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

1992 ◽  
Vol 67 (4) ◽  
pp. 861-874 ◽  
Author(s):  
L. H. Snyder ◽  
W. M. King

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)

1999 ◽  
Vol 81 (5) ◽  
pp. 2538-2557 ◽  
Author(s):  
Chiju Chen-Huang ◽  
Robert A. McCrea

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.


1999 ◽  
Vol 81 (5) ◽  
pp. 2517-2537 ◽  
Author(s):  
Chiju Chen-Huang ◽  
Robert A. McCrea

Effects of viewing distance on the responses of horizontal canal–related secondary vestibular neurons during angular head rotation. The eye movements generated by the horizontal canal–related angular vestibuloocular reflex (AVOR) depend on the distance of the image from the head and the axis of head rotation. The effects of viewing distance on the responses of 105 horizontal canal–related central vestibular neurons were examined in two squirrel monkeys that were trained to fixate small, earth-stationary targets at different distances (10 and 150 cm) from their eyes. The majority of these cells (77/105) were identified as secondary vestibular neurons by synaptic activation following electrical stimulation of the vestibular nerve. All of the viewing distance–sensitive units were also sensitive to eye movements in the absence of head movements. Some classes of eye movement–related vestibular units were more sensitive to viewing distance than others. For example, the average increase in rotational gain (discharge rate/head velocity) of position-vestibular-pause units was 20%, whereas the gain increase of eye-head-velocity units was 44%. The concomitant change in gain of the AVOR was 11%. Near viewing responses of units phase lagged the responses they generated during far target viewing by 6–25°. A similar phase lag was not observed in either the near AVOR eye movements or in the firing behavior of burst-position units in the vestibular nuclei whose firing behavior was only related to eye movements. The viewing distance–related increase in the evoked eye movements and in the rotational gain of all unit classes declined progressively as stimulus frequency increased from 0.7 to 4.0 Hz. When monkeys canceled their VOR by fixating head-stationary targets, the responses recorded during near and far target viewing were comparable. However, the viewing distance–related response changes exhibited by central units were not directly attributable to the eye movement signals they generated. Subtraction of static eye position signals reduced, but did not abolish viewing distance gain changes in most units. Smooth pursuit eye velocity sensitivity and viewing distance sensitivity were not well correlated. We conclude that the central premotor pathways that mediate the AVOR also mediate viewing distance–related changes in the reflex. Because irregular vestibular nerve afferents are necessary for viewing distance–related gain changes in the AVOR, we suggest that a central estimate of viewing distance is used to parametrically modify vestibular afferent inputs to secondary vestibuloocular reflex pathways.


2016 ◽  
Vol 116 (4) ◽  
pp. 1586-1591 ◽  
Author(s):  
Joanne Wang ◽  
Richard F. Lewis

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.


2000 ◽  
Vol 83 (1) ◽  
pp. 38-49 ◽  
Author(s):  
Benjamin T. Crane ◽  
Joseph L. Demer

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.


1995 ◽  
Vol 73 (2) ◽  
pp. 615-631 ◽  
Author(s):  
A. M. Partsalis ◽  
Y. Zhang ◽  
S. M. Highstein

1. The activity of 113 Y group neurons was recorded extracellularly in 5 alert squirrel monkeys. Sixty-two cells were recorded in naive animals, and 51 cells were recorded after adaptation of the vestibuloocular reflex (VOR) with the use of telescopic lenses. The animals were lying on their right side, so that head rotation was in the vertical (pitch) plane and optokinetic stimulation elicited vertical eye movement. The responses of most cells, as well as the concurrent eye movement, were studied during 1) the VOR, elicited in darkness or in light by sinusoidal head rotation, 2) visual following, elicited by sinusoidal rotation of a full-field optokinetic drum around the stationary animal, and 3) paradigms of visual-vestibular interaction, elicited by combined sinusoidal vestibular and optokinetic stimulation. Stimulation parameters for both head and drum velocity were usually 0.5 Hz, 35 degrees/s peak velocity. 2. Y group cells respond vigorously during visual following and during suppression of the VOR (produced by in-phase rotation of the head and the optokinetic drum); the response is approximately in-phase with eye velocity during visual following, and approximately in-phase with head velocity during suppression of the VOR. During the VOR in darkness, Y cells usually exhibit only slight modulation. The results suggest a linear interaction of visual following and vestibular signals on Y cells during vertical visual-vestibular interaction. Taking into account the excitatory projection of Y cells to superior rectus and inferior oblique motoneurons, a causal role of the Y group in rapid modification of VOR gain during visual-vestibular interaction is suggested. 3. Nine Y neurons from two animals were recorded continuously, for periods ranging from 30 min to 5 h, while the VOR was being adapted to higher or lower gain. Progressive changes of the gain of the VOR in darkness were evident after approximately 30 min from the initiation of head rotation under visual-vestibular mismatch. Consistent changes of the gain and/or phase of the neuronal response during the VOR in darkness were noted in all cases. The phase of the neuronal response gradually approximated head velocity phase during adaptation of the VOR to low gain, increases in the neuronal gain thereafter ensued; the opposite changes were observed during adaptation of the VOR to high gain. 4. Sixteen Y cells were recorded from 1 animal chronically adapted to high VOR gain with the use of magnifying lenses, and 35 cells were recorded from 2 animals chronically adapted to low VOR gain with the use of miniaturizing lenses.(ABSTRACT TRUNCATED AT 400 WORDS)


2004 ◽  
Vol 92 (3) ◽  
pp. 1501-1511 ◽  
Author(s):  
G. R. Barnes ◽  
G. D. Paige

We compared the predictive behavior of smooth pursuit (SP) and suppression of the vestibuloocular reflex (VOR) in humans by examining anticipatory smooth eye movements, a phenomenon that arises after repeated presentations of sudden target movement preceded by an auditory warning cue. We investigated whether anticipatory smooth eye movements also occur prior to cued head motion, particularly when subjects expect interaction between the VOR and either real or imagined head-fixed targets. Subjects were presented with horizontal motion stimuli consisting of a visual target alone (SP), head motion in darkness (VOR), or head motion in the presence of a real or imagined head-fixed target (HFT and IHFT, respectively). Stimulus sequences were delivered as single cycles of a velocity sinusoid (frequency: 0.5 or 1.0 Hz) that were either cued (a sound cue 400 ms earlier) or noncued. For SP, anticipatory smooth eye movements developed over repeated trials in the cued, but not the noncued, condition. In the VOR condition, no such anticipatory eye movements were observed even when cued. In contrast, anticipatory responses were observed under cued, but not noncued, HFT and IHFT conditions, as for SP. Anticipatory HFT responses increased in proportion to the velocity of preceding stimuli. In general, anticipatory gaze responses were similar in cued SP, HFT, and IHFT conditions and were appropriate for expected target motion in space. Anticipatory responses may represent the output of a central mechanism for smooth-eye-movement generation that operates during predictive SP as well as VOR modulations that are linked with SP even in the absence of real visual targets.


1986 ◽  
Vol 56 (2) ◽  
pp. 439-450 ◽  
Author(s):  
E. Viirre ◽  
D. Tweed ◽  
K. Milner ◽  
T. Vilis

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.


2002 ◽  
Vol 88 (5) ◽  
pp. 2445-2462 ◽  
Author(s):  
Keisuke Kushiro ◽  
Mingjia Dai ◽  
Mikhail Kunin ◽  
Sergei B. Yakushin ◽  
Bernard Cohen ◽  
...  

Nystagmus induced by off-vertical axis rotation (OVAR) about a head yaw axis is composed of a yaw bias velocity and modulations in eye position and velocity as the head changes orientation relative to gravity. The bias velocity is dependent on the tilt of the rotational axis relative to gravity and angular head velocity. For axis tilts <15°, bias velocities increased monotonically with increases in the magnitude of the projected gravity vector onto the horizontal plane of the head. For tilts of 15–90°, bias velocity was independent of tilt angle, increasing linearly as a function of head velocity with gains of 0.7–0.8, up to the saturation level of velocity storage. Asymmetries in OVAR bias velocity and asymmetries in the dominant time constant of the angular vestibuloocular reflex (aVOR) covaried and both were reduced by administration of baclofen, a GABAB agonist. Modulations in pitch and roll eye positions were in phase with nose-down and side-down head positions, respectively. Changes in roll eye position were produced mainly by slow movements, whereas vertical eye position changes were characterized by slow eye movements and saccades. Oscillations in vertical and roll eye velocities led their respective position changes by ≈90°, close to an ideal differentiation, suggesting that these modulations were due to activation of the orienting component of the linear vestibuloocular reflex (lVOR). The beating field of the horizontal nystagmus shifted the eyes 6.3°/ g toward gravity in side down position, similar to the deviations observed during static roll tilt (7.0°/ g). This demonstrates that the eyes also orient to gravity in yaw. Phases of horizontal eye velocity clustered ∼180° relative to the modulation in beating field and were not simply differentiations of changes in eye position. Contributions of orientating and compensatory components of the lVOR to the modulation of eye position and velocity were modeled using three components: a novel direct otolith-oculomotor orientation, orientation-based velocity modulation, and changes in velocity storage time constants with head position re gravity. Time constants were obtained from optokinetic after-nystagmus, a direct representation of velocity storage. When the orienting lVOR was combined with models of the compensatory lVOR and velocity estimator from sequential otolith activation to generate the bias component, the model accurately predicted eye position and velocity in three dimensions. These data support the postulates that OVAR generates compensatory eye velocity through activation of velocity storage and that oscillatory components arise predominantly through lVOR orientation mechanisms.


2002 ◽  
Vol 87 (5) ◽  
pp. 2337-2357 ◽  
Author(s):  
Jefferson E. Roy ◽  
Kathleen E. Cullen

The vestibuloocular reflex (VOR) effectively stabilizes the visual world on the retina over the wide range of head movements generated during daily activities by producing an eye movement of equal and opposite amplitude to the motion of the head. Although an intact VOR is essential for stabilizing gaze during walking and running, it can be counterproductive during certain voluntary behaviors. For example, primates use rapid coordinated movements of the eyes and head (gaze shifts) to redirect the visual axis from one target of interest to another. During these self-generated head movements, a fully functional VOR would generate an eye-movement command in the direction opposite to that of the intended shift in gaze. Here, we have investigated how the VOR pathways process vestibular information across a wide range of behaviors in which head movements were either externally applied and/or self-generated and in which the gaze goal was systematically varied (i.e., stabilize vs. redirect). VOR interneurons [i.e., type I position-vestibular-pause (PVP) neurons] were characterized during head-restrained passive whole-body rotation, passive head-on-body rotation, active eye-head gaze shifts, active eye-head gaze pursuit, self-generated whole-body motion, and active head-on-body motion made while the monkey was passively rotated. We found that regardless of the stimulation condition, type I PVP neuron responses to head motion were comparable whenever the monkey stabilized its gaze. In contrast, whenever the monkey redirected its gaze, type I PVP neurons were significantly less responsive to head velocity. We also performed a comparable analysis of type II PVP neurons, which are likely to contribute indirectly to the VOR, and found that they generally behaved in a quantitatively similar manner. Thus our findings support the hypothesis that the activity of the VOR pathways is reduced “on-line” whenever the current behavioral goal is to redirect gaze. By characterizing neuronal responses during a variety of experimental conditions, we were also able to determine which inputs contribute to the differential processing of head-velocity information by PVP neurons. We show that neither neck proprioceptive inputs, an efference copy of neck motor commands nor the monkey's knowledge of its self-motion influence the activity of PVP neurons per se. Rather we propose that efference copies of oculomotor/gaze commands are responsible for the behaviorally dependent modulation of PVP neurons (and by extension for modulation of the status of the VOR) during gaze redirection.


1992 ◽  
Vol 68 (6) ◽  
pp. 2003-2015 ◽  
Author(s):  
A. M. Pastor ◽  
R. R. de la Cruz ◽  
R. Baker

1. The normal and adapted vestibuloocular reflex (VOR) of goldfish was characterized by means of sinusoidal, velocity step, and position step head rotations about the vertical axis. VOR adaptation was induced by short-term, 1- to 4-h, presentation of visual and vestibular stimuli that altered the ratio of eye to head velocity. 2. The VOR response measured with sinusoidal oscillations in the dark was close to ideal compensatory values over 2 decades (1/32-2 Hz). Gain approximated unity, and phase, in relation to the head, was nearly 180 degrees. The VOR was linear within the range of head velocity tested (4-64 degrees/s). 3. Head velocity steps from 1/8 to 1 Hz produced steplike eye velocity profiles that could be divided into an early acceleration-related "dynamic" component and a later constant-velocity "sustained" period frequently separated by a sag at approximately 0.1-0.15 s from the initiation of eye movement. The sustained response exhibited no decay during the constant-velocity component of the step. 4. Higher temporal resolution of the dynamic response showed the adducting eye movement to have a shorter latency, faster rise time, and larger peak gain than the abducting eye movement. The characteristics of this directional asymmetry were similar for position steps and electrical stimulation of the vestibular nerve. However, the asymmetry was not observed during sinusoidal head rotation, the sustained component of the step response, or after electrical stimulation of the VIth and IIIrd nerves. We conclude that this directional asymmetry is of central origin and may be largely due to the parallel vestibular and abducens internuclear neuron pathways onto medial rectus motoneurons. 5. The VOR adaptation process for both higher and lower eye velocity exhibited an exponential time course with time constants of 55 and 45 min, respectively. After continuous sinusoidal training for 4 h, VOR gain reached an asymptotic level 5% away from perfect suppression in the low-gain training, but 19% away from the actual performance in the high-gain paradigm. The time constant for VOR gain reversal was 5 h, and an asymptotic level 40% less than performance was reached within 10 h. 6. Adapted VOR gain was symmetrical for both directions of eye movement measured either during sinusoidal rotation or the sustained part of the velocity step. VOR adaptation also produced a comparable gain change in the nasal and temporal directions of the dynamic component, but this reflected the asymmetric characteristics observed in the preadapted condition.(ABSTRACT TRUNCATED AT 400 WORDS)


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