A reexamination of the gain of the vestibuloocular reflex

The properties of the vestibuloocular reflex (VOR) when the axis of rotation is behind the eyes and fixation of a near target is required were studied in the monkey. The magnitude of VOR gain in each eye was found to be above 1.0 and near the ideal value for stabilizing a retinal image. Evidence that this large VOR gain was not visually mediated was provided by the observations that no reduction in gain and no phase lag were observed at high frequencies of head rotation (2 Hz), large gain was observed in the dark, and large gain was observed within 10-20 ms of the start of head rotation. The magnitude of VOR gain was found to increase with increasing radius of head rotation and also to increase with decreasing target distance. When the distances from the two eyes to the target were different the instantaneous velocities and VOR gains of the eyes were also different. The dependence on radius of rotation indicates that the VOR is mediated by a combination of otolith and canal inputs. A general model for otolith-canal interaction is proposed in which VOR gain is based on a computation of target location relative to the head. This model simplifies to the classical VOR reflex when a cyclopean eye is subjected only to angular displacement.

Download Full-text

Effect of viewing distance and location of the axis of head rotation on the monkey's vestibuloocular reflex. I. Eye movement responses

Journal of Neurophysiology ◽

10.1152/jn.1992.67.4.861 ◽

1992 ◽

Vol 67 (4) ◽

pp. 861-874 ◽

Cited By ~ 87

Author(s):

L. H. Snyder ◽

W. M. King

Keyword(s):

Eye Movement ◽

Visual Target ◽

Head Rotation ◽

Rotational Axis ◽

Viewing Distance ◽

Vestibuloocular Reflex ◽

Velocity Signal ◽

Head Velocity ◽

Axis Of Rotation ◽

Pure Delay

1. The vestibuloocular reflex (VOR) stabilizes images on the retina against movements of the head in space. Viewing distance, target eccentricity, and location of the axis of rotation may influence VOR responses because rotation of the head about most axes in space rotates and translates the eyes relative to visual targets. To study the VOR response to combined rotation and translation, monkeys were placed on a rate table and rotated briefly in the dark about a vertical axis that was located in front of or behind the eyes. The monkeys fixated a near or far visual target that was extinguished before the rotation. Eye movements were recorded from both eyes by the use of the search coil technique. 2. Peak eye velocity evoked by the VOR was linearly related to vergence angle for any axis of rotation. The percent change in the VOR with near target viewing relative to far target viewing at a vergence angle of 20 degrees was linearly related to the location of the axis of rotation. Axes located behind the eyes produced positive changes in VOR amplitude, and axes located in front of the eyes produced negative changes in VOR amplitude. An axis of rotation located in the coronal plane containing the centers of rotation of the eyes produced no modification of VOR amplitude. For any axis, the VOR compensated for approximately 90% of the translation of the eye relative to near targets. 3. The initial VOR response was not correct in magnitude but was refined by a series of three temporally delayed corrections of increasing complexity. The earliest VOR-evoked eye movement (10-20 ms after rotation onset) was independent of viewing distance and rotational axis location. In the next 100 ms, eye speed appeared to be sequentially modified three times: within 20 ms by viewing distance; within 30 ms by otolith translation; and within 100 ms by eye translation relative to the visual target. 4. These data suggest a formal model of the VOR consisting of four channels. Channel 1 conveys an unmodified head rotation signal with a pure delay of 10 ms. Channel 2 conveys an angular head velocity signal, modified by viewing distance with a pure delay of 20 ms, but invariant with respect to the location of the axis of rotation. Channel 3 conveys a linear head velocity signal, dependent on the location of the axis of rotation, that is modified by viewing distance with a pure delay of 30 ms.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text

Effect of Adaptation to Telescopic Spectacles on the Initial Human Horizontal Vestibuloocular Reflex

Journal of Neurophysiology ◽

10.1152/jn.2000.83.1.38 ◽

2000 ◽

Vol 83 (1) ◽

pp. 38-49 ◽

Cited By ~ 13

Author(s):

Benjamin T. Crane ◽

Joseph L. Demer

Keyword(s):

Head Rotation ◽

Head Movements ◽

Target Distance ◽

Whole Body ◽

Rotational Axis ◽

Vestibuloocular Reflex ◽

Head Acceleration ◽

Gain Enhancement ◽

Lower Head ◽

Distant Target

Gain of the vestibuloocular reflex (VOR) not only varies with target distance and rotational axis, but can be chronically modified in response to prolonged wearing of head-mounted magnifiers. This study examined the effect of adaptation to telescopic spectacles on the variation of the VOR with changes in target distance and yaw rotational axis for head velocity transients having peak accelerations of 2,800 and 1,000°/s2. Eye and head movements were recorded with search coils in 10 subjects who underwent whole body rotations around vertical axes that were 10 cm anterior to the eyes, centered between the eyes, between the otoliths, or 20 cm posterior to the eyes. Immediately before each rotation, subjects viewed a target 15 or 500 cm distant. Lighting was extinguished immediately before and was restored after completion of each rotation. After initial rotations, subjects wore 1.9× magnification binocular telescopic spectacles during their daily activities for at least 6 h. Test spectacles were removed and measurement rotations were repeated. Of the eight subjects tolerant of adaptation to the telescopes, six demonstrated VOR gain enhancement after adaptation, while gain in two subjects was not increased. For all subjects, the earliest VOR began 7–10 ms after onset of head rotation regardless of axis eccentricity or target distance. Regardless of adaptation, VOR gain for the proximate target exceeded that for the distant target beginning at 20 ms after onset of head rotation. Adaptation increased VOR gain as measured 90–100 ms after head rotation onset by an average of 0.12 ± 0.02 (SE) for the higher head acceleration and 0.19 ± 0.02 for the lower head acceleration. After adaptation, four subjects exhibited significant increases in the canal VOR gain only, whereas two subjects exhibited significant increases in both angular and linear VOR gains. The latencies of linear and early angular target distance effects on VOR gain were unaffected by adaptation. The earliest significant change in angular VOR gain in response to adaptation occurred 50 and 68 ms after onset of the 2,800 and 1,000°/s2 peak head accelerations, respectively. The latency of the adaptive increase in linear VOR gain was ∼50 ms for the peak head acceleration of 2,800°/s2, and 100 ms for the peak head acceleration of 1,000°/s2. Thus VOR gain changes and latency were consistent with modification in the angular VOR in most subjects, and additionally in the linear VOR in a minority of subjects.

Download Full-text

Effects of Viewing Distance on the Responses of Vestibular Neurons to Combined Angular and Linear Vestibular Stimulation

Journal of Neurophysiology ◽

10.1152/jn.1999.81.5.2538 ◽

1999 ◽

Vol 81 (5) ◽

pp. 2538-2557 ◽

Cited By ~ 42

Author(s):

Chiju Chen-Huang ◽

Robert A. McCrea

Keyword(s):

Eye Movements ◽

Eye Movement ◽

Vestibular Stimulation ◽

The Other ◽

Viewing Distance ◽

Vestibuloocular Reflex ◽

Horizontal Canal ◽

Head Velocity ◽

Vestibular Neurons ◽

Axis Of Rotation

Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation. The firing behavior of 59 horizontal canal–related secondary vestibular neurons was studied in alert squirrel monkeys during the combined angular and linear vestibuloocular reflex (CVOR). The CVOR was evoked by positioning the animal’s head 20 cm in front of, or behind, the axis of rotation during whole body rotation (0.7, 1.9, and 4.0 Hz). The effect of viewing distance was studied by having the monkeys fixate small targets that were either near (10 cm) or far (1.3–1.7 m) from the eyes. Most units (50/59) were sensitive to eye movements and were monosynaptically activated after electrical stimulation of the vestibular nerve (51/56 tested). The responses of eye movement–related units were significantly affected by viewing distance. The viewing distance–related change in response gain of many eye-head-velocity and burst-position units was comparable with the change in eye movement gain. On the other hand, position-vestibular-pause units were approximately half as sensitive to changes in viewing distance as were eye movements. The sensitivity of units to the linear vestibuloocular reflex (LVOR) was estimated by subtraction of angular vestibuloocular reflex (AVOR)–related responses recorded with the head in the center of the axis of rotation from CVOR responses. During far target viewing, unit sensitivity to linear translation was small, but during near target viewing the firing rate of many units was strongly modulated. The LVOR responses and viewing distance–related LVOR responses of most units were nearly in phase with linear head velocity. The signals generated by secondary vestibular units during voluntary cancellation of the AVOR and CVOR were comparable. However, unit sensitivity to linear translation and angular rotation were not well correlated either during far or near target viewing. Unit LVOR responses were also not well correlated with their sensitivity to smooth pursuit eye movements or their sensitivity to viewing distance during the AVOR. On the other hand there was a significant correlation between static eye position sensitivity and sensitivity to viewing distance. We conclude that secondary horizontal canal–related vestibuloocular pathways are an important part of the premotor neural substrate that produces the LVOR. The otolith sensory signals that appear on these pathways have been spatially and temporally transformed to match the angular eye movement commands required to stabilize images at different distances. We suggest that this transformation may be performed by the circuits related to temporal integration of the LVOR.

Download Full-text

Optical method of measuring angular displacement when the axis of rotation inclines

Applied Optics ◽

10.1364/ao.23.001255 ◽

1984 ◽

Vol 23 (8) ◽

pp. 1255 ◽

Cited By ~ 5

Author(s):

Keijin Sato ◽

Osamu Kamada ◽

Sumio Yamamoto ◽

Shoji Utsumi ◽

Hideo Hayashi

Keyword(s):

Optical Method ◽

Angular Displacement ◽

Axis Of Rotation

Download Full-text

Neural correlates of nystagmus in abducens nerve

Journal of Neurophysiology ◽

10.1152/jn.1979.42.5.1282 ◽

1979 ◽

Vol 42 (5) ◽

pp. 1282-1296 ◽

Cited By ~ 4

Author(s):

V. Honrubia ◽

D. B. Reingold ◽

C. G. Lau ◽

P. H. Ward

Keyword(s):

Low Frequency ◽

Abducens Nerve ◽

Head Rotation ◽

Phase Lag ◽

Neural Firing ◽

Neural Responses ◽

Firing Rates ◽

Viscous Forces ◽

Phase Angle Difference ◽

Phase Lead

1. The firing rates of action potentials of abducens nerve single fibers were recorded in the cat's orbit during a variety of vestibular and optokinetic stimulations. 2. Comparison was made of the neural firing rates associated with agonist and antagonist responses during slow and fast components of vestibular and optokinetic nystagmus. It was found that the relationship between the motoneuron firing rates and the eye motion was independent of the reflex with which they were associated--vestibular or optokinetic, or the type of response--agonist or antagonist. No neurons were observed that responded only during the fast or only during the slow nystagmus phase. Motoneuron firing rates were proportional to both velocity and position of the eye in a ratio of 1 (spikes/s)/(deg/s) to 7.2 (spikes/s)/deg. The behavior of the motoneurons was compatible with the hypothesis that thier firing rates are sufficient to overcome both elastic and viscous forces by which the muscles and ligaments hold the eye in the orbit. 3. For low-frequency head rotations, eye displacement and neural responses showed a small phase angle difference. At higher frequencies, however, while the eyes maintained a fixed relationship to the head rotation, the neural responses showed an increasing phase lead. One component of this phase lead compensated for the phase lag introduced by the orbital mechanics. The other was modeled as a constant delay of approximately 70 ms, which may be accounted for by neuromuscular transmission and transduction.

Download Full-text

Rotational kinematics of the human vestibuloocular reflex. II. Velocity steps

Journal of Neurophysiology ◽

10.1152/jn.1994.72.5.2480 ◽

1994 ◽

Vol 72 (5) ◽

pp. 2480-2489 ◽

Cited By ~ 24

Author(s):

D. Tweed ◽

M. Fetter ◽

D. Sievering ◽

H. Misslisch ◽

E. Koenig

Keyword(s):

Cross Talk ◽

Human Subjects ◽

Head Rotation ◽

Horizontal Axis ◽

Main Diagonal ◽

Velocity Storage ◽

Vestibuloocular Reflex ◽

Simple Explanation ◽

Time Constants ◽

Axis Rotation

1. Gain matrices were used to quantify the three-dimensional vestibuloocular reflex (VOR) in five human subjects who were accelerated over 1 s and then spun at a constant 150 degrees/s for 29 s in darkness. Rotations were torsional, vertical and horizontal, about earth-vertical and earth-horizontal axes. 2. Elements on the main diagonal of the gain matrices were much smaller than the optimal value of -1, and torsional gain was weaker than vertical or horizontal. Off-diagonal elements, indicating cross talk, were minimal except for a small but consistent horizontal response to torsional head rotation. 3. Downward slow phases were more than twice as fast as upward at the start of rotation about both earth-vertical and earth-horizontal axes, but the asymmetry vanished later in the rotation. 4. During earth-vertical-axis rotation, all matrix elements decayed to zero. The main-diagonal torsional and vertical gains waned with time constants close to that of the cupula (6.7 and 7.3 s). Velocity storage prolonged the horizontal response to horizontal head rotation (time constant 14.2 s) but not the horizontal response to torsion (7.7 s). A simple explanation is that velocity storage acts on a central estimate of head motion that accurately distinguishes horizontal from torsional and that the inappropriate horizontal eye velocity response to torsion occurs because of cross talk downstream from velocity storage. 5. During earth-horizontal-axis rotation, the torsional, vertical, and horizontal main-diagonal elements declined, with time constants of 7.6, 8.2, and 7.9 s, to maintained nonzero values, all equal to about -0.1. Off-diagonal elements, including the horizontal response to torsion, decayed to zero, so that the otolith-driven reflex, late in the rotation, was equally strong in all dimensions and almost free of detectable cross talk. 6. The difference between gain curves over the course of earth-vertical- and earth-horizontal-axis rotations was not constant but increased with time, suggesting that the VOR response to earth-horizontal-axis rotation is not a simple sum of canal and otolith reflexes.

Download Full-text

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.

Download Full-text

Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons

Journal of Neurophysiology ◽

10.1152/jn.1994.72.2.928 ◽

1994 ◽

Vol 72 (2) ◽

pp. 928-953 ◽

Cited By ~ 102

Author(s):

S. G. Lisberger ◽

T. A. Pavelko ◽

D. M. Broussard

Keyword(s):

Eye Movements ◽

Motor Learning ◽

Firing Rate ◽

Brain Stem ◽

Head Rotation ◽

Head Motion ◽

Vestibuloocular Reflex ◽

Neural Basis ◽

Ventral Paraflocculus ◽

The Brain

1. We recorded from neurons in the brain stem of monkeys before and after they had worn magnifying or miniaturizing spectacles to cause changes in the gain of the vestibuloocular reflex (VOR). The gain of the VOR was estimated as eye speed divided by head speed during passive horizontal head rotation in darkness. Electrical stimulation in the cerebellum was used to identify neurons that receive inhibition at monosynaptic latencies from the flocculus and ventral paraflocculus (flocculus target neurons or FTNs). Cells were studied during smooth pursuit eye movements with the head stationary, fixation of different positions, cancellation of the VOR, and the VOR evoked by rapid changes in head velocity. 2. FTNs were divided into two populations according to their responses during pursuit with the head stationary. The two groups showed increased firing during smooth eye motion toward the side of recording (Eye-ipsiversive or E-i) or away from the side of recording (Eye-contraversive or E-c). A higher percentage of FTNs showed increased firing rate for contraversive pursuit when the gain of the VOR was high (> or = 1.6) than when the gain of the VOR was low (< or = 0.4). 3. Changes in the gain of the VOR had a striking effect on the responses during the VOR for the FTNs that were E-c during pursuit with the head stationary. Firing rate increased during contraversive VOR eye movements when the gain of the VOR was high or normal and decreased during contraversive VOR eye movements when the gain of the VOR was low. Changes in the gain of the VOR caused smaller changes in the responses during the VOR of FTNs that were E-i during pursuit with the head stationary. We argue that motor learning in the VOR is the result of changes in the responses of individual FTNs. 4. The responses of E-i and E-c FTNS during cancellation of the VOR depended on the gain of the VOR. Responses tended to be in phase with contraversive head motion when the gain of the VOR was low and in phase with ipsiversive head motion when the gain of the VOR was high. Comparison of the effect of motor learning on the responses of FTNs during cancellation of the VOR with the results of similar experiments on horizontal-gaze velocity Purkinje cells in the flocculus and ventral paraflocculus suggests that the brain stem vestibular inputs to FTNs are one site of motor learning in the VOR.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text

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.

Download Full-text