Biasing the semicircular canal cupula in excitatory direction decreases the gain of the vestibuloocular reflex for head impulses

It is well established that the head and eye velocity axes do not always align during compensatory vestibular slow phases. It has been shown that the eye velocity axis systematically tilts away from the head velocity axis in a manner that is dependent on eye-in-head position. The mechanisms responsible for producing these axis tilts are unclear. In this model-based study, we aimed to determine whether muscle pulleys could be involved in bringing about these phenomena. The model presented incorporates semicircular canals, central vestibular pathways, and an ocular motor plant with pulleys. The pulleys were modeled so that they brought about a rotation of the torque axes of the extraocular muscles that was a fraction of the angle of eye deviation from primary position. The degree to which the pulleys rotated the torque axes was altered by means of a pulley coefficient. Model input was head velocity and initial eye position data from passive and active yaw head impulses with fixation at 0°, 20° up and 20° down, obtained from a previous experiment. The optimal pulley coefficient required to fit the data was determined by calculating the mean square error between data and model predictions of torsional eye velocity. For active head impulses, the optimal pulley coefficient varied considerably between subjects. The median optimal pulley coefficient was found to be 0.5, the pulley coefficient required for producing saccades that perfectly obey Listing's law when using a two-dimensional saccadic pulse signal. The model predicted the direction of the axis tilts observed in response to passive head impulses from 50 ms after onset. During passive head impulses, the median optimal pulley coefficient was found to be 0.21, when roll gain was fixed at 0.7. The model did not accurately predict the alignment of the eye and head velocity axes that was observed early in the response to passive head impulses. We found that this alignment could be well predicted if the roll gain of the angular vestibuloocular reflex was modified during the initial period of the response, while pulley coefficient was maintained at 0.5. Hence a roll gain modification allows stabilization of the retinal image without requiring a change in the pulley effect. Our results therefore indicate that the eye position–dependent velocity axis tilts could arise due to the effects of the pulleys and that a roll gain modification in the central vestibular structures may be responsible for countering the pulley effect.

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Unilateral Head Impulses Training in Uncompensated Vestibular Hypofunction

Case Reports in Otolaryngology ◽

10.1155/2017/2145173 ◽

2017 ◽

Vol 2017 ◽

pp. 1-6 ◽

Cited By ~ 3

Author(s):

Ana Carolina Binetti ◽

Andrea Ximena Varela ◽

Dana Lucila Lucarelli ◽

Daniel Héctor Verdecchia

Keyword(s):

Young Woman ◽

Head Rotation ◽

Rehabilitation Program ◽

Vestibuloocular Reflex ◽

Blurred Vision ◽

Head Impulse ◽

Vestibular Hypofunction ◽

Affected Side ◽

Head Impulses

The aim of this paper is to report a case of a young woman with unilateral vestibular chronic failure with a poorly compensated vestibuloocular reflex during rapid head rotation. Additionally, she developed migraine symptoms during the treatment with associated chronic dizzy sensations and blurred vision. Her report of blurred vision only improved after she completed a rehabilitation program using fast head impulse rotations towards the affected side for 5 consecutive days. We discuss why we elected this form of treatment and how this method may be useful for different patients.

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Contribution of Vestibular Commissural Pathways to Spatial Orientation of the Angular Vestibuloocular Reflex

Journal of Neurophysiology ◽

10.1152/jn.1997.78.2.1193 ◽

1997 ◽

Vol 78 (2) ◽

pp. 1193-1197 ◽

Cited By ~ 39

Author(s):

Susan Wearne ◽

Theodore Raphan ◽

Bernard Cohen

Keyword(s):

Spatial Orientation ◽

Semicircular Canal ◽

Vertical Axis ◽

Vestibular Stimulation ◽

Velocity Storage ◽

Vestibuloocular Reflex ◽

Time Constants ◽

Commissural Pathways ◽

Before And After ◽

Axis Rotation

Wearne, Susan, Theodore Raphan, and Bernard Cohen. Contribution of vestibular commissural pathways to spatial orientation of the angular vestibuloocular reflex. J. Neurophysiol. 78: 1193–1197, 1997. During nystagmus induced by the angular vestibuloocular reflex (aVOR), the axis of eye velocity tends to align with the direction of gravitoinertial acceleration (GIA), a process we term “spatial orientation of the aVOR.” We studied spatial orientation of the aVOR in rhesus and cynomolgus monkeys before and after midline section of the rostral medulla abolished all oculomotor functions related to velocity storage, leaving the direct optokinetic and vestibular pathways intact. Optokinetic afternystagmus and the bias component of off-vertical-axis rotation were lost, and the aVOR time constant was reduced to a value commensurate with the time constants of primary semicircular canal afferents. Spatial orientation of the aVOR, induced either during optokinetic or vestibular stimulation, was also lost. Vertical and roll aVOR time constants could no longer be lengthened in side-down or supine/prone positions, and static and dynamic tilts of the GIA no longer produced cross-coupling from the yaw to pitch and yaw to roll axes. Consequently, the induced nystagmus remained entirely in head coordinates after the lesion, regardless of the direction of the resultant GIA vector. Gains of the aVOR and of optokinetic nystagmus to steps of velocity were unaffected or slightly increased. These results are consistent with a model in which the direct aVOR pathways are organized in semicircular canal coordinates and spatial orientation is restricted to the indirect (velocity storage) pathways.

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Cerebellar Disease Alters the Axis of the High-Acceleration Vestibuloocular Reflex

Journal of Neurophysiology ◽

10.1152/jn.00375.2005 ◽

2005 ◽

Vol 94 (5) ◽

pp. 3417-3429 ◽

Cited By ~ 35

Author(s):

Mark F. Walker ◽

David S. Zee

Keyword(s):

Head Rotation ◽

Normal Subjects ◽

Vestibuloocular Reflex ◽

Cerebellar Disease ◽

Characteristic Finding ◽

High Acceleration ◽

The Difference ◽

Head Impulses ◽

Cross Axis ◽

Eye Velocity

L. W. Schultheis and D. A. Robinson showed that the axis of the rotational vestibuloocular reflex (RVOR) cannot be altered by visual-vestibular mismatch (“cross-axis adaptation”) when the vestibulocerebellum is lesioned. This suggests that the cerebellum may calibrate the axis of eye velocity of the RVOR under natural conditions. Thus we asked whether patients with cerebellar disease have alterations in the RVOR axis and, if so, what might be the mechanism. We used three-axis scleral coils to record head and eye movements during yaw, pitch, and roll head impulses in 18 patients with cerebellar disease and in a comparison group of eight subjects without neurologic disease. We found distinct shifts of the eye-velocity axis in patients. The characteristic finding was a disconjugate upward eye velocity during yaw. Measured at 70 ms after the onset of head rotation, the median upward gaze velocity was 15% of yaw head velocity for patients and <1% for normal subjects ( P < 0.001). Upward eye velocity was greater in the contralateral (abducting) eye during yaw and in the ipsilateral eye during roll. Patients had a higher gain (eye speed/head speed) for downward than for upward pitch (median ratio of downward to upward gain: 1.3). In patients, upward gaze velocities during both yaw and roll correlated with the difference in anterior (AC) and posterior canal excitations, scaled by the respective pitch gains. Our findings support the hypothesis that upward eye velocity during yaw results from AC excitation, which must normally be suppressed by the intact cerebellum.

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Diagnostic Bedside Vestibuloocular Reflex Evaluation in the Setting of a False Negative Fistula Test in Cholesteatoma of the Middle Ear

Case Reports in Otolaryngology ◽

10.1155/2017/2919463 ◽

2017 ◽

Vol 2017 ◽

pp. 1-5

Author(s):

Ricardo D’Albora ◽

Ligia Silveira ◽

Sergio Carmona ◽

Nicolas Perez-Fernandez

Keyword(s):

Middle Ear ◽

Semicircular Canal ◽

False Negative ◽

Case Series ◽

Mass Effect ◽

Head Impulse Test ◽

Vestibuloocular Reflex ◽

Suppurative Otitis Media ◽

Head Impulse ◽

Rule Out

Background. False negative fistula testing in patients with chronic suppurative otitis media is a dilemma when proceeding to surgery. It is imperative to rule out a dead labyrinth or a mass effect secondary to the cholesteatoma in an otherwise normally functioning inner ear. We present a case series of three patients in whom a bedside vestibuloocular reflex (VOR) evaluation using a head impulse test was used successfully for further evaluation prior to surgery. Results. In all three cases with a false negative fistula test we were able to further evaluate at the bedside and were not only able to register the abnormal VOR but also localize its deterioration to a particular semicircular canal eroded by the fistula. Conclusion. Vestibuloocular reflex evaluation is mandatory in patients with suspected labyrinthine fistula due to cholesteatoma of the middle ear before proceeding to surgery. We demonstrate successful use of a bedside head impulse test for further evaluation prior to surgery in patients with false negative fistula test.

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Kinematics of the Rotational Vestibuloocular Reflex: Role of the Cerebellum

Journal of Neurophysiology ◽

10.1152/jn.00215.2007 ◽

2007 ◽

Vol 98 (1) ◽

pp. 295-302 ◽

Cited By ~ 4

Author(s):

Mark F. Walker ◽

Jing Tian ◽

David S. Zee

Keyword(s):

Tilt Angle ◽

Three Dimensional ◽

Head Rotation ◽

Normal Subjects ◽

Eye Position ◽

Vestibuloocular Reflex ◽

Gaze Stabilization ◽

Eye Rotation ◽

Axis Rotation ◽

Head Impulses

We studied the effect of cerebellar lesions on the 3-D control of the rotational vestibuloocular reflex (RVOR) to abrupt yaw-axis head rotation. Using search coils, three-dimensional (3-D) eye movements were recorded from nine patients with cerebellar disease and seven normal subjects during brief chair rotations (200°/s2 to 40°/s) and manual head impulses. We determined the amount of eye-position dependent torsion during yaw-axis rotation by calculating the torsional-horizontal eye-velocity axis for each of three vertical eye positions (0°, ±15°) and performing a linear regression to determine the relationship of the 3-D velocity axis to vertical eye position. The slope of this regression is the tilt angle slope. Overall, cerebellar patients showed a clear increase in the tilt angle slope for both chair rotations and head impulses. For chair rotations, the effect was not seen at the onset of head rotation when both patients and normal subjects had nearly head-fixed responses (no eye-position-dependent torsion). Over time, however, both groups showed an increasing tilt-angle slope but to a much greater degree in cerebellar patients. Two important conclusions emerge from these findings: the axis of eye rotation at the onset of head rotation is set to a value close to head-fixed (i.e., optimal for gaze stabilization during head rotation), independent of the cerebellum and once the head rotation is in progress, the cerebellum plays a crucial role in keeping the axis of eye rotation about halfway between head-fixed and that required for Listing's Law to be obeyed.

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Long-term adaptive changes in primate vestibuloocular reflex. II. Electrophysiological observations on semicircular canal primary afferents.

Journal of Neurophysiology ◽

10.1152/jn.1980.43.5.1426 ◽

1980 ◽

Vol 43 (5) ◽

pp. 1426-1436 ◽

Cited By ~ 33

Author(s):

F A Miles ◽

D J Braitman

Keyword(s):

Semicircular Canal ◽

Primary Afferents ◽

Vestibuloocular Reflex ◽

Adaptive Changes

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Semicircular canal plane head impulses detect absent function of individual semicircular canals

Brain ◽

10.1093/brain/121.4.699 ◽

1998 ◽

Vol 121 (4) ◽

pp. 699-716 ◽

Cited By ~ 120

Author(s):

P. Cremer

Keyword(s):

Semicircular Canal ◽

Semicircular Canals ◽

Head Impulses

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Vertical Eye Position–Dependence of the Human Vestibuloocular Reflex During Passive and Active Yaw Head Rotations

Journal of Neurophysiology ◽

10.1152/jn.1999.81.5.2415 ◽

1999 ◽

Vol 81 (5) ◽

pp. 2415-2428 ◽

Cited By ~ 28

Author(s):

Matthew J. Thurtell ◽

Ross A. Black ◽

G. Michael Halmagyi ◽

Ian S. Curthoys ◽

Swee T. Aw

Keyword(s):

Three Dimensional ◽

Head Position ◽

Eye Position ◽

Vestibuloocular Reflex ◽

Head Velocity ◽

High Acceleration ◽

Position Dependence ◽

Head Impulses ◽

Eye Velocity ◽

Head Rotations

Vertical eye position–dependence of the human vestibuloocular reflex during passive and active yaw head rotations. The effect of vertical eye-in-head position on the compensatory eye rotation response to passive and active high acceleration yaw head rotations was examined in eight normal human subjects. The stimuli consisted of brief, low amplitude (15–25°), high acceleration (4,000–6,000°/s2) yaw head rotations with respect to the trunk (peak velocity was 150–350°/s). Eye and head rotations were recorded in three-dimensional space using the magnetic search coil technique. The input-output kinematics of the three-dimensional vestibuloocular reflex (VOR) were assessed by finding the difference between the inverted eye velocity vector and the head velocity vector (both referenced to a head-fixed coordinate system) as a time series. During passive head impulses, the head and eye velocity axes aligned well with each other for the first 47 ms after the onset of the stimulus, regardless of vertical eye-in-head position. After the initial 47-ms period, the degree of alignment of the eye and head velocity axes was modulated by vertical eye-in-head position. When fixation was on a target 20° up, the eye and head velocity axes remained well aligned with each other. However, when fixation was on targets at 0 and 20° down, the eye velocity axis tilted forward relative to the head velocity axis. During active head impulses, the axis tilt became apparent within 5 ms of the onset of the stimulus. When fixation was on a target at 0°, the velocity axes remained well aligned with each other. When fixation was on a target 20° up, the eye velocity axis tilted backward, when fixation was on a target 20° down, the eye velocity axis tilted forward. The findings show that the VOR compensates very well for head motion in the early part of the response to unpredictable high acceleration stimuli—the eye position– dependence of the VOR does not become apparent until 47 ms after the onset of the stimulus. In contrast, the response to active high acceleration stimuli shows eye position–dependence from within 5 ms of the onset of the stimulus. A model using a VOR-Listing’s law compromise strategy did not accurately predict the patterns observed in the data, raising questions about how the eye position–dependence of the VOR is generated. We suggest, in view of recent findings, that the phenomenon could arise due to the effects of fibromuscular pulleys on the functional pulling directions of the rectus muscles.

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Head impulses reveal loss of individual semicircular canal function

Journal of Vestibular Research ◽

10.3233/ves-1999-9304 ◽

1999 ◽

Vol 9 (3) ◽

pp. 173-180

Author(s):

S.T. Aw ◽

G.M. Halmagyi ◽

R.A. Black ◽

I.S. Curthoys ◽

R.A. Yavor ◽

...

Keyword(s):

Semicircular Canal ◽

Three Dimensional ◽

Semicircular Canals ◽

Normal Subjects ◽

Three Dimensions ◽

Posterior Canal ◽

Head Velocity ◽

Ocular Reflex ◽

Vestibular Ocular Reflex ◽

Head Impulses

We studied individual semicircular canal responses in three dimensions to high-acceleration head rotations (“head impulses”) in subjects with known surgical lesions of the semicircular canals, and compared their results to those of normal subjects. We found that vestibular-ocular reflex (VOR) gains at close to peak head velocity in response to yaw, pitch and roll impulses were reliable indicators of semicircular canal function. When compared to normals, lateral canal function showed a 70–80% gain at peak of yaw head velocity during ipsilesional yaw impulses. After the loss of one vertical canal function there was a 30–50% and torsional VOR gain in response to ipsilesional pitch and roll impulses respectively. Bilateral deficits in anterior or posterior canal function resulted in a 80–90% impulses, while the loss of ipsilateral anterior and posterior canal functions will result in a 80–90% ipsilesional roll impulses. Three-dimensional vector analysis and animation of the VOR responses in a unilateral vestibular deafferented subject to yaw, pitch and roll impulses further demonstrated the deficits in magnitude and direction of the VOR responses following the loss of unilateral lateral, anterior and posterior canal functions.

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