The contribution of the horizontal semicircular canals to the response to off-vertical-axis rotation in the cat

Summary The response to off-vertical-axis rotation (OVAR) was measured in cats under circumstances in which the signals from the horizontal semicircular canals and otoliths were opposed. Opposition was achieved by sudden acceleration or deceleration during constant velocity OVAR. The degree of opposition was expressed as a canal/otolith ratio where a ratio of unity indicated agreement. For a canal/otolith ratio of 1, the OVAR gain (eye velocity/ stimulus velocity) was 0.73 (±0.13). The steady-state OVAR response was, however, reduced if the canals and otoliths were opposed. The reduction depended on the degree of opposition with a fall-off of 0.15 gain/(unit of canal/otolith ratio). These findings are discussed with respect to the central velocity store and the mechanism underlying the generation of the OVAR response.     

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     

Role of irregular otolith afferents in the steady-state nystagmus during off-vertical axis rotation.

1. During constant velocity off-vertical axis rotations (OVAR) in the dark a compensatory ocular nystagmus is present throughout rotation despite the lack of a maintained signal from the semicircular canals. Lesion experiments and canal plugging have attributed the steady-state ocular nystagmus during OVAR to inputs from the otolith organs and have demonstrated that it depends on an intact velocity storage mechanism. 2. To test whether irregularly discharging otolith afferents play a crucial role in the generation of the steady-state eye nystagmus during OVAR, we have used anodal (inhibitory) currents bilaterally to selectively and reversibly block irregular vestibular afferent discharge. During delivery of DC anodal currents (100 microA) bilaterally to both ears, the slow phase eye velocity of the steady-state nystagmus during OVAR was reduced or completely abolished. The disruption of the steady-state nystagmus was transient and lasted only during the period of galvanic stimulation. 3. To distinguish a possible effect of ablation of the background discharge rates of irregular vestibular afferents on the velocity storage mechanism from specific contributions of the dynamic responses from irregular otolith afferents to the circuit responsible for the generation of the steady-state nystagmus, bilateral DC anodal galvanic stimulation was applied during optokinetic nystagmus (OKN) and optokinetic afternystagmus (OKAN). No change in OKN and OKAN was observed.(ABSTRACT TRUNCATED AT 250 WORDS)     

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.     

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.     

Parabrachial nucleus neuronal responses to off-vertical axis rotation in macaques

The caudal aspect of the parabrachial nucleus (PBN) contains neurons responsive to whole body, periodic rotational stimulation in alert monkeys (Balaban et al. in J Neurophysiol 88:3175–3193, 2002). This study characterizes the angular and linear motion-sensitive response properties of PBN unit responses during off-vertical axis rotation (OVAR) and position trapezoid stimulation. The OVAR responses displayed a constant firing component which varied from the firing rate at rest. Nearly two-thirds of the units also modulated their discharges with respect to head orientation (re: gravity) during constant velocity OVAR stimulation. The modulated response magnitudes were equal during ipsilateral and contralateral OVARs, indicative of a one-dimensional accelerometer. These response orientations during OVAR divided the units into three spatially tuned populations, with peak modulation responses centered in the ipsilateral ear down, contralateral anterior semicircular canal down, and occiput down orientations. Because the orientation of the OVAR modulation response was opposite in polarity to the orientation of the static tilt component of responses to position trapezoids for the majority of units, the linear acceleration responses were divided into colinear dynamic linear and static tilt components. The orientations of these unit responses formed two distinct population response axes: (1) units with an interaural linear response axis and (2) units with an ipsilateral anterior semicircular canal-contralateral posterior semicircular canal plane linear response axis. The angular rotation sensitivity of these units is in a head-vertical plane that either contains the linear acceleration response axis or is perpendicular to the linear acceleration axis. Hence, these units behave like head-based (‘strapdown’) inertial guidance sensors. Because the PBN contributes to sensory and interoceptive processing, it is suggested that vestibulo-recipient caudal PBN units may detect potentially dangerous anomalies in control of postural stability during locomotion. In particular, these signals may contribute to the range of affective and emotional responses that include panic associated with falling, malaise associated with motion sickness and mal-de-debarquement, and comorbid balance and anxiety disorders.     

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.     

Recovery of otolith function in patients with benign paroxysmal positional vertigo evaluated by sinusoidal off-vertical axis rotation

The vestibulo-ocular reflex (VOR) was studied via sinusoidal off-vertical axis rotation (OVAR) to evaluate 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 degrees /s in earth vertical axis rotation (EVAR) and OVAR. Ten patients with BPPV patients were investigated. We performed OVAR tests for all patients for the following different points and compared otolith function: (1) The point at which patients had typical nystagmus; we call this state 'Before', that is, before recovery. (2) The point when their nystagmus disappeared; we call this state 'After' that is, after nystagmus disappear. Results showed that VOR gain during OVAR at 0.8 Hz in a 30 degrees nose-up position in BPPV patients was significantly less than the gain during EVAR at the point Before. On the other hand, gain was not significantly different between EVAR and OVAR at the point After. VOR gain itself at 0.8 Hz nose-up OVAR showed a significant increase at the point After compared to Before. This increase of VOR gain might be caused by the recovery of the otolith function in patients with BPPV.     

Spatial and temporal properties of eye movements produced by electrical stimulation of semicircular canal afferents

To investigate the characteristics of eye movements produced by electrical stimulation of semicircular canal afferents, we studied the spatial and temporal features of eye movements elicited by short-term lateral canal stimulation in two squirrel monkeys with plugged lateral canals, with the head upright or statically tilted in the roll plane. The electrically induced vestibuloocular reflex (eVOR) evoked with the head upright decayed more quickly than the stimulation signal provided by the electrode, demonstrating an absence of the classic velocity storage effect that improves the dynamics of the low-frequency VOR. When stimulation was provided with the head tilted in roll, however, the eVOR decayed more rapidly than when the head was upright, and a cross-coupled vertical response developed that shifted the eye's rotational axis toward alignment with gravity. These results demonstrate that rotational information provided by electrical stimulation of canal afferents interacts with otolith inputs (or other graviceptive cues) in a qualitatively normal manner, a process that is thought to be mediated by the velocity storage network. The observed interaction between the eVOR and graviceptive cues is of critical importance for the development of a functionally useful vestibular prosthesis. Furthermore, the presence of gravity-dependent effects (dumping, spatial orientation) despite an absence of low-frequency augmentation of the eVOR has not been previously described in any experimental preparation.     

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.     

Otolith and canal reflexes in human standing

We used galvanic vestibular stimulation (GVS) to identify human balance reflexes of the semicircular canals and otolith organs. The experiment used a model of vestibular signals arising from GVS modulation of the net signal from vestibular afferents. With the head upright, the model predicts that the GVS-evoked canal signal indicates lateral head rotation while the otolith signal indicates lateral tilt or acceleration. Both signify body sway transverse to the head. With the head bent forward, the model predicts that the canal signal indicates body spin about a vertical axis but the otolith signal still signifies lateral body motion. Thus, we compared electromyograms (EMG) in the leg muscles and body sway evoked by GVS when subjects stood with the head upright or bent forward. With the head upright, GVS evoked a large sway in the direction of the anodal electrode. This response was abolished with the head bent forward leaving only small, oppositely directed, transient responses at the start and end of the stimulus. With the head upright, GVS evoked short-latency (60–70 ms), followed by medium-latency (120 ms) EMG responses, of opposite polarity. Bending the head forward abolished the medium-latency but preserved the short-latency response. This is compatible with GVS evoking separate otolithic and canal reflexes, indicating that balance is controlled by independent canal and otolith reflexes, probably through different pathways. We propose that the short-latency reflex and small transient sway are driven by the otolith organs and the medium-latency response and the large sway are driven by the semicircular canals.     

The response of vestibulo-ocular reflex pathways to electrical stimulation after canal plugging

The vestibulo-ocular reflex (VOR) allows clear vision during head movements by generating compensatory eye movements. Its response to horizontal rotation is reduced after one horizontal semicircular canal is plugged, but recovers partially over time. The majority of VOR interneurons contribute to the shortest VOR pathway, the so-called three-neuron arc, which includes only two synapses in the brainstem. After a semicircular canal is plugged, transmission of signals by the three-neuron arc originating from the undamaged side may be altered during recovery. We measured the oculomotor response to single current pulses delivered to the vestibular labyrinth of alert cats between 9 h and 1 month after plugging the contralateral horizontal canal. The same response was also measured after motor learning induced by continuously-worn telescopes (optically induced motor learning). Optically induced learning did not change the peak velocity of the evoked eye movement (PEEV) significantly but, after a canal plug, the PEEV increased significantly, reaching a maximum during the first few post-plug days and then decreasing. VOR gain also showed transient changes during recovery. Because the PEEV occurred early in the eye movement evoked by a current pulse, we think the observed increase in PEEV represented changes in transmission by the three-neuron arc. Sham surgery did not result in significant changes in the response to electrical stimulation or in VOR gain. Our data suggest that different pathways and processes may underlie optically induced motor learning and recovery from plugging of the semicircular canals. Electronic Publication     

Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. II. Responses after canal plugging.

The horizontal angular vestibuloocular reflex (VOR) evoked by high-frequency, high-acceleration rotations was studied in four squirrel monkeys after unilateral plugging of the three semicircular canals. During the period (1-4 days) that animals were kept in darkness after plugging, the gain during steps of acceleration (3, 000 degrees /s(2), peak velocity = 150 degrees /s) was 0.61 +/- 0.14 (mean +/- SD) for contralesional rotations and 0.33 +/- 0.03 for ipsilesional rotations. Within 18-24 h after animals were returned to light, the VOR gain for contralesional rotations increased to 0. 88 +/- 0.05, whereas there was only a slight increase in the gain for ipsilesional rotations to 0.37 +/- 0.07. A symmetrical increase in the gain measured at the plateau of head velocity was noted after animals were returned to light. The latency of the VOR was 8.2 +/- 0. 4 ms for ipsilesional and 7.1 +/- 0.3 ms for contralesional rotations. The VOR evoked by sinusoidal rotations of 0.5-15 Hz, +/-20 degrees /s had no significant half-cycle asymmetries. The recovery of gain for these responses after plugging was greater at lower than at higher frequencies. Responses to rotations at higher velocities for frequencies >/=4 Hz showed an increase in contralesional half-cycle gain, whereas ipsilesional half-cycle gain was unchanged. A residual response that appeared to be canal and not otolith mediated was noted after plugging of all six semicircular canals. This response increased with frequency to reach a gain of 0.23 +/- 0.03 at 15 Hz, resembling that predicted based on a reduction of the dominant time constant of the canal to 32 ms after plugging. A model incorporating linear and nonlinear pathways was used to simulate the data. The coefficients of this model were determined from data in animals with intact vestibular function. Selective increases in the gain for the linear and nonlinear pathways predicted the changes in recovery observed after canal plugging. An increase in gain of the linear pathway accounted for the recovery in VOR gain for both responses at the velocity plateau of the steps of acceleration and for the sinusoidal rotations at lower peak velocities. The increase in gain for contralesional responses to steps of acceleration and sinusoidal rotations at higher frequencies and velocities was due to an increase in the gain of the nonlinear pathway. This pathway was driven into inhibitory cutoff at low velocities and therefore made no contribution for rotations toward the ipsilesional side.     

Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation

Summary Activity of vestibular only (VO) and vestibular plus saccade (VPS) units was recorded in the rostral part of the medial vestibular nucleus and caudal part of the superior vestibular nucleus of alert rhesus monkeys. By estimating the null axes of recorded units (n = 79), the optimal plane of activation was approximately the mean plane of reciprocal semicircular canals, i.e., lateral canals, left anterior-right posterior (LARP) canals or right anterior-left posterior (RALP) canals. All units were excited by rotation in a direction that excited a corresponding ipsilateral semicircular canal. Thus, they all displayed a type I response. With the animal upright, there were rapid changes in firing rates of both VO and VPS units in response to steps of angular velocity about a vertical axis. The units were bidirectionally activated during vestibular nystagmus (VN), horizontal optokinetic nystagmus (OKN), optokinetic afternystagmus (OKAN) and off-vertical axis rotation (OVAR). The rising and falling time constants of the responses to rotation indicated that they were closely linked to velocity storage. There were differences between VPS and VO neurons in that activity of VO units followed the expected time course in response to a stimulus even during periods of drowsiness, when eye volocity was reduced. Firing rates of VPS units, on the other hand, were significantly reduced in the drowsy state. Lateral canal-related units had average firing rates that were linearly related to the bias or steady state level of horizontal eye velocity during OVAR over a range of ±60 deg/s. These units could be further divided into two classes according to whether they were modulated during OVAR. Non-modulated units (n = 5) were VO types and all modulated units (n = 5) were VPS types. There was no significant difference between the bias level sensitivities relative to eye velocity of the units with and without modulation (P>0.05). The modulated units had no sustained change in firing rate in response to static head tilts and their phases relative to head position varied from unit to unit. The phase did not appear to be linked to the modulation of horizontal eye velocity during OVAR. The sensitivities of unit activity to eye velocity were similar during all stimulus modalities despite the different gains of eye velocity vs stimulus velocity during VN, OKN and OVAR. Therefore, VO and VPS units are likely to carry an eye velocity signal related to velocity storage. For example, when unit sensitivities were related to head or surround velocity, sensitivity relative to OVAR was less than for VN or OKN. Firing rates of both vertical canal-related VO and VPS units (n= 19) were strongly modulated during OVAR, although they did not show changes in discharge rate during static head tilts relative to the spatial vertical up to a maximal 25 deg. In some cases the amplitude of the modulation increased with increases in head velocity and eye velocity. Average activity of vertical canal-related units was linearly related to steady state horizontal eye velocity in the ipsilateral direction during OVAR. The mean sensitivities of RALP units were not significantly different from those of LARP neurons (P>0.05). Together, their mean sensitivity during OVAR about a subject yaw axis was 0.34 (imp/s)/(deg/s) relative to horizontal eye velocity. This could be explained as a contribution of the vertical canals to horizontal eye velocity due to their orientation in the head. During OVAR to the ipsilateral side, the bias level of neuronal activity decreased and saturated. For steps of rotation about a vertical axis with the animal upright, the firing rates of RALP and LARP units were linearly related to stimulus velocity and eye velocity. Contralateral rotation excited the units reflecting the orientation of the semicircular canals relative to the yaw axis of rotation. RALP and LARP units also responded during horizontal optokinetic stimulation producing both OKN and OKAN. All the vertical canal units had dynamic characteristics closely related to velocity storage. Their response characteristics were consistent with the model that they contribute to horizontal slow phase velocity as part of a three-dimensional system based on a semicircular canal frame of reference. Otolith-related units (n= 5) in the vestibular nuclei showed no evidence of velocity storage and were modulated in accordance with head position during OVAR. Mean amplitude of the modulation of activity during OVAR at a 20 deg tilt and 60 deg/s rotational velocity was 24 imp/s. The data indicate that the vestibular nuclei contain the requisite signals to generate horizontal eye velocity during OVAR. VO and VPS units probably contribute to the bias or velocity storage component while otolith units mainly contribute to the oscillations in eye velocity by generating gravity dependent eye position changes during OVAR. In addition to the velocity storage component of horizontal eye velocity, the vertical VO neurons also have oscillations in their discharge patterns probably related to the vertical component of eye movements generated by the velocity storage integrator.     

Asymmetric integration recorded from vestibular-only cells in response to position transients

Angular and translational accelerations excite the semicircular canals and otolith organs, respectively. While canal afferents approximately encode head angular velocity due to the biomechanical integration performed by the canals, otolith signals have been found to approximate head translational acceleration. Because central vestibular pathways require velocity and position signals for their operation, the question has been raised as to how the integration of the otolith signals is accomplished. We recorded responses from 62 vestibular-only neurons in the vestibular nucleus of two monkeys to position transients in the naso-occipital and interaural orientations and varying directions in between. Responses to the transients were directionally asymmetric; one direction elicited a response that approximated the integral of the acceleration of the stimulus. In the opposite direction, the cells simply encoded the acceleration of the motion. We present a model that suggests that a neural integrator is not needed. Instead a neuron with a long membrane time constant and an excitatory postsynaptic potential duration that increases with the firing rate of the presynaptic cell can emulate the observed behavior.     

Neural processing of gravito-inertial cues in humans. I. Influence of the semicircular canals following post-rotatory tilt

Sensory systems often provide ambiguous information. Integration of various sensory cues is required for the CNS to resolve sensory ambiguity and elicit appropriate responses. The vestibular system includes two types of sensors: the semicircular canals, which measure head rotation, and the otolith organs, which measure gravito-inertial force (GIF), the sum of gravitational force and inertial force due to linear acceleration. According to Einstein's equivalence principle, gravitational force is indistinguishable from inertial force due to linear acceleration. As a consequence, otolith measurements must be supplemented with other sensory information for the CNS to distinguish tilt from translation. The GIF resolution hypothesis states that the CNS estimates gravity and linear acceleration, so that the difference between estimates of gravity and linear acceleration matches the measured GIF. Both otolith and semicircular canal cues influence this estimation of gravity and linear acceleration. The GIF resolution hypothesis predicts that inaccurate estimates of both gravity and linear acceleration can occur due to central interactions of sensory cues. The existence of specific patterns of vestibuloocular reflexes (VOR) related to these inaccurate estimates can be used to test the GIF resolution hypothesis. To investigate this hypothesis, we measured eye movements during two different protocols. In one experiment, eight subjects were rotated at a constant velocity about an earth-vertical axis and then tilted 90 degrees in darkness to one of eight different evenly spaced final orientations, a so-called "dumping" protocol. Three speeds (200, 100, and 50 degrees /s) and two directions, clockwise (CW) and counterclockwise (CCW), of rotation were tested. In another experiment, four subjects were rotated at a constant velocity (200 degrees /s, CW and CCW) about an earth-horizontal axis and stopped in two different final orientations (nose-up and nose-down), a so-called "barbecue" protocol. The GIF resolution hypothesis predicts that post-rotatory horizontal VOR eye movements for both protocols should include an "induced" VOR component, compensatory to an interaural estimate of linear acceleration, even though no true interaural linear acceleration is present. The GIF resolution hypothesis accurately predicted VOR and induced VOR dependence on rotation direction, rotation speed, and head orientation. Alternative hypotheses stating that frequency segregation may discriminate tilt from translation or that the post-rotatory VOR time constant is dependent on head orientation with respect to the GIF direction did not predict the observed VOR for either experimental protocol.     

Compensation of the human vertical vestibulo-ocular reflex following occlusion of one vertical semicircular canal is incomplete

The vestibulo-ocular reflex (VOR) was studied in nine human subjects 2–15 months after permanent surgical occlusion of one posterior semicircular canal. The stimuli used were rapid, passive, unpredictable, low-amplitude (10–20°), high-acceleration (3000–4000°/s²) head rotations in pitch and yaw planes. The responses measured were vertical and horizontal eye rotations, and the results were compared with those from 19 normal subjects. After unilateral occlusion of the posterior semi-circular canal, the gain of the head-up pitch vertical VOR — the vertical VOR generated by excitation from only one and disfacilitation from two vertical semicircular canals — was reduced to 0.61±0.06 (normal 0.92±0.06) at a head velocity of 200°/s. In contrast the gain of the head-down pitch vertical VOR — the VOR still generated by excitation from two, but disfacilitation from only one vertical semicircular canal — was within normal limits: 0.86±0.11 (normal 0.96±0.04). The gain of the horizontal VOR in response to yaw head rotations — ipsilesion 0.81±0.06 (normal 0.88±0.05) and contralesion 0.80±0.11 (normal 0.92±0.11) — was within normal limits in both directions (group means ± two-tailed 95% confidence intervals given in each case). These results show that occlusion of just one vertical semicircular canal produces a permanent deficit of about 30% in the vertical VOR gain in response to rapid pitch head rotations in the excitatory direction of the occluded canal. This observation indicates that, in response to a stimulus in the higher dynamic range, compensation of the human VOR for the loss of excitatory input from even one vertical semicircular canal is incomplete.     

Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis

Summary Horizontal and vertical eye movements were recorded from cats in response to either a) off-vertical axis rotation (OVAR) at a range of velocities (5–72 deg/s) and a range of tilts (0–60 deg) or b) horizontal (with respect to the cat) optokinetic stimulation (10–80 deg/s), also around a range of tilted axes (0–60 deg). The responses to stopping either of these stimuli were also measured: post-rotatory nystagmus (PRN) following actual rotation, and optokinetic after nystagmus (OKAN) following optokinetic stimulation. The response found during OVAR was a nystagmus with a bias slow-phase velocity that was sinusoidally modulated. The bias was dependent on the tilt and reached 50% of its maximum velocity (maximum was 73±23% of the table velocity) at a tilt of 16 deg. The phase of modulation in horizontal eye velocity bore no consistent relation to the angular rotation. The amplitude of this modulation was roughly correlated with the bias with a slope of 0.13 (deg/s) modulation/(deg/s) bias velocity. There was also a low-velocity vertical bias with the slow-phases upwardly directed. The vertical bias was also modulated and the amplitude depended on the bias velocity (0.27 (deg/s) modulation/ (deg/s) bias velocity). When separated from the canal dependent response, the build up of the OVAR response had a time constant of 5.0±0.8 s. Following OVAR there was no decline in the time constant of PRN which remained at the value measured during earth-vertical axis rotation (EVAR) (6.3±2 s). The peak amplitude of PRN was reduced, dependent on the tilt, reaching only 20% of its EVAR value for a tilt of 20 deg. When a measurable PRN was found, it was accompanied by a slowly-emerging vertical component (time constant 5.4±2s) the effect of which was to vector the PRN accurately onto the earth horizontal. OKN measured about a tilted axis showed no differences in magnitude or direction from EVAR OKN even for tilts as large as 60 deg. OKAN following optokinetic stimulation around a tilted axis appeared normal in the horizontal plane (with respect to the animal) but was accompanied by a slowly emerging (time constant 4.1±2 s) vertical component, the effect of which was to vector the overall OKAN response onto the earth horizontal for tilts less than 20 deg. These results are compared with data from monkey and man and discussed in terms of the involvement of the velocity storage mechanism.     

Canal-otolith interaction in the fastigial nucleus of the alert monkey

To determine the contribution of the otoliths as well as the horizontal and vertical semicircular canals to the response of "vestibular only" neurons in the rostral fastigial nucleus of the alert monkey, we applied natural sinusoidal vestibular stimuli (0.6 Hz; +/-15 deg) around different axes. During the experiment the monkey sat erect in a primate chair with the head immobile. Semicircular canal responses were investigated during tilted yaw stimulation around an earth vertical axis. The tilt angle was varied by 30 deg and included the optimal plane for horizontal canal stimulation (15 deg nose down from the stereotactic plane). The otoliths and mainly the vertical canals made contributions during stimulation around an earth-fixed horizontal axis (vertical stimulation). Head orientation was also slowly altered (2-3 deg/s) over a range of 180 deg under both stimulus conditions (tilted yaw and vertical stimulation). Neuronal data for each paradigm were fitted by a least squares best-sine function. Computation of the hypothetical contributions made by all three pairs of semicircular canals and the otoliths to these responses showed that 74% of the 46 neurons investigated received an otolith input; in most instances it was combined with a canal input. Neurons most often received input from the horizontal and vertical canals as well as the otoliths. Only a minority of neurons received a purely otolith (13%), vertical canal (13%), or horizontal canal (4%) input. Conventional criteria (head position-related activity, spatiotemporal convergence, STC) failed to detect an otolith contribution in several such instances. Thus, canal-otolith convergence is the general rule at this central stage of vestibular information processing in the fastigial nucleus. The large variety of response types allows these neurons to participate in multiple tasks of vestibulospinal movement control.