The effect of gravity on the horizontal and vertical vestibulo-ocular reflex in the rat

Horizontal and vertical eye movements were recorded in alert pigmented rats using chronically implanted scleral search coils or temporary glue-on coils to test the dependence of the vestibulo-ocular reflex (VOR) upon rotation axis and body orientation. The contributions of semicircular-canal versus otolith-organ signals to the VOR were investigated by providing canal-only (vertical axis) and canal plus otolith (horizontal axis) stimulation conditions. Rotations that stimulated canals only (upright yaw and nose-up roll) produced an accurate VOR during middle- and high-frequency rotations (0.2-2 Hz). However, at frequencies below 0.2 Hz, the canal-only rotations elicited a phase-advanced VOR. The addition of a changing gravity stimulus, and thus dynamic otolith stimulation, to the canal signal (nose-up yaw, on-side yaw, and upright roll) produced a VOR response with accurate phase down to the lowest frequency tested (0.02 Hz). In order to further test the dependence of the VOR on gravitational signals, we tested vertical VOR with the head in an inverted posture (inverted roll). The VOR in this condition was advanced in phase across all frequencies tested. At low frequencies, the VOR during inverted roll was anticompensatory, characterized by slow-phase eye movement in the same direction as head movement. The substantial differences between canalonly VOR and canal plus otolith VOR suggest an important role of otolith organs in rat VOR. Anticompensatory VOR during inverted roll suggests that part of the otolith contribution arises from static tilt signals that are inverted when the head is inverted.     

Characterization of the 3D angular vestibulo-ocular reflex in C57BL6 mice

We characterized the three-dimensional angular vestibulo-ocular reflex (3D aVOR) of adult C57BL6 mice during static tilt testing, sinusoidal, and high-acceleration rotations and compared it with that of another lateral-eyed mammal with afoveate retinae (chinchilla) and two primate species with forward eye orientation and retinal foveae (human and squirrel monkey). Noting that visual acuity in mice is poor compared to chinchillas and even worse compared to primates, we hypothesized that the mouse 3D aVOR would be relatively low in gain (eye-velocity/head-velocity) compared to other species and would fall off for combinations of head rotation velocity and frequency for which peak-to-peak position changes fall below the minimum visual angle resolvable by mice. We also predicted that as in chinchilla, the mouse 3D aVOR would be more isotropic (eye/head velocity gain independent of head rotation axis) and better aligned with the axis of head rotation than the 3D aVOR of primates. In 12 adult C57BL6 mice, binocular 3D eye movements were measured in darkness during whole-body static tilts, 20-100°/s whole-body sinusoidal rotations (0.02-10 Hz) and acceleration steps of 3,000°/s2 to a 150°/s plateau (dominant spectral content 8-12 Hz). Our results show that the mouse has a robust static tilt counter-roll response gain of ~0.35 (eye-position Δ/head-position Δ) and mid-frequency aVOR gain (~0.6-0.8), but relatively low aVOR gain for high-frequency sinusoidal head rotations and for steps of head rotation acceleration (~0.5). Due to comparatively poor static visual acuity in the mouse, a perfectly compensatory 3D aVOR would confer relatively little benefit during high-frequency, low-amplitude movements. Therefore, our data suggest that the adaptive drive for maintaining a compensatory 3D aVOR depends on the static visual acuity in different species. Like chinchillas, mice have a much more nearly isotropic 3D aVOR than do the primates for which comparable data are available. Relatively greater isotropy in lateral-eyed species without retinal foveae (e.g., mice and chinchillas in the present study) compared to forward-eyed species with retinal foveae (e.g., squirrel monkeys and humans) suggests that the parallel resting optic axes and/or radially symmetric retinal foveae of primates underlie their characteristically low 3D aVOR gain for roll head rotations.     

Combined influence of vergence and eye position on three-dimensional vestibulo-ocular reflex in the monkey

This study examined two kinematical features of the rotational vestibulo-ocular reflex (VOR) of the monkey in near vision. First, is there an effect of eye position on the axes of eye rotation during yaw, pitch and roll head rotations when the eyes are converged to fixate near targets? Second, do the three-dimensional positions of the left and right eye during yaw and roll head rotations obey the binocular extension of Listing's law (L2), showing eye position planes that rotate temporally by a quarter as far as the angle of horizontal vergence? Animals fixated near visual targets requiring 17 or 8.5 degrees vergence and placed at straight ahead, 20 degrees up, down, left, or right during yaw, pitch, and roll head rotations at 1 Hz. The 17 degrees vergence experiments were performed both with and without a structured visual background, the 8.5 degrees vergence experiments with a visual background only. A 40 degrees horizontal change in eye position never influenced the axis of eye rotation produced by the VOR during pitch head rotation. Eye position did not affect the VOR eye rotation axes, which stayed aligned with the yaw and roll head rotation axes, when torsional gain was high. If torsional gain was low, eccentric eye positions produced yaw and roll VOR eye rotation axes that tilted somewhat in the directions predicted by Listing's law, i.e., with or opposite to gaze during yaw or roll. These findings were seen in both visual conditions and in both vergence experiments. During yaw and roll head rotations with a 40 degrees vertical change in gaze, torsional eye position followed on average the prediction of L2: the left eye showed counterclockwise (ex-) torsion in down gaze and clockwise (in-) torsion in up gaze and vice versa for the right eye. In other words, the left and right eye's position plane rotated temporally by about a quarter of the horizontal vergence angle. Our results indicate that torsional gain is the central mechanism by which the brain adjusts the retinal image stabilizing function of the VOR both in far and near vision and the three dimensional eye positions during yaw and roll head rotations in near vision follow on average the predictions of L2, a kinematic pattern that is maintained by the saccadic/quick phase system.     

Effect of viewing distance on the generation of vertical eye movements during locomotion

Vertical head and eye coordination was studied as a function of viewing distance during locomotion. Vertical head translation and pitch movements were measured using a video motion analysis system (Optotrak 3020). Vertical eye movements were recorded using a video-based pupil tracker (Iscan). Subjects (five) walked on a linear treadmill at a speed of 1.67 m/s (6 km/h) while viewing a target screen placed at distances ranging from 0.25 to 2.0 m at 0.25-m intervals. The predominant frequency of vertical head movement was 2 Hz. In accordance with previous studies, there was a small head pitch rotation, which was compensatory for vertical head translation. The magnitude of the vertical head movements and the phase relationship between head translation and pitch were little affected by viewing distance, and tended to orient the naso-occipital axis of the head at a point approximately 1 m in front of the subject (the head fixation distance or HFD). In contrast, eye velocity was significantly affected by viewing distance. When viewing a far (2-m) target, vertical eye velocity was 180° out of phase with head pitch velocity, with a gain of 0.8. This indicated that the angular vestibulo-ocular reflex (aVOR) was generating the eye movement response. The major finding was that, at a close viewing distance (0.25 m), eye velocity was in phase with head pitch and compensatory for vertical head translation, suggesting that activation of the linear vestibulo-ocular reflex (lVOR) was contributing to the eye movement response. There was also a threefold increase in the magnitude of eye velocity when viewing near targets, which was consistent with the goal of maintaining gaze on target. The required vertical lVOR sensitivity to cancel an unmodified aVOR response and generate the observed eye velocity magnitude for near targets was almost 3 times that previously measured. Supplementary experiments were performed utilizing body-fixed active head pitch rotations at 1 and 2 Hz while viewing a head-fixed target. Results indicated that the interaction of smooth pursuit and the aVOR during visual suppression could modify both the gain and phase characteristics of the aVOR at frequencies encountered during locomotion. When walking, targets located closer than the HFD (1.0 m) would appear to move in the same direction as the head pitch, resulting in suppression of the aVOR. The results of the head-fixed target experiment suggest that phase modification of the aVOR during visual suppression could play a role in generating eye movements consistent with the goal of maintaining gaze on targets closer than the HFD, which would augment the lVOR response. Received: 23 November 1998 / Accepted: 17 May 1999     

Head stabilization by vestibulocollic reflexes during quadrupedal locomotion in monkey

Little is known about the three-dimensional characteristics of vestibulocollic reflexes during natural locomotion. Here we determined how well head stability is maintained by the angular and linear vestibulocollic reflexes (aVCR, lVCR) during quadrupedal locomotion in rhesus and cynomolgus monkeys. Animals walked on a treadmill at velocities of 0.4-1.25 m/s. Head rotations were represented by Euler angles (Fick convention). The head oscillated in yaw and roll at stride frequencies (approximately 1-2 Hz) and pitched at step frequencies (approximately 2-4 Hz). Head angular accelerations (100-2,500 degrees/s2) were sufficient to have excited the aVOR to stabilize gaze. Pitch and roll head movements were <7 degrees , peak to peak, and the amplitude was unrelated to stride frequency. Yaw movements were larger due to spontaneous voluntary head shifts and were smaller at higher walking velocities. Head translations were small (< or =4 cm). Cynomolgus monkeys positioned their heads more forward in pitch than the rhesus monkeys. None of the animals maintained a forward head fixation point, indicating that the lVCR contributed little to compensatory head movements in these experiments. Significantly, aVCR gains in roll and pitch were close to unity and phases were approximately 180 degrees over the full frequency range of natural walking, which is in contrast to previous findings using anesthesia or passive trunk rotation with body restraint. We conclude that the behavioral state associated with active body motion is necessary to maintain head stability in pitch and roll over the full range of stride/step frequencies encountered during walking.     

Aging attenuates the vestibulorespiratory reflex in humans

Activation of the vestibular system changes ventilation in humans. The purpose of the present study was to investigate whether aging alters the vestibulorespiratory reflex in humans. Because aging attenuates the vestibulosympathetic reflex, it was hypothesized that aging would attenuate the vestibulorespiratory reflex. Changes in ventilation during engagement of the semicircular canals and/or the otolith organs were measured in fourteen young (26 ± 1 years) and twelve older subjects (66 ± 1 years). In young subjects, natural engagement of the semicircular canals and the otolith organs by head rotation increased breathing frequency during dynamic upright pitch at 0.25 Hz (15 cycles min⁻¹) and 0.5 Hz (30 cycles min⁻¹) (Δ2 ± 1 and Δ4 ± 1 breaths min⁻¹, respectively; P < 0.05) and during dynamic upright roll (Δ2 ± 1 and Δ4 ± 1, respectively; P < 0.05). In older subjects, the only significant changes in breathing frequency occurred during dynamic pitch and roll at 0.5 Hz (Δ2 ± 1 and Δ2 ± 1 for pitch and roll, respectively). Stimulation of the horizontal semicircular canals by yaw rotation increased minute ventilation in young but not older subjects. Selective engagement of the otolith organs during static head-down rotation did not alter breathing frequency in either the young or older subjects. The results of this study indicate that the vestibulorespiratory reflex is attenuated in older humans, with greater vestibular stimulation needed to activate the reflex.     

The three-dimensional vestibulo-ocular reflex evoked by high-acceleration rotations in the squirrel monkey

The aim of this study was to determine if the angular vestibulo-ocular reflex (VOR) in response to pitch, roll, left anterior–right posterior (LARP), and right anterior–left posterior (RALP) head rotations exhibited the same linear and nonlinear characteristics as those found in the horizontal VOR. Three-dimensional eye movements were recorded with the scleral search coil technique. The VOR in response to rotations in five planes (horizontal, vertical, torsional, LARP, and RALP) was studied in three squirrel monkeys. The latency of the VOR evoked by steps of acceleration in darkness (3,000°/s² reaching a velocity of 150°/s) was 5.8±1.7 ms and was the same in response to head rotations in all five planes of rotation. The gain of the reflex during the acceleration was 36.7±15.4% greater than that measured at the plateau of head velocity. Polynomial fits to the trajectory of the response show that eye velocity is proportional to the cube of head velocity in all five planes of rotation. For sinusoidal rotations of 0.5–15 Hz with a peak velocity of 20°/s, the VOR gain did not change with frequency (0.74±0.06, 0.74±0.07, 0.37±0.05, 0.69±0.06, and 0.64±0.06, for yaw, pitch, roll, LARP, and RALP respectively). The VOR gain increased with head velocity for sinusoidal rotations at frequencies 4 Hz. For rotational frequencies 4 Hz, we show that the vertical, torsional, LARP, and RALP VORs have the same linear and nonlinear characteristics as the horizontal VOR. In addition, we show that the gain, phase and axis of eye rotation during LARP and RALP head rotations can be predicted once the pitch and roll responses are characterized.This work was supported by NIH grant R01 DC02390     

Timing of low frequency responses of anterior and posterior canal vestibulo-ocular neurons in alert cats

The pitch vertical vestibulo-ocular reflex (VOR) is accurate and symmetrical when tested in the normal upright posture, where otolith organ and central velocity storage signals supplement the basic VOR mediated by the semicircular canals. However, when the animal and rotation axis are together repositioned by rolling 90° to one side, head forward pitch rotations that excite the anterior semicircular canals elicit a more accurately timed VOR than do oppositely directed rotations that excite the posterior canals. This suggests that velocity storage of posterior canal signals is lost when the head is placed on its side. We recorded from 47 VOR relay neurons, second-order vestibulo-ocular neurons, of alert cats to test whether asymmetries are evident in the responses of neurons in the medial and superior vestibular nuclei during earth-horizontal axis rotations in the normal upright posture. Neurons were identified by antidromic responses to oculomotor nucleus stimulation and orthodromic responses to labyrinth stimulation, and were classified as having primarily anterior, posterior, or horizontal canal input based on response directionality. Neuronal response gains and phases were recorded during 0.5 Hz and 0.05 Hz sinusoidal oscillations in darkness. During 0.5 Hz rotations, anterior canal second-order vestibulo-ocular neurons responded approximately in phase with head velocity (mean phase re head position, ±SE, 80°±3°, n=18), as did posterior canal second-order vestibulo-ocular neurons (mean phase 81°±1°, n=25). Lowering the rotation frequency to 0.05 Hz resulted in only slight advances in response phases of individual anterior canal second-order vestibulo-ocular neurons (mean phase 86°±6°, mean advance 7°±5°, n=12). In contrast, posterior canal second-order vestibulo-ocular neurons behaved more like semicircular canal afferents, with responses markedly phase-advanced (mean advance 28°±5°, n=14) by lowering rotation frequency to 0.05 Hz (mean phase 111°±5°, n=14). In summary, low frequency responses of anterior and posterior canal second-order vestibulo-ocular neurons recorded during horizontal axis pitch correspond to the VOR they excite during vertical axis pitch. These results show that velocity storage is evident at anterior but not posterior canal second-order vestibulo-ocular neurons. We conclude that responses of posterior canal second-order vestibulo-ocular neurons are insufficient to explain the accurate low frequency VOR phase observed during backward head pitch in the upright posture, and that velocity storage or otolith signals required for VOR accuracy are carried by other neurons. Electronic Publication     

Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis

By sensing three-dimensional (3D) head rotation and electrically stimulating the three ampullary branches of a vestibular nerve to encode head angular velocity, a multichannel vestibular prosthesis (MVP) can restore vestibular sensation to individuals disabled by loss of vestibular hair cell function. However, current spread to afferent fibers innervating non-targeted canals and otolith end organs can distort the vestibular nerve activation pattern, causing misalignment between the perceived and actual axis of head rotation. We hypothesized that over time, central neural mechanisms can adapt to correct this misalignment. To test this, we rendered five chinchillas vestibular deficient via bilateral gentamicin treatment and unilaterally implanted them with a head-mounted MVP. Comparison of 3D angular vestibulo-ocular reflex (aVOR) responses during 2 Hz, 50°/s peak horizontal sinusoidal head rotations in darkness on the first, third, and seventh days of continual MVP use revealed that eye responses about the intended axis remained stable (at about 70% of the normal gain) while misalignment improved significantly by the end of 1 week of prosthetic stimulation. A comparable time course of improvement was also observed for head rotations about the other two semicircular canal axes and at every stimulus frequency examined (0.2-5 Hz). In addition, the extent of disconjugacy between the two eyes progressively improved during the same time window. These results indicate that the central nervous system rapidly adapts to multichannel prosthetic vestibular stimulation to markedly improve 3D aVOR alignment within the first week after activation. Similar adaptive improvements are likely to occur in other species, including humans.     

The human horizontal vestibulo-ocular reflex during combined linear and angular acceleration

 We employed binocular magnetic search coils to study the vestibulo-ocular reflex (VOR) and visually enhanced vestibulo-ocular reflex (VVOR) of 15 human subjects undergoing passive, whole-body rotations about a vertical (yaw) axis delivered as a series of pseudorandom transients and sinusoidal oscillations at frequencies from 0.8 to 2.0 Hz. Rotations were about a series of five axes ranging from 20 cm posterior to the eyes to 10 cm anterior to the eyes. Subjects were asked to regard visible or remembered targets 10 cm, 25 cm, and 600 cm distant from the right eye. During sinusoidal rotations, the gain and phase of the VOR and VVOR were found to be highly dependent on target distance and eccentricity of the rotational axis. For axes midway between or anterior to the eyes, sinusoidal gain decreased progressively with increasing target proximity, while, for axes posterior to the otolith organs, gain increased progressively with target proximity. These effects were large and highly significant. When targets were remote, rotational axis eccentricity nevertheless had a small but significant effect on sinusoidal gain. For sinusoidal rotational axes midway between or anterior to the eyes, a phase lead was present that increased with rotational frequency, while for axes posterior to the otolith organs phase lag increased with rotational frequency. Transient trials were analyzed during the first 25 ms and from 25 to 80 ms after the onset of the head rotation. During the initial 25 ms of transient head rotations, VOR and VVOR gains were not significantly influenced by rotational eccentricity or target distance. Later in the transient responses, 25–80 ms from movement onset, both target distance and eccentricity significantly influenced gain in a manner similar to the behavior during sinusoidal rotation. Vergence angle generally remained near the theoretically ideal value during illuminated test conditions (VVOR), while in darkness vergence often varied modestly from the ideal value. Regression analysis of instantaneous VOR gain as a function of vergence demonstrated only a weak correlation, indicating that instantaneous gain is not likely to be directly dependent on vergence. A model was proposed in which linear acceleration as sensed by the otoliths is scaled by target distance and summed with angular acceleration as sensed by the semicircular canals to control eye movements. The model was fit to the sinusoidal VOR data collected in darkness and was found to describe the major trends observed in the data. The results of the model suggest that a linear interaction exists between the canal and otolithic inputs to the VOR. Received: 1 April 1996 / Accepted: 15 October 1996     

Eye movements during multi-axis whole-body rotations

The semi-circular canals and the otolith organs both contribute to gaze stabilization during head movement. We investigated how these sensory signals interact when they provide conflicting information about head orientation in space. Human subjects were reoriented 90 degrees in pitch or roll during long-duration, constant-velocity rotation about the earth-vertical axis while we measured three-dimensional eye movements. After the reorientation, the otoliths correctly indicated the static orientation of the subject with respect to gravity, while the semicircular canals provided a strong signal of rotation. This rotation signal from the canals could only be consistent with a static orientation with respect to gravity if the rotation-axis indicated by the canals was exactly parallel to gravity. This was not true, so a cue-conflict existed. These conflicting stimuli elicited motion sickness and a complex tumbling sensation. Strong horizontal, vertical, and/or torsional eye movements were also induced, allowing us to study the influence of the conflict between the otoliths and the canals on all three eye-movement components. We found a shortening of the horizontal and vertical time constants of the decay of nystagmus and a trend for an increase in peak velocity following reorientation. The dumping of the velocity storage occurred regardless of whether eye velocity along that axis was compensatory to the head rotation or not. We found a trend for the axis of eye velocity to reorient to make the head-velocity signal from the canals consistent with the head-orientation signal from the otoliths, but this reorientation was small and only observed when subjects were tilted to upright. Previous models of canal-otolith interaction could not fully account for our data, particularly the decreased time constant of the decay of nystagmus. We present a model with a mechanism that reduces the velocity-storage component in the presence of a strong cue-conflict. Our study, supported by other experiments, also indicates that static otolith signals exhibit considerably smaller effects on eye movements in humans than in monkeys.     

Dynamic otolith stimulation improves the low frequency horizontal vestibulo-ocular reflex

Summary The horizontal vestibulo-ocular reflex was measured electrooculographically in four cats during sinusoidal rotations in the dark at frequencies from 0.01 Hz to 1.0 Hz in five body orientations. Vertical axis rotations in the prone and supine positions were used to stimulate horizontal canals only. Horizontal axis rotations, with the cat on the left or right side or nose down (pitched 90° from prone) were used to stimulate horizontal canal plus otolith organs. At frequencies below 0.05 Hz the horizontal vestibulo-ocular reflex produced by horizontal canal plus otolith stimulation showed a more accurately compensatory response than the horizontal vestibuloocular reflex produced by horizontal canal stimulation alone. Canal plus otolith horizontal vestibulo-ocular reflex gain and phase remained relatively constant across all frequencies, while the horizontal vestibulo-ocular reflex gain and phase from orientations involving canal stimulation alone changed dramatically as rotation frequency decreased. In addition, the reflex in the supine position showed gain decreases and phase advances at higher frequencies than in the prone position.     

Spatial orientation of the angular vestibulo-ocular reflex (aVOR) after semicircular canal plugging and canal nerve section

We investigated spatial responses of the aVOR to small and large accelerations in six canal-plugged and lateral canal nerve-sectioned monkeys. The aim was to determine whether there was spatial adaptation after partial and complete loss of all inputs in a canal plane. Impulses of torques generated head thrusts of ≈ 3,000°/s2. Smaller accelerations of ≈ 300°/s2 initiated the steps of velocity (60°/s). Animals were rotated about a spatial vertical axis while upright (0°) or statically tilted fore-aft up to ± 90°. Temporal aVOR yaw and roll gains were computed at every head orientation and were fit with a sinusoid to obtain the spatial gains and phases. Spatial gains peaked at ≈ 0° for yaw and ≈ 90° for roll in normal animals. After bilateral lateral canal nerve section, the spatial yaw and roll gains peaked when animals were tilted back ≈ 50°, to bring the intact vertical canals in the plane of rotation. Yaw and roll gains were identical in the lateral canal nerve-sectioned monkeys tested with both low- and high-acceleration stimuli. The responses were close to normal for high-acceleration thrusts in canal-plugged animals, but were significantly reduced when these animals were given step stimuli. Thus, high accelerations adequately activated the plugged canals, whereas yaw and roll spatial aVOR gains were produced only by the intact vertical canals after total loss of lateral canal input. We conclude that there is no spatial adaptation of the aVOR even after complete loss of specific semicircular canal input.     

Response characteristics of semicircular canal and otolith systems in cat. II. Responses of trochlear motoneurons

1. The electrical activity of single trochlear motoneurons (TMns) and axons of second order vestibular neurons presumably terminating on these motoneurons were studied during natural stimulation of semicircular canals and otolith organs in cats anesthetized with Ketamine. 2. Null point analysis showed that TMns received an excitatory canal input from the contralateral posterior canal, and labyrinthine lesion experiments suggested that the functionally synergistic, ipsilateral anterior canal provides an inhibitory input. A small number of motoneurons showed orthogonal canal convergence. 3. In addition to the canal projections most TMns received an otolithic input. Firing rate was proportional to lateral head tilt and was of the beta type. Most units also responded to pitch with an increase and decrease in firing rate on nose-up and nose-down positioning, respectively. Lesion experiments indicated that the otolith responses are the results of reciprocal innervation of TMns by contralateral (excitatory) and ipsilateral (inhibitory) otolith projections. 4. During sinusoidal rotation in yaw (canal only stimulation) the mean phase lag re acceleration of the response of TMns increased from 60 degrees at 0.025 Hz to 126 degrees at 1.0 Hz. In roll (canal plus otolith stimulation) the phase lag of TMn responses measured 180 degrees and 130 degrees at 0.025 and 1.0 Hz, respectively. Phase-lags measured in Vi and Vc axons were less by ca. 15 degrees. 5. The otolith contribution to TMn responses in roll was calculated by vectorial subtraction of the yaw from the roll responses: A phase lag of 10 (0.025 Hz) to 90 degrees (0.5 Hz) re. displacement was noted and gain was constant over the same range. Similar lag dynamics were revealed in TMns when studied during ramp displacement of the head. 6. The possible functional role of central canal-otolith convergence and the differences between the response of primary vestibular afferents and secondary vestibular neurons and TMns will be discussed.     

Response of vestibular neurons to head rotations in vertical planes. II. Response to neck stimulation and vestibular-neck interaction

1. We have studied the responses of neurons in the lateral and descending vestibular nuclei of decerebrate cats to stimulation of neck receptors, produced by rotating the body in vertical planes with the head stationary. The responses to such neck stimulation were compared with the responses to vestibular stimulation produced by whole-body tilt, described in the preceding paper. 2. After determining the optimal vertical plane of neck rotation (response vector orientation), the dynamics of the neck response were studied over a frequency range of 0.02-1 Hz. The majority of the neurons were excited by neck rotations that brought the chin toward the ipsilateral side; most neurons responded better to roll than to pitch rotations. The typical neck response showed a low-frequency phase lead of 30 degrees, increasing to 60 degrees at higher frequencies, and a gain that increased about threefold per decade. 3. Neck input was found in about one-half of the vestibular-responsive neurons tested with vertical rotations. The presence of a neck response was correlated with the predominant vestibular input to these neurons; neck input was most prevalent on neurons with vestibular vector orientations near roll and receiving convergent vestibular input, either input from both ipsilateral vertical semicircular canals, or from canals plus the otolith organs. 4. Neurons with both vestibular and neck responses tend to have the respective orientation vectors pointing in opposite directions, i.e., a head tilt that produces an excitatory vestibular response would produce an inhibitory neck response. In addition, the gain components of these responses were similar. These results suggest that during head movements on a stationary body, these opposing neck and vestibular inputs will cancel each other. 5. Cancellation was observed in 12 out of 27 neurons tested with head rotation in the mid-frequency range. For most of the remaining neurons, the response to such a combined stimulus was greatly attenuated: the vestibular and neck interaction was largely antagonistic. 6. Neck response dynamics were similar to those of the vestibular input in many neurons, permitting cancellation to take place over a wide range of stimulus frequencies. Another pattern of interaction, observed in some neurons with canal input, produced responses to head rotation that had a relatively constant gain and remained in phase with position over the entire frequency range; such neurons possibly code head position in space.     

Complementary gain modifications of the cervico-ocular (COR) and angular vestibulo-ocular (aVOR) reflexes after canal plugging

To determine whether the COR compensates for the loss of aVOR gain, independent of species, we studied cynomolgus and rhesus monkeys in which all six semicircular canals were plugged. Gains and phases of the aVOR and COR were determined at frequencies ranging from 0.02 to 6?Hz and fit with model-based transfer functions. Following canal plugging in a rhesus monkey, the acute stage aVOR gain was small and there were absent responses to thrusts of yaw rotation. In the chronic state, aVOR behavior was characterized by a cupula/endolymph time constant of ??0.07?s, responding only to high frequencies of head rotation. COR gains were ??0 before surgery but increased to ??0.15 at low frequencies just after surgery; the COR gains increased to ??0.4 over the next 12?weeks. Nine weeks after surgery, the summated aVOR?+?COR responses compensated for head velocity in space in the 0.5?C3?Hz frequency range. The gains and phases continued to improve until the 35th week, where the combined aVOR?+?COR stabilized with gains of ??0.5?C0.6 and the phases were compensatory over all frequencies. Two cynomolgus monkeys operated 3?C12 years earlier had similar frequency characteristics of the aVOR and COR. The combined aVOR?+?COR gains were ??0.4?C0.8 with compensatory phases. To achieve gains close to 1.0, other mechanisms may contribute to gaze compensation, especially with the head free. Thus, while there are individual variations in the time of adaptation of the gain and phase parameters, the essential functional organization of the adaption to vestibular lesions is uniform across these species.     

Inactivation of semicircular canals causes adaptive increases in otolith-driven tilt responses

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.     

Noncommutative control in the rotational vestibuloocular reflex

To investigate the role of noncommutative computations in the oculomotor system, three-dimensional (3D) eye movements were measured in seven healthy subjects using a memory-contingent vestibulooculomotor paradigm. Subjects had to fixate a luminous point target that appeared briefly at an eccentricity of 20 degrees in one of four diagonal directions in otherwise complete darkness. After a fixation period of approximately 1 s, the subject was moved through a sequence of two rotations about mutually orthogonal axes in one of two orders (30 degrees yaw followed by 30 degrees pitch and vice versa in upright and 30 degrees yaw followed by 20 degrees roll and vice versa in both upright and supine orientations). We found that the change in ocular torsion induced by consecutive rotations about the yaw and the pitch axis depended on the order of rotations as predicted by 3D rotation kinematics. Similarly, after rotations about the yaw and roll axis, torsion depended on the order of rotations but now due to the change in final head orientation relative to gravity. Quantitative analyses of these ocular responses revealed that the rotational vestibuloocular reflexes (VORs) in far vision closely matched the predictions of 3D rotation kinematics. We conclude that the brain uses an optimal VOR strategy with the restriction of a reduced torsional position gain. This restriction implies a limited oculomotor range in torsion and systematic tilts of the angular eye velocity as a function of gaze direction.     

Three-dimensional vestibuloocular reflex of the monkey: optimal retinal image stabilization versus listing's law

If the rotational vestibuloocular reflex (VOR) were to achieve optimal retinal image stabilization during head rotations in three-dimensional space, it must turn the eye around the same axis as the head, with equal velocity but in the opposite direction. This optimal VOR strategy implies that the position of the eye in the orbit must not affect the VOR. However, if the VOR were to follow Listing's law, then the slow-phase eye rotation axis should tilt as a function of current eye position. We trained animals to fixate visual targets placed straight ahead or 20 degrees up, down, left or right while being oscillated in yaw, pitch, and roll at 0.5-4 Hz, either with or without a full-field visual background. Our main result was that the visually assisted VOR of normal monkeys invariantly rotated the eye around the same axis as the head during yaw, pitch, and roll (optimal VOR). In the absence of a visual background, eccentric eye positions evoked small axis tilts of slow phases in normal animals. Under the same visual condition, a prominent effect of eye position was found during roll but not during pitch or yaw in animals with low torsional and vertical gains following plugging of the vertical semicircular canals. This result was in accordance with a model incorporating a specific compromise between an optimal VOR and a VOR that perfectly obeys Listing's law. We conclude that the visually assisted VOR of the normal monkey optimally stabilizes foveal as well as peripheral retinal images. The finding of optimal VOR performance challenges a dominant role of plant mechanics and supports the notion of noncommutative operations in the oculomotor control system.     

Gravity-specific adaptation of the angular vestibuloocular reflex: dependence on head orientation with regard to gravity

The gain of the vertical angular vestibuloocular reflex (aVOR) was adaptively altered by visual-vestibular mismatch during rotation about an interaural axis, using steps of velocity in three head orientations: upright, left-side down, and right-side down. Gains were decreased by rotating the animal and visual surround in the same direction and increased by visual and surround rotation in opposite directions. Gains were adapted in one head position (single-state adaptation) or decreased with one side down and increased with the other side down (dual-state adaptation). Animals were tested in darkness using sinusoidal rotation at 0.5 Hz about an interaural axis that was tilted from horizontal to vertical. They were also sinusoidally oscillated from 0.5 to 4 Hz about a spatial vertical axis in static tilt positions from yaw to pitch. After both single- and dual-state adaptation, gain changes were maximal when the monkeys were in the position in which the gain had been adapted, and the gain changes progressively declined as the head was tilted away from that position. We call this gravity-specific aVOR gain adaptation. The spatial distribution of the specific aVOR gain changes could be represented by a cosine function that was superimposed on a bias level, which we called gravity-independent gain adaptation. Maximal gravity-specific gain changes were produced by 2-4 h of adaptation for both single- and dual-state adaptations, and changes in gain were similar at all test frequencies. When adapted while upright, the magnitude and distribution of the gravity-specific adaptation was comparable to that when animals were adapted in side-down positions. Single-state adaptation also produced gain changes that were independent of head position re gravity particularly in association with gain reduction. There was no bias after dual-state adaptation. With this difference, fits to data obtained by altering the gain in separate sessions predicted the modulations in gain obtained from dual-state adaptations. These data show that the vertical aVOR gain changes dependent on head position with regard to gravity are continuous functions of head tilt, whose spatial phase depends on the position in which the gain was adapted. From their different characteristics, it is likely that gravity-specific and gravity-independent adaptive changes in gain are produced by separate neural processes. These data demonstrate that head orientation to gravity plays an important role in both orienting and tuning the gain of the vertical aVOR.