scholarly journals Angular vestibuloocular reflex responses in Otop1 mice. II. Otolith sensor input improves compensation after unilateral labyrinthectomy

2019 ◽  
Vol 121 (6) ◽  
pp. 2300-2307 ◽  
Author(s):  
Serajul I. Khan ◽  
Charles C. Della Santina ◽  
Americo A. Migliaccio
Keyword(s):  
Semicircular Canals ◽  
Vertical Axis ◽  
Vestibuloocular Reflex ◽  
Peripheral Injury ◽  
Axis Parallel ◽  
Vor Adaptation ◽  
Unilateral Labyrinthectomy ◽  
Context Specific ◽  
Gain Loss

The role of the otoliths in mammals in the normal angular vestibuloocular reflex (VOR) was characterized in an accompanying study based on the Otopetrin1 (Otop1) mouse, which lacks functioning otoliths because of failure to develop otoconia but seems to have otherwise normal peripheral anatomy and neural circuitry. That study showed that otoliths do not contribute to the normal horizontal (rotation about Earth-vertical axis parallel to dorso-ventral axis) and vertical (rotation about Earth-vertical axis parallel to interaural axis) angular VOR but do affect gravity context-specific VOR adaptation. By using these animals, we sought to determine whether the otoliths play a role in the angular VOR after unilateral labyrinthectomy when the total canal signal is reduced. In five Otop1 mice and five control littermates we measured horizontal and vertical left-ear-down and right-ear-down sinusoidal VOR (0.2–10 Hz, 20–100°/s) during the early (3–5 days) and plateau (28–32 days) phases of compensation after unilateral labyrinthectomy and compared these measurements with baseline preoperative responses from the accompanying study. From similar baselines, acute gain loss was ~25% less in control mice, and chronic gain recovery was ~40% more in control mice. The acute data suggest that the otoliths contribute to the angular VOR when there is a loss of canal function. The chronic data suggest that a unilateral otolith signal can significantly improve angular VOR compensation. These data have implications for vestibular rehabilitation of patients with both canal and otolith loss and the development of vestibular implants, which currently only mimic the canals on one side.NEW & NOTEWORTHY This is the first study examining the role of the otoliths (defined here as the utricle and saccule) on the acute and chronic angular vestibuloocular reflex (VOR) after unilateral labyrinthectomy in an animal model in which the otoliths are reliably inactivated and the semicircular canals preserved. This study shows that the otolith signal is used to augment the acute angular VOR and help boost VOR compensation after peripheral injury.

scholarly journals Angular vestibuloocular reflex responses in Otop1 mice. I. Otolith sensor input is essential for gravity context-specific adaptation

2019 ◽  
Vol 121 (6) ◽  
pp. 2291-2299 ◽  
Author(s):  
Serajul I. Khan ◽  
Charles C. Della Santina ◽  
Americo A. Migliaccio
Keyword(s):  
Semicircular Canals ◽  
Vertical Axis ◽  
Neural Circuitry ◽  
Vestibuloocular Reflex ◽  
Training Context ◽  
Specific Adaptation ◽  
Axis Parallel ◽  
Vor Adaptation ◽  
Context Specific

The role of the otoliths in mammals in the angular vestibuloocular reflex (VOR) has been difficult to determine because there is no surgical technique that can reliably ablate them without damaging the semicircular canals. The Otopetrin1 (Otop1) mouse lacks functioning otoliths because of failure to develop otoconia but seems to have otherwise normal peripheral anatomy and neural circuitry. By using these animals we sought to determine the role of the otoliths in angular VOR baseline function and adaptation. In six Otop1 mice and six control littermates we measured baseline ocular countertilt about the three primary axes in head coordinates; baseline horizontal (rotation about an Earth-vertical axis parallel to the dorsal-ventral axis) and vertical (rotation about an Earth-vertical axis parallel to the interaural axis) sinusoidal (0.2–10 Hz, 20–100°/s) VOR gain (= eye/head velocity); and the horizontal and vertical VOR after gain-increase (1.5×) and gain-decrease (0.5×) adaptation training. Countertilt responses were significantly reduced in Otop1 mice. Baseline horizontal and vertical VOR gains were similar between mouse types, and so was horizontal VOR adaptation. For control mice, vertical VOR adaptation was evident when the testing context, left ear down (LED) or right ear down (RED), was the same as the training context (LED or RED). For Otop1 mice, VOR adaptation was evident regardless of context. Our results suggest that the otolith translational signal does not contribute to the baseline angular VOR, probably because the mouse VOR is highly compensatory, and does not alter the magnitude of adaptation. However, we show that the otoliths are important for gravity context-specific angular VOR adaptation. NEW & NOTEWORTHY This is the first study examining the role of the otoliths (defined here as the utricle and saccule) in adaptation of the angular vestibuloocular reflex (VOR) in an animal model in which the otoliths are reliably inactivated and the semicircular canals preserved. We show that they do not contribute to adaptation of the normal angular VOR. However, the otoliths provide the main cue for gravity context-specific VOR adaptation.

Sensorimotor aspects of high-speed artificial gravity: II. The effect of head position on illusory self motion

2003 ◽  
Vol 12 (5-6) ◽  
pp. 283-289
Author(s):  
Fred W. Mast ◽  
Nathaniel J. Newby ◽  
Laurence R. Young
Keyword(s):  
Healthy Subjects ◽  
Horizontal Plane ◽  
High Speed ◽  
Semicircular Canals ◽  
Vertical Axis ◽  
Head Position ◽  
Artificial Gravity ◽  
Axis Of Rotation ◽  
Self Motion

The effects of cross-coupled stimuli on the semicircular canals are shown to be influenced by the position of the subject's head with respect to gravity and the axis of rotation, but not by the subject's head position relative to the trunk. Seventeen healthy subjects made head yaw movements out of the horizontal plane while lying on a horizontal platform (MIT short radius centrifuge) rotating at 23 rpm about an earth-vertical axis. The subjects reported the magnitude and duration of the illusory pitch or roll sensations elicited by the cross-coupled rotational stimuli acting on the semicircular canals. The results suggest an influence of head position relative to gravity. The magnitude estimation is higher and the sensation decays more slowly when the head's final position is toward nose-up (gravity in the subject's head x-z-plane) compared to when the head is turned toward the side (gravity in the subject's head y-z-plane). The results are discussed with respect to artificial gravity in space and the possible role of pre-adaptation to cross-coupled angular accelerations on earth.

scholarly journals Efferent-Mediated Responses in Vestibular Nerve Afferents of the Alert Macaque

2009 ◽  
Vol 101 (2) ◽  
pp. 988-1001 ◽  
Author(s):  
Soroush G. Sadeghi ◽  
Jay M. Goldberg ◽  
Lloyd B. Minor ◽  
Kathleen E. Cullen
Keyword(s):  
Rotational Velocity ◽  
Semicircular Canals ◽  
Macaque Monkey ◽  
Nerve Fibers ◽  
Vestibular Nerve ◽  
Vestibular Afferents ◽  
Motion Responses ◽  
Unilateral Labyrinthectomy ◽  
Vestibular Nerve Afferents

The peripheral vestibular organs have long been known to receive a bilateral efferent innervation from the brain stem. However, the functional role of the efferent vestibular system has remained elusive. In this study, we investigated efferent-mediated responses in vestibular afferents of alert behaving primates (macaque monkey). We found that efferent-mediated rotational responses could be obtained from vestibular nerve fibers innervating the semicircular canals after conventional afferent responses were nulled by placing the corresponding canal plane orthogonal to the plane of motion. Responses were type III, i.e., excitatory for rotational velocity trapezoids (peak velocity, 320°/s) in both directions of rotation, consistent with those previously reported in the decerebrate chinchilla. Responses consisted of both fast and slow components and were larger in irregular (∼10 spikes/s) than in regular afferents (∼2 spikes/s). Following unilateral labyrinthectomy (UL) on the side opposite the recording site, similar responses were obtained. To confirm the vestibular source of the efferent-mediated responses, the ipsilateral horizontal and posterior canals were plugged following the UL. Responses to high-velocity rotations were drastically reduced when the superior canal (SC), the only intact canal, was in its null position, compared with when the SC was pitched 50° upward from the null position. Our findings show that vestibular afferents in alert primates show efferent-mediated responses that are related to the discharge regularity of the afferent, are of vestibular origin, and can be the result of both afferent excitation and inhibition.

Role of semicircular canals in positional alcohol nystagmus

1965 ◽  
Vol 208 (6) ◽  
pp. 1065-1070 ◽  
Author(s):  
K. E. Money ◽  
W. H. Johnson ◽  
B. M. A. Corlett
Keyword(s):  
Semicircular Canal ◽  
Semicircular Canals ◽  
The Other ◽  
Positional Nystagmus ◽  
Horizontal Semicircular Canal ◽  
Horizontal Canal ◽  
Unilateral Labyrinthectomy

Following unilateral labyrinthectomy or inactivation of one horizontal semicircular canal in cats, a horizontal positional nystagmus was observed when the cat, after ingesting alcohol, was held with the head up or with the head down. This nystagmus was toward the operated ear in the head-up position and away from the operated ear in the head-down position. It disappeared following inactivation of the horizontal canal of the other ear. In cats with both horizontal canals discretely inactivated, there was no horizontal alcohol nystagmus in any position, but the vertical and rotary components of positional alcohol nystagmus were still present. It was concluded that positional alcohol nystagmus is initiated by the action of gravity on receptors of the semicircular canals. No conclusion could be drawn concerning the site or mechanism of the action of alcohol.

Inactivation of Semicircular Canals Causes Adaptive Increases in Otolith-Driven Tilt Responses

2002 ◽  
Vol 87 (3) ◽  
pp. 1635-1640 ◽  
Author(s):  
Dora E. Angelaki ◽  
Shawn D. Newlands ◽  
J. David Dickman
Keyword(s):  
Eye Movements ◽  
Semicircular Canal ◽  
Translational Motion ◽  
Semicircular Canals ◽  
Vertical Axis ◽  
Lateral Motion ◽  
Functional Interaction ◽  
Gaze Stabilization ◽  
Theoretical Evidence ◽  
Ocular System

Growing experimental and theoretical evidence suggests a functional synergy in the processing of otolith and semicircular canal signals for the generation of the vestibulo-ocular reflexes (VORs). In this study we have further tested this functional interaction by quantifying the adaptive changes in the otolith-ocular system during both rotational and translational movements after surgical inactivation of the semicircular canals. For 0.1–0.5 Hz (stimuli for which there is no recovery of responses from the plugged canals), pitch and roll VOR gains recovered during earth-horizontal (but not earth-vertical) axis rotations. Corresponding changes were also observed in eye movements elicited by translational motion (0.1–5 Hz). Specifically, torsional eye movements increased during lateral motion, whereas vertical eye movements increased during fore-aft motion. The findings indicate that otolith signals can be adapted according to a compromised strategy that leads to improved gaze stabilization during motion. Because canal-plugged animals permanently lose the ability to discriminate gravitoinertial accelerations, adapted animals can use the presence of gravity through otolith-driven tilt responses to assist gaze stabilization during earth-horizontal axis rotations.

Possible cues driving context-specific adaptation of optocollic reflex in pigeons (Columba livia)

2012 ◽  
Vol 107 (2) ◽  
pp. 704-717 ◽  
Author(s):  
Henri Gioanni ◽  
Pierre-Paul Vidal
Keyword(s):  
Columba Livia ◽  
Motor Command ◽  
Slow Phase ◽  
Gaze Stabilization ◽  
Specific Adaptation ◽  
Body Vibration ◽  
Fast Phase ◽  
Context Specific ◽  
Context Cues

Context-specific adaptation (Shelhamer M, Clendaniel R. Neurosci Lett 332: 200–204, 2002) explains that reflexive responses can be maintained with different “calibrations” for different situations (contexts). Which context cues are crucial and how they combine to evoke context-specific adaptation is not fully understood. Gaze stabilization in birds is a nice model with which to tackle that question. Previous data showed that when pigeons ( Columba livia) were hung in a harness and subjected to a frontal airstream provoking a flying posture (“flying condition”), the working range of the optokinetic head response [optocollic reflex (OCR)] extended toward higher velocities compared with the “resting condition.” The present study was aimed at identifying which context cues are instrumental in recalibrating the OCR. We investigated that question by using vibrating stimuli delivered during the OCR provoked by rotating the visual surroundings at different velocities. The OCR gain increase and the boost of the fast phase velocity observed during the “flying condition” were mimicked by body vibration. On the other hand, the newly emerged relationship between the fast-phase and slow-phase velocities in the “flying condition” was mimicked by head vibration. Spinal cord lesion at the lumbosacral level decreased the effects of body vibration, whereas lesions of the lumbosacral apparatus had no effect. Our data suggest a major role of muscular proprioception in the context-specific adaptation of the stabilizing behavior, while the vestibular system could contribute to the context-specific adaptation of the orienting behavior. Participation of an efferent copy of the motor command driving the flight cannot be excluded.

Horizontal Vestibuloocular Reflex Evoked by High-Acceleration Rotations in the Squirrel Monkey. II. Responses After Canal Plugging

1999 ◽  
Vol 82 (3) ◽  
pp. 1271-1285 ◽  
Author(s):  
David M. Lasker ◽  
Douglas D. Backous ◽  
Anna Lysakowski ◽  
Griffin L. Davis ◽  
Lloyd B. Minor
Keyword(s):  
High Frequency ◽  
Peak Velocity ◽  
Vestibular Function ◽  
Semicircular Canals ◽  
Vestibuloocular Reflex ◽  
Half Cycle ◽  
High Acceleration ◽  
Linear And Nonlinear ◽  
Residual Response ◽  
Sinusoidal Rotations

The horizontal angular vestibuloocular reflex (VOR) evoked by high-frequency, high-acceleration rotations was studied in four squirrel monkeys after unilateral plugging of the three semicircular canals. During the period (1–4 days) that animals were kept in darkness after plugging, the gain during steps of acceleration (3,000°/s2, peak velocity = 150°/s) was 0.61 ± 0.14 (mean ± SD) for contralesional rotations and 0.33 ± 0.03 for ipsilesional rotations. Within 18–24 h after animals were returned to light, the VOR gain for contralesional rotations increased to 0.88 ± 0.05, whereas there was only a slight increase in the gain for ipsilesional rotations to 0.37 ± 0.07. A symmetrical increase in the gain measured at the plateau of head velocity was noted after animals were returned to light. The latency of the VOR was 8.2 ± 0.4 ms for ipsilesional and 7.1 ± 0.3 ms for contralesional rotations. The VOR evoked by sinusoidal rotations of 0.5–15 Hz, ±20°/s had no significant half-cycle asymmetries. The recovery of gain for these responses after plugging was greater at lower than at higher frequencies. Responses to rotations at higher velocities for frequencies ≥4 Hz showed an increase in contralesional half-cycle gain, whereas ipsilesional half-cycle gain was unchanged. A residual response that appeared to be canal and not otolith mediated was noted after plugging of all six semicircular canals. This response increased with frequency to reach a gain of 0.23 ± 0.03 at 15 Hz, resembling that predicted based on a reduction of the dominant time constant of the canal to 32 ms after plugging. A model incorporating linear and nonlinear pathways was used to simulate the data. The coefficients of this model were determined from data in animals with intact vestibular function. Selective increases in the gain for the linear and nonlinear pathways predicted the changes in recovery observed after canal plugging. An increase in gain of the linear pathway accounted for the recovery in VOR gain for both responses at the velocity plateau of the steps of acceleration and for the sinusoidal rotations at lower peak velocities. The increase in gain for contralesional responses to steps of acceleration and sinusoidal rotations at higher frequencies and velocities was due to an increase in the gain of the nonlinear pathway. This pathway was driven into inhibitory cutoff at low velocities and therefore made no contribution for rotations toward the ipsilesional side.

scholarly journals Contribution of intravestibular sensory conflict to motion sickness and dizziness in migraine disorders

2016 ◽  
Vol 116 (4) ◽  
pp. 1586-1591 ◽  
Author(s):  
Joanne Wang ◽  
Richard F. Lewis
Keyword(s):  
Motion Sickness ◽  
Semicircular Canals ◽  
Inverse Correlation ◽  
Normal Subjects ◽  
Otolith Organs ◽  
Rotational Axis ◽  
Vestibuloocular Reflex ◽  
Sensory Conflict ◽  
Velocity Signal ◽  
Episodic Vertigo

Migraine is associated with enhanced motion sickness susceptibility and can cause episodic vertigo [vestibular migraine (VM)], but the mechanisms relating migraine to these vestibular symptoms remain uncertain. We tested the hypothesis that the central integration of rotational cues (from the semicircular canals) and gravitational cues (from the otolith organs) is abnormal in migraine patients. A postrotational tilt paradigm generated a conflict between canal cues (which indicate the head is rotating) and otolith cues (which indicate the head is tilted and stationary), and eye movements were measured to quantify two behaviors that are thought to minimize this conflict: suppression and reorientation of the central angular velocity signal, evidenced by attenuation (“dumping”) of the vestibuloocular reflex and shifting of the rotational axis of the vestibuloocular reflex toward the earth vertical. We found that normal and migraine subjects, but not VM patients, displayed an inverse correlation between the extent of dumping and the size of the axis shift such that the net “conflict resolution” mediated through these two mechanisms approached an optimal value and that the residual sensory conflict in VM patients (but not migraine or normal subjects) correlated with motion sickness susceptibility. Our findings suggest that the brain normally controls the dynamic and spatial characteristics of central vestibular signals to minimize intravestibular sensory conflict and that this process is disrupted in VM, which may be responsible for the enhance motion intolerance and episodic vertigo that characterize this disorder.

Context-Specific Gain Switching in the Human Vestibuloocular Reflex

1992 ◽  
Vol 656 (1 Sensing and C) ◽  
pp. 889-891 ◽  
Author(s):  
MARK SHELHAMER ◽  
DAVID A. ROBINSON ◽  
HENDRA S. TAN
Keyword(s):  
Vestibuloocular Reflex ◽  
Gain Switching ◽  
Context Specific
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