Changes in the dynamics of the vertical vestibulo-ocular reflex due to linear acceleration in the frontal plane of the cat

Summary The vertical and horizontal components of the vestibulo-ocular reflex (VOR) were recorded in alert, restrained cats who were placed on their sides and subjected to whole-body rotations in the horizontal plane. The head was either on the axis or 45 cm eccentric from the axis of rotation. During off-axis rotation there was a change in the linear force acting on the otolith organs due to the presence of a centripetal acceleration along the animal's vertical axis. Otolith forces (defined to be opposite to the centripetal acceleration) directed ventrally with respect to the animal (negative) decreased both the amplitude and time constant of the first-order approximation to the slow phase eye velocity of the vertical vestibulo-ocular reflex (VVOR). Otolith forces directed dorsally (positive) increased the amplitude and time constant. The effects were greater for the up VOR. The asymmetry in the VVOR time constant also depended on the otolith forces, being less in the presence of negative otolith forces that caused the resultant otolith force to move ventrally, towards the direction along which gravity normally acts when the animal is in the upright position. The effects of otolith forces on the up VVOR were independent of whether the animals were tested in the dark or in the light with a stationary visual surround (i.e., during visual suppression). In contrast, the changes in the time constant of the down VVOR were smaller during visual suppression. Simulations of the eye velocity storage mechanism suggest that the gain of the feedback in the storage integrator was modified by the angle between the resultant otolith force and an animal-fixed reference. This could be the animal's vertical, i.e., the direction along which gravity normally acts. For larger angles the feedback was less and the amplitude and time constant of the VVOR increased. The transformation of the otolith input was the same for both the up and down VOR, even though the final effect on the eye velocity was asymmetric (larger for up VOR) due to a separate, asymmetric gain element in the velocity storage feedback pathway.     

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     

Visual-vestibular interaction in early infancy

The development of visual and vestibular control of smooth gaze adjustments was studied longitudinally in 3- to 18-week-old infants. Eye and head movements were measured with electro-oculography (EOG) and an optoelectronic system, respectively. The infant was placed in a chair providing full support to the trunk but allowing relatively free head movements. The chair was positioned at the center of a striped-patterned drum. The chair and the drum were oscillated sinusoidally, either individually or in synchrony at 0.25 Hz. When the drum oscillated around the infant (the optokinetic response condition, OKR), the gain of both smooth eye and head tracking components was low up to 6 weeks of age, after which the eye gain increased dramatically and the lag decreased. The most substantial increase in head gain was observed at 13-18 weeks of age. When only the chair was oscillated (visual VOR, VVOR), the compensatory eye gain was high at 3 weeks and the head contributed significantly to the compensation (vestibulocollic reflex, VCR). The head gain increased significantly at 13-18 weeks of age as in the OKR case. When the drum and the chair were oscillated synchronously (inhibition of VOR, VORINHIB), the compensatory eye gain was significantly lower than in the VVOR, indicating suppression of VOR. This effect was considerable at 3 weeks. However, VCR was not suppressed but comparable to the VVOR condition at all ages studied. In summary, we found that the vestibular control of smooth gaze adjustment functions earlier than the visual control. At 2 months, the visual control improves dramatically and at 3-4 months head participation increases considerably. The eye gain in the VORINHIB condition could be well predicted by vector addition of the eye position signals in the OKR and VVOR conditions.     

Specific effects of unilateral lesions in the flocculus upon eye movements in albino rabbits

Summary The horizontal vestibulo-ocular reflex (HVOR) and optokinetic response (OKR) were examined in alert albino rabbits following unilateral flocculectomy. Chemical flocculectomy with local application of kainic acid was used to avoid the retrograde degeneration of inferior olive neurons that accompanies surgical flocculectomy. Effects of chemical flocculectomy, however, were identical to those of surgical flocculectomy. The following functional deficiencies were observed in the movements of the ipsilateral eye: (1) reduction of the HVOR gain; (2) increased lag of the HVOR phase; (3) increased non-linearity of the relationship between the HVOR gain and the amplitude of turntable rotation; (4) decreased OKR gain; (5) delay with increased variation in the OKR phase; (6) impairment of rapid visual-vestibular interaction; (7) loss of the adaptation of the HVOR. Only a transient depression of the HVOR gain was seen in the contralateral eye. Control experiments with lesions in the paraflocculus, nodulus, and uvula, or lobules VI and VII, revealed no such deficiencies, except that lesions in the nodulus and uvula produced marked advancement of the HVOR phase. The effects of flocculectomy are consistent with present knowledge of both neuronal circuitry and activity of the rabbit flocculus.Abbreviations and Definitions iHVOR and iOKR HVOR and OKR in the eye ipsilateral to flocculectomy - cHVOR and cOKR HVOR and OKR in the eye contralateral to flocculectomy - HVOR gain amplitude ratio of eye movement in darkness to turntable rotation - OKR gain amplitude ratio of eye movement to light slit movement - HVOR phase defined as 0 ° when the eye movement is shifted 180 ° with respect to the rotation of the turntable - OKR phase defined as 0 ° when the eye movement is shifted 0 ° with respect to light slit movement Supported by a grant from the Japanese Ministry of Education, Science, and Culture (544021)On leave from Nencki Institute of Experimental Biology (Warsaw) and supported by a Polish-Japanese Cultural Relations Program Fellowship (January 1977 through January 1978, and April 1979 through October 1979)     

Adaptive modification of the cat's vestibulospinal reflex during sustained vestibular and neck stimulation

In decerebrate cats, rotation about the longitudinal axis of the whole animal at 0.15 Hz,±10° produced an increased electromyogram (EMG) activity of the triceps brachii during side-down tilt and a decreased activity during side-up tilt. This vestibulospinal reflex (VSR) was tested before, during and after a sustained (3-h) period of roll tilt of the head at the parameters indicated above, associated with a synchronous roll tilt of the body at 0.15 Hz, but at the peak amplitude of either 12.5° or 7.5°. This additional stimulus led to 2.5° of neck rotation, which was respectively out of phase (condition A) or in-phase (condition B) with head rotation. In a few instances the peak amplitude of neck rotation was increased to 5°. In the first experimental condition A, the gain of the VSR (tested every 10–15 min) progressively increased, starting from the first hour of out of phase neck-vestibular stimulation to reach, on average, 241% of the control value at the end of the third hour of stimulation. On the other hand, in the second experimental condition B, the mean gain of the VSR first decreased to 82% during the first hour of in-phase neck-vestibular stimulation, but then increased to 165% of the corresponding control during the last hour of recording. In other experiments an adaptive increase in gain of the pure VSR occurred during a sustained (3-h) period of selective roll tilt of the whole animal, but it was less consistent and, on average, smaller in amplitude than that obtained during out of phase neck-vestibular stimulation.The adaptive changes in gain of the VSR described above were not associated with changes in the phase angle of the responses, and were also observed during the post-adaptation period. Further experiments indicated that the gain of the N-VSR, i. e. of the EMG responses to combined neck-vestibular stimulation, displayed a prominent adaptive increase during the sustained out of phase stimulation, but not during the inphase stimulation.     

The human vertical vestibulo-ocular reflex during combined linear and angular acceleration with near-target fixation

The purpose of this study was to examine the effect of fixation target distance on the human vestibuloocular reflex (VOR) during eccentric rotation in pitch. Such rotation induces both angular and linear acceleration. Eight normal subjects viewed earth-fixed targets that were either remote or near to the eyes during wholebody rotation about an earth-horizontal axis that was either oculocentric or 15 cm posterior (eccentric) to the eyes. Eye and head movements were recorded using magnetic search coils. Using a servomotor-driven chair, passive whole-body rotations were delivered as trains of single-frequency sinusoids at frequencies from 0.8 to 2.0 Hz and as pseudorandom impulses of acceleration. In the light, the visually enhanced VOR (VVOR) was recorded while subjects were asked to fixate targets at one of several distances. In darkness, subjects were asked to remember targets that had been viewed immediately prior to the rotation. In order to eliminate slip of the retinal image of a near target when the axis of rotation of the head is posterior to the eyes, the ideal gain (compensatory eye velocity divided by head velocity) of the VVOR and VOR must exceed 1.0. Both the VOR and VVOR were found to have significantly enhanced gains during sinusoidal and pseudorandom impulses of rotation (P<0.05). Enhancement of VVOR gain was greatest at low frequencies of head rotation and decreased with increasing frequency. However, enhanced VOR gain only slightly exceeded 1.0, and VVOR gain enhancement was significantly lower than the expected ideal values for the stimulus conditions employed (P<0.05). During oculocentric rotations with near targets, both the VOR and VVOR tended to exhibit small phase leads that increased with rotational frequency. In contrast, during eccentric rotations with near targets, there were small phase lags that increased with frequency. Visual tracking contributes during ocular compensatory responses to sustained head rotation, although the latency of visual tracking reflexes exceeds 100 ms. In order to study initial vestibular responses prior to modification by visual tracking, we presented impulses of head acceleration in pseudorandom sequence of initial positions and directions, and evaluated the ocular response in the epoch from 25 to 80 ms after movement onset. As with sinusoidal rotations, pseudorandom eccentric head rotation in the presence of a near, earth-fixed target was associated with enhancement of VVOR and VOR gains in the interval from 25 to 80 ms from movement onset. Despite the inability of visual tracking to contribute to these responses, VVOR gain significantly exceeded VOR gain for pseudorandom accelerations. This gain enhancement indicates that target distance and linear motion of the head are considered by the human ocular motor system in adjustment of performance of the early VOR, prior to a contribution by visual following reflexes. Vergence was appropriate to target distance during all VVOR rotations, but varied during VOR rotations with remembered targets. For the 3-m target distance, vergence during the VOR was stable over each entire trial but slightly exceeded the ideal value. For the 0.1-m near target, instantaneous vergence during the VOR typically declined gradually in a manner not corresponding to the time course of instantaneous VOR gain change; mean vergence over entire trials ranged from 60 to 90% of ideal, corresponding to target distances for which ideal gain would be much higher than actually observed. These findings suggest a dissociation between vergence and VOR gain during eccentric rotation with near targets in the frequency range from 0.8 to 2.0 Hz.     

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.     

Cerebellar nodulectomy impairs spatial memory of vestibular and optokinetic stimulation in rabbits

Natural vestibular and optokinetic stimulation were used to investigate the possible role of the cerebellar nodulus in the regulation and modification of reflexive eye movements in rabbits. The nodulus and folium 9d of the uvula were destroyed by surgical aspiration. Before and after nodulectomy the vertical and horizontal vestibuloocular reflexes (VVOR, HVOR) were measured during sinusoidal vestibular stimulation about the longitudinal (roll) and vertical (yaw) axes. Although the gain of the HVOR (G(HVOR) = peak eye movement velocity/peak head velocity) was not affected by the nodulectomy, the gain of the VVOR (G(VVOR)) was reduced. The gains of the vertical and horizontal optokinetic reflexes (G(VOKR), G(HOKR)) were measured during monocular, sinusoidal optokinetic stimulation (OKS) about the longitudinal and vertical axes. Following nodulectomy, there was no reduction in G(VOKR) or G(HOKR). Long-term binocular OKS was used to generate optokinetic afternystagmus, OKAN II, that lasts for hours. After OKAN II was induced, rabbits were subjected to static pitch and roll, to determine how the plane and velocity of OKAN II is influenced by a changing vestibular environment. During static pitch, OKAN II slow phase remained aligned with earth-horizontal. This was true for normal and nodulectomized rabbits. During static roll, OKAN II remained aligned with earth-horizontal in normal rabbits. During static roll in nodulectomized rabbits, OKAN II slow phase developed a centripetal vertical drift. We examined the suppression and recovery of G(VVOR) following exposure to conflicting vertical OKS for 10-30 min. This vestibular-optokinetic conflict reduced G(VVOR) in both normal and nodulectomized rabbits. The time course of recovery of G(VVOR) after conflicting OKS was the same before and after nodulectomy. In normal rabbits, the head pitch angle, at which peak OKAN II velocity occurred, corresponded to the head pitch angle maintained during long-term OKS. If the head was maintained in a "pitched-up" or "pitched-down" orientation during long-term OKS, the subsequently measured OKAN II peak velocity occurred at the same orientation. This was not true for nodulectomized rabbits, who had OKAN II peak velocities at head pitch angles independent of those maintained during long-term OKS. We conclude that the nodulus participates in the regulation of compensatory reflexive movements. The nodulus also influences "remembered" head position in space derived from previous optokinetic and vestibular stimulation.     

Acute adaptation of the vestibuloocular reflex: signal processing by floccular and ventral parafloccular Purkinje cells

The gain of the vertical vestibuloocular reflex (VVOR), defined as eye velocity/head velocity was adapted in squirrel monkeys by employing visual-vestibular mismatch stimuli. VVOR gain, measured in the dark, could be trained to values between 0.4 and 1.5. Single-unit activity of vertical zone Purkinje cells was recorded from the flocculus and ventral paraflocculus in alert squirrel monkeys before and during the gain change training. Our goal was to evaluate the site(s) of learning of the gain change. To aid in the evaluation, a model of the vertical optokinetic reflex (VOKR) and VVOR was constructed consisting of floccular and nonfloccular systems divided into subsystems based on the known anatomy and input and output parameters. Three kinds of input to floccular Purkinje cells via mossy fibers were explicitly described, namely vestibular, visual (retinal slip), and efference copy of eye movement. The characteristics of each subsystem (gain and phase) were identified at different VOR gains by reconstructing single-unit activity of Purkinje cells during VOKR and VVOR with multiple linear regression models consisting of sensory input and motor output signals. Model adequacy was checked by evaluating the residual following the regressions and by predicting Purkinje cells' activity during visual-vestibular mismatch paradigms. As a result, parallel changes in identified characteristics with VVOR adaptation were found in the prefloccular/floccular subsystem that conveys vestibular signals and in the nonfloccular subsystem that conveys vestibular signals, while no change was found in other subsystems, namely prefloccular/floccular subsystems conveying efference copy or visual signals, nonfloccular subsystem conveying visual signals, and postfloccular subsystem transforming Purkinje cell activity to eye movements. The result suggests multiple sites for VVOR motor learning including both flocculus and nonflocculus pathways. The gain change in the nonfloccular vestibular subsystem was in the correct direction to cause VOR gain adaptation while the change in the prefloccular/floccular vestibular subsystem was incorrect (anti-compensatory). This apparent incorrect directional change might serve to prevent instability of the VOR caused by positive feedback via the efference copy pathway.     

Adaptive modification of the rabbit's horizontal vestibulo-ocular reflex during sustained vestibular and optokinetic stimulation

Summary Adaptability of the horizontal vestibulo-ocular reflex (HVOR) and the optokinetic response (OKR) was examined in alert albino rabbits during sustained runs lasting 5–12 h under four different stimulus conditions. (1) Sinusoidal rotation of the rabbit in darkness by 5 ° at 1/10 Hz, or (2) sinusoidal movement of a vertical slit light by 2.5 ° or 5 ° at 1/10 Hz around the optical axis of the stationary rabbit, affected the gain of neither the HVOR nor the OKR. (3) Combination of the stimulus as in (1) with the stationary slit light increased the gain of the HVOR gradually. A plateau at about 140% of the initial control was reached in 5 h. (4) Combination of the stimulus as in (1) with the slit light movement by 10 ° in phase with the turntable decreased the HVOR gain gradually, a plateau being obtained at about 70 % of the initial control in 5 h. Changes of the HVOR gain induced in conditions (3) and (4) were not frequency-specific and accompanied by no significant modification of either the gain or phase of the OKR or the linear property of HVOR-OKR interaction. A small but significant change of the HVOR phase was also detected under the condition (3) but not (4).On leave from Nencki Institute of Experimental Biology, Warsaw (from Jan. 1977 to Jan. 1978) and supported by a Polish-Japanese Cultural Relations Program Fellowship     

Evaluation of the vestibulo-ocular reflex using sinusoidal off-vertical axis rotation in patients with acoustic neurinoma

The vestibulo-ocular reflex (VOR) was studied to examine the utility of off-vertical axis rotation (OVAR) in the diagnosis of acoustic neurinoma. Subjects were sinusoidally rotated with eyes open in complete darkness at frequencies of 0.4 and 0.8 Hz with a maximum angular velocity of 60°/s at either earth-vertical axis rotation (EVAR) or OVAR. Thirteen patients with acoustic neurinomas were investigated. Results showed that VOR gain during OVAR at 0.8 Hz and in a 30° nose-up position in patients with internal auditory canal tumors was significantly less than the gain measured during EVAR. The VOR gain measured from all patients (including those with tumors extending to the cerebellopontine angle) was not significantly different when the patients were subjected to EVAR and OVAR. These observations were possibly due to superior vestibular nerve dysfunction. We concluded that certain stimulating parameters—patient's nose tilted up 30°; sinusoidal OVAR at 0.8 Hz and 60°/s maximum angular head velocity—were useful for evaluating vestibular function in patients suffering from an acoustic neurinoma located within the internal auditory canal.     

The effects of head and trunk position on torsional vestibular and optokinetic eye movements in humans

We measured torsional vestibular and optokinetic eye movements in human subjects with the head and trunk erect, with the head supine and the trunk erect, and with the head and trunk supine, in order to quantify the effects of otolithic and proprioceptive modulation. During active head movements, the torsional vestibulo-ocular reflex (VOR) had significantly higher gain with the head upright than with the head supine, indicating that dynamic otolithic inputs can supplement the semicircular canal-ocular reflex. During passive earth-vertical axis rotation, torsional VOR gain was similar with the head and trunk supine and with the head supine and the trunk erect. This finding implies that static proprioceptive information from the neck and trunk has little effect upon the torsional VOR. VOR gain with the head supine was not increased by active, self-generated head movement compared with passive, whole body rotation, indicating that the torsional VOR is not augmented by dynamic proprioceptive inputs or by an efference copy of a command for head movement. Viewing earth-fixed surroundings enhanced the torsional VOR, while fixating a chair-fixed target suppressed the VOR, especially at low frequencies. Torsional optokinetic nystagmus (OKN) evoked by a full-field stimulus had a mean slow-phase gain of 0.22 for 10°/s drum rotation, but gain fell to 0.06 for 80°/s stimuli. Despite this fall in gain, mean OKN slow-phase velocities increased with drum speed, reaching maxima of 2.5°/s–8.0°/s in our subjects. Optokinetic afternystagmus (OKAN) was typically absent. Torsional OKN and OKAN were not modified by otolithic or proprioceptive changes caused by altering head and trunk position with respect to gravity. Torsional velocity storage is negligible in humans, regardless of head orientation.Presented in part at the Society for Neuroscience Annual Meeting, October 31, 1989, Phoenix, AZ     

Senescence of human visual-vestibular interactions: smooth pursuit,optokinetic, and vestibular control of eye movements with aging

Natural aging entails progressive deterioration in a variety of biological systems. This study focuses on visual and vestibular influences on human eye movements as a function of aging. Eye movements were recorded (search-coil technique) during visual, vestibular, and combined stimuli in subjects across a broad range of ages (18–89 years). Two types of visual following were assessed: smooth pursuit (SP) of a small discrete target, and optokinetic (OKR) following of a large-field striped image. The vestibulo-ocular reflex (VOR) was studied during head rotation in darkness. Visualvestibular interactions were recorded during rotation in two ways: when the optokinetic scene was earth-fixed, resulting in visual enhancement of the VOR (VVOR), and when the visual image was head-fixed, allowing visual suppression of the VOR (VSVOR). Stimuli consisted of horizontal sinusoidal oscillations over the frequency range 0.025–4 Hz. Trials were analyzed to yield response gain (peak horizontal eye/stimulus velocities) and phase (asynchrony, in degrees, between eye and stimulus velocity signals). VOR gain in young subjects was greatest (near 0.9) at 2.5–4 Hz but declined steadily with decreasing frequency, while phase hovered near zero until 0.1 Hz and then developed a progressively increasing lead. Effects of advancing age were small, given the modest head velocities presented, and were most noticeable as an increase in phase lead and decline in gain at the lowest frequencies (0.1 Hz). The two forms of visual following and all conditions of visual-vestibular interactions displayed more prominent age-dependent changes. OKR and SP response characteristics (0.25–4 Hz) closely resembled each other. Gain was greatest at 0.25 Hz, while phase was near 0°. As frequency increased, gain declined while phase lag rose. However, both gain and phase lag tended to be slightly greater for OKR than for SP responses. Both SP and OKR response properties deteriorated progressively with increasing age, as witnessed by a progressive decline in gain and increase in phase lag, even at modest frequencies (e.g., 0.25–1.0 Hz). VVOR responses were generally closer to the ideal of 1.0 in gain and 0° in phase than either the VOR or visual following alone. A subtle but significant age-dependent decline in VVOR performance occurred at the lowest frequencies. VSVOR response characteristics were close to those of the VOR and VVOR at 4 Hz, where visual influences on eye movements are generally inconsequential. As frequency declined, visual suppression became more robust and gain dropped. The SP stimulus seemed surprisingly more effective than the OK scene in suppressing the VOR, but this effect is predicted by a linear model of visual-vestibular interactions. As age increased, visual influences on the VOR became progressively weaker, in concert with deterioration of visual following. The subjective sensation of circular vection (CV), a psychophysical measure of VVI, was assessed during optokinetic stimulation at 0.025 Hz. Interestingly, the likelihood and intensity of CV increased with aging, suggesting that visual inputs to the perception of self-motion are enhanced in the elderly. This may represent a form of visual compensation for age-dependent loss of vestibular self-rotation cues. In brief, the VOR, visual following, and their interactions display specific changes in response properties as a function of natural aging. The modifications may be interpreted as age-dependent deteriorations in the performance of systems underlying the control of human eye movements.     

Torsional and horizontal vestibular ocular reflex adaptation: three-dimensional eye movement analysis

This study used visual-vestibular conflict to effect short-term torsional and horizontal adaptation of the vestibulo-ocular reflex (VOR). Seven normal subjects underwent sinusoidal whole-body rotation about the earth-vertical axis for 40 min (±37°/s, 0.3 Hz) while viewing a stationary radial pattern fixed to the chair (×0 viewing). During adaptation and testing in darkness, the head was pitched either up or down 35° to excite both the horizontal and torsional VOR. The eyes were kept close to zero orbital elevation. Eye movements were recorded with a dual search coil in a three-field magnetic system. VOR gain was determined by averaging peak eye velocity from ten cycles of chair oscillation in complete darkness. The gain of the angular horizontal VOR (response to rotation about the head rostral-caudal axis) was significantly reduced after training in both head orientations. Angular torsional VOR gain (head rotation about the naso-occipital axis) was reduced in both head orientations, but this reached statistical significance only in the head down position. These results suggest that torsional and horizontal VOR gain adaptation, even when elicited together, may be subject to different influences depending upon head orientation. Differences between head up and down could be due to the relatively greater contribution of the horizontal semicircular canals with nose-down pitch. Alternatively, different VOR-adaptation processes could depend on the usual association of the head down posture to near viewing, in which case the torsional VOR is relatively suppressed.     

Evaluation of the otolith function using sinusoidal off-vertical axis rotation in patients with benign paroxysmal positional vertigo

The vestibulo-ocular reflex (VOR) was studied via sinusoidal off-vertical axis rotation (OVAR) to evaluate the otolith function in patients with benign paroxysmal positional vertigo (BPPV). Subjects were sinusoidally rotated with eyes open in complete darkness at frequencies of 0.4 and 0.8 Hz with a maximum angular velocity of 60° s⁻¹ in earth-vertical axis rotation (EVAR) and OVAR. Twenty-three controls and 24 BPPV patients were investigated. Results showed that VOR gain during OVAR at 0.8 Hz in a 30° nose-up position in BPPV patients was significantly less than the gain during EVAR, whereas the gain was not significantly different between EVAR and OVAR in the controls in each condition. In addition, to examine each type of BPPV, we also investigated whether there were any differences between the patients who suffered from dizziness and those who did not. VOR gain in OVAR of BPPV patients who were suffering from dizziness was significantly less than that of BPPV patients without dizziness. Not only cupulolithiasis or canalolithiasis, but also otolith dysfunction was considered to be the possible origin of BPPV. Because sinusoidal OVAR produced minimal nausea compared to constant velocity OVAR, the stimulation of 0.8 Hz nose-up in sinusoidal OVAR may be used to evaluate otolith function without discomfort for patients.     

A comparison of the horizontal and vertical optokinetic reflexes of the rabbit

Summary The horizontal and vertical monocular optokinetic reflexes of the rabbit were measured under closed-loop and open-loop conditions. A random noise, optokinetic stimulus subtending 70×70 deg was presented to the left eye of rabbits placed in front of a rear projection tangent screen. The position of the right eye (nonstimulated) was measured using an infrared light projection technique. During open-loop optokinetic stimulation the eye position signal was fed back to sum with a time-integrated velocity command signal driving the optokinetic stimulus. The dynamics of eye movements evoked by horizontal and vertical optokinetic stimulation were different. Horizontally evoked eye movements never exceeded a deviation of 15 deg before being interrupted by resetting saccades, which returned the eye past the primary position. By contrast, vertical eye deviations greater than 20 deg were often maintained for intervals exceeding 10 s without resetting. The closed-loop gain of optokinetically evoked horizontal eye movements was higher for monocular posterior-anterior optokinetic stimulation than for anterior-posterior stimulation. The vertical optokinetic gain for up-down stimulation was slightly greater than the gain for down-up stimulation. The vertical up-down, open-loop optokinetic gain was greater than the down-up gain over a range of retinal slip velocities of 0.5–5.0 deg/s. Measurement of the horizontal vestibulo-ocular reflex during simultaneous horizontal optokinetic stimulation demonstrated that visual and vestibular information combine linearly to produce reflex eye movements. These data suggest that the higher gain of the horizontal optokinetic reflex may compensate in part for the reduced gain of the horizontal vestibulo-ocular reflex at lower angular accelerations of the head. An equivalent vertical optokinetic gain would be obviated by the contribution of the utricular otoliths to the vertical vestibulo-ocular reflex at low frequencies of head movement.This research was supported by the National Institutes of Health Grant EY00848 and the Oregon Lions Sight and Hearing Foundation     

Eye-position dependence of torsional velocity during step-ramp pursuit and transient yaw rotation in humans

The time course of eye-position-dependent torsion during transient horizontal pursuit and yaw rotation was examined in seven normal human subjects. The stimuli consisted of step-ramp target motion (25, 40°/s) and brief chair rotation (~200°/s² accelerated to 40°/s) at three different vertical positions (center 0°, up or down 15°). Three-dimensional eye movements were recorded with dual search coils. The kinematics of pursuit and the rotational vestibulo-ocular reflex (rVOR) were assessed by determining the tilt-angle slope, a measure of the variation of the axis of eye-velocity with vertical eye position. We found that the tilt-angle slope during pursuit was initially 0.4±0.07 (mean±95% confidence interval) and then gradually rose to 0.64±0.04, at about the time that the steady-state eye-velocity was reached. The rVOR began with a nearly head-fixed axis (0.08±0.04), appropriate for full retinal image stabilization, followed by a gradual increase of the tilt-angle slope to 0.31±0.02. Thus, differences between pursuit and the rVOR with respect to Listing’s law can be seen from the onset of transient responses, although in both cases eye-position-dependent torsion increases with time. This temporal evolution of the axis of eye-velocity may involve the velocity-storage mechanism.     

Spatial coordination by descending vestibular signals

Electromyographic activity of dorsal neck muscles and neck torques was recorded to study vestibulocollic, cervicocollic, and combined reflexes in alert and decerebrate cats during rotations of the whole body, the body except for the head, and the head but not the rest of the body. Cats were rotated about many axes that lay in the frontal, sagittal, and horizontal planes using sinusoidal 0.25-Hz waveforms or sum-of-sinusoid waveforms. Robust electromyographic responses were recorded from six muscles, with response directionality that in most cases did not show strong dependence on the reflex tested or on other factors including exact neck angle, stimulus amplitude from 5° to 60°, and intact versus decerebrate state. Based on the strength of responses to rotations about all the tested axes, neck muscles could be characterized by maximal activation direction vectors representing the axis and direction of rotation in threedimensional space that was most excitatory during reflex responses. Responses to rotations about axes that lay in a coordinate plane were predicted by a cosine function of the angle between the axis under test and the maximally excitatory axis in the plane. All muscles were excited by the nose down phase of pitch rotation and by yaw and roll away from the side on which the muscle lay. Biventer cervicis was best activated by rotations with axes near nose-down pitch, and its axis of maximal activation also had small, approximately equal components of yaw and roll toward the contralateral side. Complexus was best excited by rotations with axes nearest roll, but with large components along all three axes. Occipitoscapularis was best excited by rotations about axes near pitch, but with a moderately large contralateral yaw component and a smaller but significant contralateral roll component. Splenius was best excited by rotations with a large component of contralateral yaw, considerable nose-down pitch, and a smaller component of contralateral roll. Rectus major was best excited by rotations near nose-down pitch, but with a substantial contralateral yaw component and smaller contralateral roll component. Obliquus inferior was best excited by rotations with a large component of contralateral yaw, but with considerable contralateral roll and nose-down pitch components. All muscles responded as though they received convergent input from all three semicircular canals. Vestibulocollic and combined reflex responses in alert cats and vestibulocollic, cervicocollic, and combined responses in decerebrate cats appeared to have the same directionality, as evidenced by insignificant shifts in maximal activation vectors. Cervicocollic responses in alert cats were inconsistent and often absent, but appeared upon decerebration, suggesting that higher centers suppress the cervicocollic reflex in intact animals. Decerebration and partial cerebellectomy had no significant effect on maximal activation directions, although electromyographic response magnitudes increased after each. The results suggest that common circuits or strategies are used by neck stretch and vestibular-neck reflexes. The reflex excitation directions do not match the mechanical actions of the neck muscles but agree fairly well with previously published predictions of a mathematical model of neck motor control.     

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     

Vestibulo-ocular reflex and optokinetic nystagmus in adult cats reared in stroboscopic illumination

Summary Cats reared in stroboscopic illumination (strobe reared cats) have been found to have abnormal eye movements. Visual and vestibular evoked compensatory eye movements were inefficient. Vestibuloocular reflex in the dark had a maximum gain of 0.6 (1.0 in normal animals). Optokinetic nystagmus had a mean gain which approached unity only at stimulus velocities around 7 °/s (up to 30 °/s in normal animals). The asymmetry of the Optokinetic nystagmus resulting from monocular stimulation was more pronounced in strobe reared cat than in normal animals. Interaction between vestibulo-ocular reflex and Optokinetic nystagmus to give adequate compensatory eye movements was absent in strobe reared cats: visual suppression of vestibulo-ocular reflex was absent when the animal was rotated in an illuminated environment which remained stationary with respect to the head. Optokinetic nystagmus failed to improve the gain of the vestibulo-ocular reflex when the animal was rotated in a normally lit environment. The deprived animals showed no signs of recovery after 5 months exposure to normal lighting.