVL, and guides the design of a new bedside diagnostic test to assess vestibular function in patients with dizziness and imbalance.

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          Most cited references49

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          Humans use internal models to estimate gravity and linear acceleration.

          Because sensory systems often provide ambiguous information, neural processes must exist to resolve these ambiguities. It is likely that similar neural processes are used by different sensory systems. For example, many tasks require neural processing to distinguish linear acceleration from gravity, but Einstein's equivalence principle states that all linear accelerometers must measure both linear acceleration and gravity. Here we investigate whether the brain uses internal models, defined as neural systems that mimic physical principles, to help estimate linear acceleration and gravity. Internal models may be used in motor contro, sensorimotor integration and sensory processing, but direct experimental evidence for such models is limited. To determine how humans process ambiguous gravity and linear acceleration cues, subjects were tilted after being rotated at a constant velocity about an Earth-vertical axis. We show that the eye movements evoked by this post-rotational tilt include a response component that compensates for the estimated linear acceleration even when no actual linear acceleration occurs. These measured responses are consistent with our internal model predictions that the nervous system can develop a non-zero estimate of linear acceleration even when no true linear acceleration is present.
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            The functional significance of velocity storage and its dependence on gravity.

            Research in the vestibular field has revealed the existence of a central process, called 'velocity storage', that is activated by both visual and vestibular rotation cues and is modified by gravity, but whose functional relevance during natural motion has often been questioned. In this review, we explore spatial orientation in the context of a Bayesian model of vestibular information processing. In this framework, deficiencies/ambiguities in the peripheral vestibular sensors are compensated for by central processing to more accurately estimate rotation velocity, orientation relative to gravity, and inertial motion. First, an inverse model of semicircular canal dynamics is used to reconstruct rotation velocity by integrating canal signals over time. However, its low-frequency bandwidth is limited to avoid accumulation of noise in the integrator. A second internal model uses this reconstructed rotation velocity to compute an internal estimate of tilt and inertial acceleration. The bandwidth of this second internal model is also restricted at low frequencies to avoid noise accumulation and drift of the tilt/translation estimator over time. As a result, low-frequency translation can be erroneously misinterpreted as tilt. The time constants of these two integrators (internal models) can be conceptualized as two Bayesian priors of zero rotation velocity and zero linear acceleration, respectively. The model replicates empirical observations like 'velocity storage' and 'frequency segregation' and explains spatial orientation (e.g., 'somatogravic') illusions. Importantly, the functional significance of this network, including velocity storage, is found during short-lasting, natural head movements, rather than at low frequencies with which it has been traditionally studied.
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              Vestibular perception and action employ qualitatively different mechanisms. I. Frequency response of VOR and perceptual responses during Translation and Tilt.

              To investigate the neural mechanisms that humans use to process the ambiguous force measured by the otolith organs, we measured vestibuloocular reflexes (VORs) and perceptions of tilt and translation. One primary goal was to determine if the same, or different, mechanisms contribute to vestibular perception and action. We used motion paradigms that provided identical sinusoidal inter-aural otolith cues across a broad frequency range. We accomplished this by sinusoidally tilting (20 degrees, 0.005-0.7 Hz) subjects in roll about an earth-horizontal, head-centered, rotation axis ("Tilt") or sinusoidally accelerating (3.3 m/s2, 0.005-0.7 Hz) subjects along their inter-aural axis ("Translation"). While identical inter-aural otolith cues were provided by these motion paradigms, the canal cues were substantially different because roll rotations were present during Tilt but not during Translation. We found that perception was dependent on canal cues because the reported perceptions of both roll tilt and inter-aural translation were substantially different during Translation and Tilt. These findings match internal model predictions that rotational cues from the canals influence the neural processing of otolith cues. We also found horizontal translational VORs at frequencies >0.2 Hz during both Translation and Tilt. These responses were dependent on otolith cues and match simple filtering predictions that translational VORs include contributions via simple high-pass filtering of otolith cues. More generally, these findings demonstrate that internal models govern human vestibular "perception" across a broad range of frequencies and that simple high-pass filters contribute to human horizontal translational VORs ("action") at frequencies above approximately 0.2 Hz.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/2826829/overviewRole: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/50984/overviewRole: Role:
                URI : https://loop.frontiersin.org/people/17902/overviewRole: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/837577/overviewRole: Role:
                URI : https://loop.frontiersin.org/people/29430/overviewRole: Role: Role: Role:
                Journal
                Front Neurol
                Front Neurol
                Front. Neurol.
                Frontiers in Neurology
                Frontiers Media S.A.
                1664-2295
                16 October 2024
                2024
                : 15
                : 1420699
                Affiliations
                [1] 1The Technion Autonomous Systems Program, Technion – Israel Institute of Technology , Haifa, Israel
                [2] 2Department of Neurology, University of Illinois College of Medicine , Peoria, IL, United States
                [3] 3Department of Neurology, The Johns Hopkins University , Baltimore, MD, United States
                [4] 4Department of Otolaryngology-Head and Neck Surgery, The Johns Hopkins School of Medicine , Baltimore, MD, United States
                [5] 5Department of Ophthalmology, The Johns Hopkins School of Medicine , Baltimore, MD, United States
                [6] 6Department of Neuroscience, The Johns Hopkins School of Medicine , Baltimore, MD, United States
                [7] 7Department of Otorhinolaryngology and Instituto de Cerebro, Pontifical Catholic University of Rio Grande do Sul , Porto Alegre, Brazil
                [8] 8Herbert Wertheim School of Optometry and Vision Science, University of California, Berkeley , Berkeley, CA, United States
                Author notes

                Edited by: Andreas Zwergal, Ludwig Maximilian University of Munich, Germany

                Reviewed by: Jean Laurens, Max Planck Society, Germany

                Sun-Uk Lee, Korea University Medical Center, Republic of Korea

                *Correspondence: Jorge Otero-Millan, jom@ 123456berkeley.edu
                Article
                10.3389/fneur.2024.1420699
                11523294
                39479011
                65de151b-74c2-441e-a52b-f589de743e2e
                Copyright © 2024 Shemesh, Kattah, Zee, Zuma E Maia and Otero-Millan.

                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
                : 20 April 2024
                : 24 September 2024
                Page count
                Figures: 3, Tables: 2, Equations: 4, References: 49, Pages: 9, Words: 7070
                Funding
                The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by the David Robinson scholarship fund (Ari A Shemesh), the Betty and Paul Cinquegrana endowment (Ari A Shemesh, Jorge Otero-Millan and David S Zee), Leon Levy foundation (Jorge Otero-Millan) and NEI R00EY027846 (Jorge-Otero-Millan).
                Categories
                Neurology
                Original Research
                Custom metadata
                Neuro-Otology

                Neurology
                nystagmus,vestibular testing,vestibular neuritis,gravity estimation,three dimensions
                Neurology
                nystagmus, vestibular testing, vestibular neuritis, gravity estimation, three dimensions

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