Axis Of Eye Rotation Research Articles

Abnormal Nystagmus Induced by Peripheral Vestibular Disorders

Electrophysiological measurement of the eye rotation axis using stimulation of a single semicircular canal nerve showed that the eye rotated around the axis perpendicular to the plane of the stimulated semicircular canal. Therefore, the affected semicircular canal can be identified by analyzing the eye rotation axis in cases of abnormal nystagmus. When the main component of the abnormal nystagmus is horizontal, the origin of the nystagmus is the lateral semicircular canal. When the main component of the abnormal nystagmus is torsional, the origin of the nystagmus is the anterior and/or posterior semicircular canal. The eye rotation axis in cases of excitatory nystagmus is quite the same as that in cases of inhibitory nystagmus, although the direction of eye rotation is opposite between cases of excitatory and inhibitory nystagmus. Vestibular neuritis mostly involves the superior vestibular nerve. The superior vestibular nerve transmits sensory information transmitted by from the vestibular hair cells located in the anterior and lateral semicircular canals. Therefore, patients with vestibular neuritis exhibit nystagmus with both horizontal and torsional components caused by inhibition of both the anterior and lateral semicircular canals. In patients with Ménière's disease, during a vertigo attack, excitatory nystagmus of anterior and/or posterior and/or lateral semicircular canal origin can be seen. Because the involving ratio of each contributing ratios of the three semicircular canals to nystagmus can vary, the ratio of the torsional component of the nystagmus to the horizontal component also varies. While nystagmus is purely horizontal in some cases, it is purely torsional in others. In the posterior canal type of BPPV, during the Dix-Hallpike maneuver, transient torsional nystagmus with the torsional component directed toward the affected side can be seen. In the lateral canal type of BPPV (canalolithiasis), geotropic positional nystagmus can be seen when the patient is supine. In the lateral canal type of BPPV (cupulolithiasis), apogeotropic positional nystagmus can be seen when the patient is supine.

Coding of Velocity Storage in the Vestibular Nuclei.

Semicircular canal afferents sense angular acceleration and output angular velocity with a short time constant of ≈4.5 s. This output is prolonged by a central integrative network, velocity storage that lengthens the time constants of eye velocity. This mechanism utilizes canal, otolith, and visual (optokinetic) information to align the axis of eye velocity toward the spatial vertical when head orientation is off-vertical axis. Previous studies indicated that vestibular-only (VO) and vestibular-pause-saccade (VPS) neurons located in the medial and superior vestibular nucleus could code all aspects of velocity storage. A recently developed technique enabled prolonged recording while animals were rotated and received optokinetic stimulation about a spatial vertical axis while upright, side-down, prone, and supine. Firing rates of 33 VO and 8 VPS neurons were studied in alert cynomolgus monkeys. Majority VO neurons were closely correlated with the horizontal component of velocity storage in head coordinates, regardless of head orientation in space. Approximately, half of all tested neurons (46%) code horizontal component of velocity in head coordinates, while the other half (54%) changed their firing rates as the head was oriented relative to the spatial vertical, coding the horizontal component of eye velocity in spatial coordinates. Some VO neurons only coded the cross-coupled pitch or roll components that move the axis of eye rotation toward the spatial vertical. Sixty-five percent of these VO and VPS neurons were more sensitive to rotation in one direction (predominantly contralateral), providing directional orientation for the subset of VO neurons on either side of the brainstem. This indicates that the three-dimensional velocity storage integrator is composed of directional subsets of neurons that are likely to be the bases for the spatial characteristics of velocity storage. Most VPS neurons ceased firing during drowsiness, but the firing rates of VO neurons were unaffected by states of alertness and declined with the time constant of velocity storage. Thus, the VO neurons are the prime components of the mechanism of coding for velocity storage, whereas the VPS neurons are likely to provide the path from the vestibular to the oculomotor system for the VO neurons.

Directional Plasticity Rapidly Improves 3D Vestibulo-Ocular Reflex Alignment in Monkeys Using a Multichannel Vestibular Prosthesis

Bilateral loss of vestibular sensation can be disabling. We have shown that a multichannel vestibular prosthesis (MVP) can partly restore vestibular sensation as evidenced by improvements in the 3-dimensional angular vestibulo-ocular reflex (3D VOR). However, a key challenge is to minimize misalignment between the axes of eye and head rotation, which is apparently caused by current spread beyond each electrode's targeted nerve branch. We recently reported that rodents wearing a MVP markedly improve 3D VOR alignment during the first week after MVP activation, probably through the same central nervous system adaptive mechanisms that mediate cross-axis adaptation over time in normal individuals wearing prisms that cause visual scene movement about an axis different than the axis of head rotation. We hypothesized that rhesus monkeys would exhibit similar improvements with continuous prosthetic stimulation over time. We created bilateral vestibular deficiency in four rhesus monkeys via intratympanic injection of gentamicin. A MVP was mounted to the cranium, and eye movements in response to whole-body passive rotation in darkness were measured repeatedly over 1 week of continuous head motion-modulated prosthetic electrical stimulation. 3D VOR responses to whole-body rotations about each semicircular canal axis were measured on days 1, 3, and 7 of chronic stimulation. Horizontal VOR gain during 1 Hz, 50 °/s peak whole-body rotations before the prosthesis was turned on was <0.1, which is profoundly below normal (0.94 ± 0.12). On stimulation day 1, VOR gain was 0.4-0.8, but the axis of observed eye movements aligned poorly with head rotation (misalignment range ∼30-40 °). Substantial improvement of axis misalignment was observed after 7 days of continuous motion-modulated prosthetic stimulation under normal diurnal lighting. Similar improvements were noted for all animals, all three axes of rotation tested, for all sinusoidal frequencies tested (0.05-5 Hz), and for high-acceleration transient rotations. VOR asymmetry changes did not reach statistical significance, although they did trend toward slight improvement over time. Prior studies had already shown that directional plasticity reduces misalignment when a subject with normal labyrinths views abnormal visual scene movement. Our results show that the converse is also true: individuals receiving misoriented vestibular sensation under normal viewing conditions rapidly adapt to restore a well-aligned 3D VOR. Considering the similarity of VOR physiology across primate species, similar effects are likely to occur in humans using a MVP to treat bilateral vestibular deficiency.

Three Dimensional Vestibular Ocular Reflex Testing Using a Six Degrees of Freedom Motion Platform

The vestibular organ is a sensor that measures angular and linear accelerations with six degrees of freedom (6DF). Complete or partial defects in the vestibular organ results in mild to severe equilibrium problems, such as vertigo, dizziness, oscillopsia, gait unsteadiness nausea and/or vomiting. A good and frequently used measure to quantify gaze stabilization is the gain, which is defined as the magnitude of compensatory eye movements with respect to imposed head movements. To test vestibular function more fully one has to realize that 3D VOR ideally generates compensatory ocular rotations not only with a magnitude (gain) equal and opposite to the head rotation but also about an axis that is co-linear with the head rotation axis (alignment). Abnormal vestibular function thus results in changes in gain and changes in alignment of the 3D VOR response. Here we describe a method to measure 3D VOR using whole body rotation on a 6DF motion platform. Although the method also allows testing translation VOR responses (1), we limit ourselves to a discussion of the method to measure 3D angular VOR. In addition, we restrict ourselves here to description of data collected in healthy subjects in response to angular sinusoidal and impulse stimulation. Subjects are sitting upright and receive whole-body small amplitude sinusoidal and constant acceleration impulses. Sinusoidal stimuli (f = 1 Hz, A = 4°) were delivered about the vertical axis and about axes in the horizontal plane varying between roll and pitch at increments of 22.5° in azimuth. Impulses were delivered in yaw, roll and pitch and in the vertical canal planes. Eye movements were measured using the scleral search coil technique (2). Search coil signals were sampled at a frequency of 1 kHz. The input-output ratio (gain) and misalignment (co-linearity) of the 3D VOR were calculated from the eye coil signals (3). Gain and co-linearity of 3D VOR depended on the orientation of the stimulus axis. Systematic deviations were found in particular during horizontal axis stimulation. In the light the eye rotation axis was properly aligned with the stimulus axis at orientations 0° and 90° azimuth, but gradually deviated more and more towards 45° azimuth. The systematic deviations in misalignment for intermediate axes can be explained by a low gain for torsion (X-axis or roll-axis rotation) and a high gain for vertical eye movements (Y-axis or pitch-axis rotation (see Figure 2). Because intermediate axis stimulation leads a compensatory response based on vector summation of the individual eye rotation components, the net response axis will deviate because the gain for X- and Y-axis are different. In darkness the gain of all eye rotation components had lower values. The result was that the misalignment in darkness and for impulses had different peaks and troughs than in the light: its minimum value was reached for pitch axis stimulation and its maximum for roll axis stimulation. Nine subjects participated in the experiment. All subjects gave their informed consent. The experimental procedure was approved by the Medical Ethics Committee of Erasmus University Medical Center and adhered to the Declaration of Helsinki for research involving human subjects. Six subjects served as controls. Three subjects had a unilateral vestibular impairment due to a vestibular schwannoma. The age of control subjects (six males and three females) ranged from 22 to 55 years. None of the controls had visual or vestibular complaints due to neurological, cardio vascular and ophthalmic disorders. The age of the patients with schwannoma varied between 44 and 64 years (two males and one female). All schwannoma subjects were under medical surveillance and/or had received treatment by a multidisciplinary team consisting of an othorhinolaryngologist and a neurosurgeon of the Erasmus University Medical Center. Tested patients all had a right side vestibular schwannoma and underwent a wait and watch policy (Table 1; subjects N1-N3) after being diagnosed with vestibular schwannoma. Their tumors had been stabile for over 8-10 years on magnetic resonance imaging.

Three Dimensional Vestibular Ocular Reflex Testing Using a Six Degrees of Freedom Motion Platform

The vestibular organ is a sensor that measures angular and linear accelerations with six degrees of freedom (6DF). Complete or partial defects in the vestibular organ results in mild to severe equilibrium problems, such as vertigo, dizziness, oscillopsia, gait unsteadiness nausea and/or vomiting. A good and frequently used measure to quantify gaze stabilization is the gain, which is defined as the magnitude of compensatory eye movements with respect to imposed head movements. To test vestibular function more fully one has to realize that 3D VOR ideally generates compensatory ocular rotations not only with a magnitude (gain) equal and opposite to the head rotation but also about an axis that is co-linear with the head rotation axis (alignment). Abnormal vestibular function thus results in changes in gain and changes in alignment of the 3D VOR response. Here we describe a method to measure 3D VOR using whole body rotation on a 6DF motion platform. Although the method also allows testing translation VOR responses 1, we limit ourselves to a discussion of the method to measure 3D angular VOR. In addition, we restrict ourselves here to description of data collected in healthy subjects in response to angular sinusoidal and impulse stimulation. Subjects are sitting upright and receive whole-body small amplitude sinusoidal and constant acceleration impulses. Sinusoidal stimuli (f = 1 Hz, A = 4°) were delivered about the vertical axis and about axes in the horizontal plane varying between roll and pitch at increments of 22.5° in azimuth. Impulses were delivered in yaw, roll and pitch and in the vertical canal planes. Eye movements were measured using the scleral search coil technique 2. Search coil signals were sampled at a frequency of 1 kHz. The input-output ratio (gain) and misalignment (co-linearity) of the 3D VOR were calculated from the eye coil signals 3. Gain and co-linearity of 3D VOR depended on the orientation of the stimulus axis. Systematic deviations were found in particular during horizontal axis stimulation. In the light the eye rotation axis was properly aligned with the stimulus axis at orientations 0° and 90° azimuth, but gradually deviated more and more towards 45° azimuth. The systematic deviations in misalignment for intermediate axes can be explained by a low gain for torsion (X-axis or roll-axis rotation) and a high gain for vertical eye movements (Y-axis or pitch-axis rotation (see Figure 2). Because intermediate axis stimulation leads a compensatory response based on vector summation of the individual eye rotation components, the net response axis will deviate because the gain for X- and Y-axis are different. In darkness the gain of all eye rotation components had lower values. The result was that the misalignment in darkness and for impulses had different peaks and troughs than in the light: its minimum value was reached for pitch axis stimulation and its maximum for roll axis stimulation. Case Presentation Nine subjects participated in the experiment. All subjects gave their informed consent. The experimental procedure was approved by the Medical Ethics Committee of Erasmus University Medical Center and adhered to the Declaration of Helsinki for research involving human subjects. Six subjects served as controls. Three subjects had a unilateral vestibular impairment due to a vestibular schwannoma. The age of control subjects (six males and three females) ranged from 22 to 55 years. None of the controls had visual or vestibular complaints due to neurological, cardio vascular and ophthalmic disorders. The age of the patients with schwannoma varied between 44 and 64 years (two males and one female). All schwannoma subjects were under medical surveillance and/or had received treatment by a multidisciplinary team consisting of an othorhinolaryngologist and a neurosurgeon of the Erasmus University Medical Center. Tested patients all had a right side vestibular schwannoma and underwent a wait and watch policy (Table 1; subjects N1-N3) after being diagnosed with vestibular schwannoma. Their tumors had been stabile for over 8-10 years on magnetic resonance imaging.

Tonic eye movements induced by bilateral and unilateral galvanic vestibular stimulation (GVS) in guinea pigs

Galvanic vestibular stimulation (GVS) stimulates primary vestibular afferents innervating the semicircular canals (SCCs) and otoliths found in the inner ear of humans and other mammals, including guinea pigs. To determine which pathways contribute to eye movements generated by this artificial vestibular stimulation in guinea pigs, low current intensities of GVS were passed either bilaterally between the tensor-tympani muscles of the two ears (up to 30 μA) or unilaterally between one tensor-tympani electrode and an indifferent on the back of the neck (up to 60 μA). Both forms of GVS were found to selectively generate tonic eye movements without nystagmus, characteristic of the otolith-ocular reflex; the axis of eye rotation did not align with any semicircular canal plane, but was oriented close to the expected axis of eye rotation that would occur in response to the net stimulation of otolith afferents. The induced eye rotation was predominantly vertical with a smaller horizontal deviation and very little torsion. Consistent with the results of previous human studies, the tonic eye movements were found to exhibit bilateral gain enhancement, whereby bilateral GVS generated twice the amplitude of eye rotation as unilateral anodal or cathodal stimulation alone. Eye movement responses to unilateral GVS were symmetrical in amplitude during equivalent intensities of anodal and cathodal stimulation, consistent with the known responses of more regularly and intermediately discharging primary vestibular afferents to GVS. These results together suggest that more regularly discharging otolith-ocular projections may mediate the tonic changes in eye position induced during maintained, low-intensity GVS in guinea pigs.

The Under-compensatory Roll aVOR Does Not Affect Dynamic Visual Acuity

Rotations of the head evoke compensatory reflexive eye rotations in the orbit to stabilize images onto the fovea. In normal humans, the angular vestibulo-ocular reflex (aVOR) gain (eye/head velocity) changes depending on the head rotation plane. For pitch and yaw head rotations, the gain is near unity, but during roll head rotations, the aVOR gain is ∼ 0.7. The purpose of this study was to determine whether this physiological discrepancy affects dynamic visual acuity (DVA)--a functional measure of the aVOR that requires subjects to identify letters of varying acuities during head rotation. We used the scleral search coil technique to measure eye and head velocity during passive DVA testing in yaw, roll, and pitch head impulses in healthy controls and patients with unilateral vestibular hypofunction (UVH). For control subjects, the mean aVOR gain during roll impulses was significantly lower than the mean aVOR gain during yaw and pitch impulses; however, there was no difference in DVA between yaw, roll, or pitch. For subjects with UVH, only aVOR gain during head rotations toward the affected side (yaw) were asymmetric (ipsilesional, 0.32 ± 0.17, vs. contralesional, 0.95 ± 0.05), with no asymmetry during roll or pitch. Similarly, there was a large asymmetry for DVA only during yaw head rotations, with no asymmetry in roll or pitch. Interestingly, DVA during roll toward the affected ear was better than DVA during yaw toward the affected ear--even though the ipsilesional roll aVOR gain was 60 % lower. During roll, the axis of eye rotation remains nearly perpendicular to the fovea, resulting in minimal displacement between the fovea and fixation target image projected onto the back of the eye. For subjects with UVH, the DVA score during passive horizontal impulses is a better indicator of poor gaze stability than during passive roll or pitch.

Planer orientation of the bilateral semicircular canals in dizzy patients

Recent development of 3-dimensional analysis of eye movement enabled to detect the eye rotation axis, which is used to determine the responsible semicircular canal(s) in dizzy patients. Therefore, the knowledge of anatomical orientation of bilateral semicircular canals is essential, as all 6 canals influence the eye movements. Employing the new head coordinate system suitable for MR imaging, we calculated the angles of semicircular canal planes of both ears in 11 dizzy patients who had normal caloric response in both ears. The angles between adjacent canal pairs were nearly perpendicular in both ears. The angle between the posterior canal planes and head sagittal plane was 51° and significantly larger the angle between the anterior canal planes and head sagittal plane, which was 35°. The angle between the horizontal canal plane and head sagittal plane was almost orthogonal. Pairs of contralateral synergistic canal planes were not parallel, forming 10° between right and left horizontal canal planes, 17° between right anterior and left posterior canal planes and 19° between the right posterior and left anterior canal planes. Our measurement of the angles of adjacent canal pairs and the angle between each semicircular canal and head sagittal plane coincided with those of previous reports obtained from CT images and skull specimens. However, the angles between contralateral synergistic canal planes were more parallel than those of previous reports.

Quick phases control ocular torsion during smooth pursuit

One of the open questions in oculomotor control of visually guided eye movements is whether it is possible to smoothly track a target along a curvilinear path across the visual field without changing the torsional stance of the eye. We show in an experimental study of three-dimensional eye movements in subhuman primates (Macaca mulatta) that although the pursuit system is able to smoothly change the orbital orientation of the eye's rotation axis, the smooth ocular motion was interrupted every few hundred milliseconds by a small quick phase with amplitude <1.5° while the animal tracked a target along a circle or ellipse. Specifically, during circular pursuit of targets moving at different angular eccentricities (5°, 10°, and 15°) relative to straight ahead at spatial frequencies of 0.067 and 0.1 Hz, the torsional amplitude of the intervening quick phases was typically around 1° or smaller and changed direction for clockwise vs. counterclockwise tracking. Reverse computations of the eye rotation based on the recorded angular eye velocity showed that the quick phases facilitate the overall control of ocular orientation in the roll plane, thereby minimizing torsional disturbances of the visual field. On the basis of a detailed kinematic analysis, we suggest that quick phases during curvilinear smooth tracking serve to minimize deviations from Donders' law, which are inevitable due to the spherical configuration space of smooth eye movements.

Three-Dimensional Vibration-Induced Vestibulo-ocular Reflex Identifies Vertical Semicircular Canal Dehiscence

Vertical semicircular canal dehiscence (VSCD) due to superior canal dehiscence (SCD) or posterior canal dehiscence (PCD) of the temporal bone causes vestibular and cochlear hypersensitivity to sound. This study aimed to characterize the vibration-induced vestibulo-ocular reflex (ViVOR) in VSCD. ViVORs in one PCD and 17 SCD patients, confirmed by CT imaging reformatted in semicircular canal planes, were measured with dual-search coils as binocular three-dimensional eye rotations induced by skull vibrations from a bone oscillator (B71-10 ohms) at 7 ms, 500 Hz, 135-dB peak-force level (re: 1 μN). The ViVOR eye rotation axes were computed by vector analysis and referenced to known semicircular canal planes. Onset latency of the ViVOR was 11 ms. ViVOR from VSCD was up to nine times greater than normal. The ViVOR's torsional rotation was always contraversive-torsional (the eye's upper pole rotated away from the stimulated ear), i.e. its direction was clockwise from a left and counterclockwise from a right VSCD, thereby lateralizing the side of the VSCD. The ViVORs vertical component distinguishes PCD from SCD, being downwards in PCD and upwards in SCD. In unilateral VSCD, the ViVOR eye rotation axis aligned closest to the dehiscent vertical semicircular canal axis from either ipsilateral or contralateral mastoid vibrations. However, in bilateral VSCDs, the ViVOR eye rotation axis lateralized to the ipsilateral dehiscent vertical semicircular canal axis. ViVOR was evoked in ossicular chain dysfunction, even when air-conducted click vestibulo-ocular reflex (VOR) was absent or markedly reduced. Hence, ViVOR could be a useful measurement to identify unilateral or bilateral VSCD even in the presence of ossicular chain dysfunction.

Ataxia telangiectasia: a “disease model” to understand the cerebellar control of vestibular reflexes

Experimental animal models have suggested that the modulation of the amplitude and direction of vestibular reflexes are important functions of the vestibulocerebellum and contribute to the control of gaze and balance. These critical vestibular functions have been infrequently quantified in human cerebellar disease. In 13 subjects with ataxia telangiectasia (A-T), a disease associated with profound cerebellar cortical degeneration, we found abnormalities of several key vestibular reflexes. The vestibuloocular reflex (VOR) was measured by eye movement responses to changes in head rotation. The vestibulocollic reflex (VCR) was assessed with cervical vestibular-evoked myogenic potentials (cVEMPs), in which auditory clicks led to electromyographic activity of the sternocleidomastoid muscle. The VOR gain (eye velocity/head velocity) was increased in all subjects with A-T. An increase of the VCR, paralleling that of the VOR, was indirectly suggested by an increase in cVEMP amplitude. In A-T subjects, alignment of the axis of eye rotation was not with that of head rotation. Subjects with A-T thus manifested VOR cross-coupling, abnormal eye movements directed along axes orthogonal to that of head rotation. Degeneration of the Purkinje neurons in the vestibulocerebellum probably underlie these deficits. This study offers insights into how the vestibulocerebellum functions in healthy humans. It may also be of value to the design of treatment trials as a surrogate biomarker of cerebellar function that does not require controlling for motivation or occult changes in motor strategy on the part of experimental subjects.

Virtual labyrinth model of vestibular afferent excitation via implanted electrodes: validation and application to design of a multichannel vestibular prosthesis

To facilitate design of a multichannel vestibular prosthesis that can restore sensation to individuals with bilateral loss of vestibular hair cell function, we created a virtual labyrinth model. Model geometry was generated through 3-dimensional (3D) reconstruction of microMRI and microCT scans of normal chinchillas (Chinchilla lanigera) acquired with 30-48 μm and 12 μm voxels, respectively. Virtual electrodes were positioned based on anatomic landmarks, and the extracellular potential field during a current pulse was computed using finite element methods. Potential fields then served as inputs to stochastic, nonlinear dynamic models for each of 2,415 vestibular afferent axons with spiking dynamics based on a modified Smith and Goldberg model incorporating parameters that varied with fiber location in the neuroepithelium. Action potential propagation was implemented by a well validated model of myelinated fibers. We tested the model by comparing predicted and actual 3D angular vestibulo-ocular reflex (aVOR) axes of eye rotation elicited by prosthetic stimuli. Actual responses were measured using 3D video-oculography. The model was individualized for each animal by placing virtual electrodes based on microCT localization of real electrodes. 3D eye rotation axes were predicted from the relative proportion of model axons excited within each of the three ampullary nerves. Multiple features observed empirically were observed as emergent properties of the model, including effects of active and return electrode position, stimulus amplitude and pulse waveform shape on target fiber recruitment and stimulation selectivity. The modeling procedure is partially automated and can be readily adapted to other species, including humans.

Peaks and Troughs of Three-Dimensional Vestibulo-ocular Reflex in Humans

The three-dimensional vestibulo-ocular reflex (3D VOR) ideally generates compensatory ocular rotations not only with a magnitude equal and opposite to the head rotation but also about an axis that is collinear with the head rotation axis. Vestibulo-ocular responses only partially fulfill this ideal behavior. Because animal studies have shown that vestibular stimulation about particular axes may lead to suboptimal compensatory responses, we investigated in healthy subjects the peaks and troughs in 3D VOR stabilization in terms of gain and alignment of the 3D vestibulo-ocular response. Six healthy upright sitting subjects underwent whole body small amplitude sinusoidal and constant acceleration transients delivered by a six-degree-of-freedom motion platform. Subjects were oscillated about the vertical axis and about axes in the horizontal plane varying between roll and pitch at increments of 22.5° in azimuth. Transients were delivered in yaw, roll, and pitch and in the vertical canal planes. Eye movements were recorded in with 3D search coils. Eye coil signals were converted to rotation vectors, from which we calculated gain and misalignment. During horizontal axis stimulation, systematic deviations were found. In the light, misalignment of the 3D VOR had a maximum misalignment at about 45°. These deviations in misalignment can be explained by vector summation of the eye rotation components with a low gain for torsion and high gain for vertical. In the dark and in response to transients, gain of all components had lower values. Misalignment in darkness and for transients had different peaks and troughs than in the light: its minimum was during pitch axis stimulation and its maximum during roll axis stimulation. We show that the relatively large misalignment for roll in darkness is due to a horizontal eye movement component that is only present in darkness. In combination with the relatively low torsion gain, this horizontal component has a relative large effect on the alignment of the eye rotation axis with respect to the head rotation axis.Electronic supplementary materialThe online version of this article (doi:10.1007/s10162-010-0210-y) contains supplementary material, which is available to authorized users.

A Multichannel Semicircular Canal Neural Prosthesis Using Electrical Stimulation to Restore 3-D Vestibular Sensation

Bilateral loss of vestibular sensation can be disabling. Those afflicted suffer illusory visual field movement during head movements, chronic disequilibrium and postural instability due to failure of vestibulo-ocular and vestibulo-spinal reflexes. A neural prosthesis that emulates the normal transduction of head rotation by semicircular canals could significantly improve quality of life for these patients. Like the three semicircular canals in a normal ear, such a device should at least transduce three orthogonal (or linearly separable) components of head rotation into activity on corresponding ampullary branches of the vestibular nerve. We describe the design, circuit performance and in vivo application of a head-mounted, semi-implantable multichannel vestibular prosthesis that encodes head movement in three dimensions as pulse-frequency-modulated electrical stimulation of three or more ampullary nerves. In chinchillas treated with intratympanic gentamicin to ablate vestibular sensation bilaterally, prosthetic stimuli elicited a partly compensatory angular vestibulo-ocular reflex in multiple planes. Minimizing misalignment between the axis of eye and head rotation, apparently caused by current spread beyond each electrode's targeted nerve branch, emerged as a key challenge. Increasing stimulation selectivity via improvements in electrode design, surgical technique and stimulus protocol will likely be required to restore AVOR function over the full range of normal behavior.

Kinematics of the Rotational Vestibuloocular Reflex: Role of the Cerebellum

We studied the effect of cerebellar lesions on the 3-D control of the rotational vestibuloocular reflex (RVOR) to abrupt yaw-axis head rotation. Using search coils, three-dimensional (3-D) eye movements were recorded from nine patients with cerebellar disease and seven normal subjects during brief chair rotations (200 degrees /s(2) to 40 degrees /s) and manual head impulses. We determined the amount of eye-position dependent torsion during yaw-axis rotation by calculating the torsional-horizontal eye-velocity axis for each of three vertical eye positions (0 degrees , +/-15 degrees ) and performing a linear regression to determine the relationship of the 3-D velocity axis to vertical eye position. The slope of this regression is the tilt angle slope. Overall, cerebellar patients showed a clear increase in the tilt angle slope for both chair rotations and head impulses. For chair rotations, the effect was not seen at the onset of head rotation when both patients and normal subjects had nearly head-fixed responses (no eye-position-dependent torsion). Over time, however, both groups showed an increasing tilt-angle slope but to a much greater degree in cerebellar patients. Two important conclusions emerge from these findings: the axis of eye rotation at the onset of head rotation is set to a value close to head-fixed (i.e., optimal for gaze stabilization during head rotation), independent of the cerebellum and once the head rotation is in progress, the cerebellum plays a crucial role in keeping the axis of eye rotation about halfway between head-fixed and that required for Listing's Law to be obeyed.

Click-evoked vestibulo-ocular reflex

An enlarged, low-threshold click-evoked vestibulo-ocular reflex (VOR) can be averaged from the vertical electro-oculogram in a superior canal dehiscence (SCD), a temporal bone defect between the superior semicircular canal and middle cranial fossa. To determine the origin and quantitative stimulus-response properties of the click-evoked VOR. Three-dimensional, binocular eye movements evoked by air-conducted 100-microsecond clicks (110 dB normal hearing level, 145 dB sound pressure level, 2 Hz) were measured with dual-search coils in 11 healthy subjects and 19 patients with SCD confirmed by CT imaging. Thresholds were established by decrementing loudness from 110 dB to 70 dB in 10-dB steps. Eye rotation axis of click-evoked VOR computed by vector analysis was referenced to known semicircular canal planes. Response characteristics were investigated with regard to enhancement using trains of three to seven clicks with 1-millisecond interclick intervals, visual fixation, head orientation, click polarity, and stimulation frequency (2 to 15 Hz). In subjects and SCD patients, click-evoked VOR comprised upward, contraversive-torsional eye rotations with onset latency of approximately 9 milliseconds. Its eye rotation axis aligned with the superior canal axis, suggesting activation of superior canal receptors. In subjects, the amplitude was less than 0.01 degrees, and the magnitude was less than 3 degrees/second; in SCD, the amplitude was up to 60 times larger at 0.66 degrees, and its magnitude was between 5 and 92 degrees/second, with a threshold 10 to 40 dB below normal (110 dB). The click-evoked VOR magnitude was enhanced approximately 2.5 times with trains of five clicks but was unaffected by head orientation, visual fixation, click polarity, and stimulation frequency up to 10 Hz; it was also present on the surface electro-oculogram. In superior canal dehiscence, clicks evoked a high-magnitude, low-threshold, 9-millisecond-latency vestibulo-ocular reflex that aligns with the superior canal, suggesting superior canal receptor hypersensitivity to sound.

Axis of Eye Rotation Changes with Head-Pitch Orientation during Head Impulses about Earth-Vertical

The goal of this study was to assess how the axis of head rotation, Listing's law, and eye position influence the axis of eye rotation during brief, rapid head rotations. We specifically asked how the axis of eye rotation during the initial angular vestibuloocular reflex (VOR) changed when the pitch orientation of the head relative to Earth-vertical was varied, but the initial position of the eye in the orbit and the orientation of Listing's plane with respect to the head were fixed. We measured three-dimensional eye and head rotation axes in eight normal humans using the search coil technique during head-and-trunk (whole-body) and head-on-trunk (head-only) "impulses" about an Earth-vertical axis. The head was initially oriented at one of five pitch angles (30 degrees nose down, 15 degrees nose down, 0 degrees, 15 degrees nose up, 30 degrees nose up). The fixation target was always aligned with the nasooccipital axis. Whole-body impulses were passive, unpredictable, manual, rotations with peak-amplitude of approximately 20 degrees , peak-velocity of approximately 80 degrees /s, and peak-acceleration of approximately 1000 degrees /s2. Head-only impulses were also passive, unpredictable, manual, rotations with peak-amplitude of approximately 20 degrees , peak-velocity of approximately 150 degrees /s, and peak-acceleration of approximately 3000 degrees /s2. During whole-body impulses, the axis of eye rotation tilted in the same direction, and by an amount proportional (0.51 +/- 0.09), to the starting pitch head orientation (P < 0.05). This proportionality constant decreased slightly to 0.39 +/- 0.08 (P < 0.05) during head-only impulses. Using the head-only impulse data, with the head pitched up, we showed that only 50% of the tilt in the axis of eye rotation could be predicted from vectorial summation of the gains (eye velocity/head velocity) obtained for rotations about the pure yaw and roll head axes. Thus, even when the orientation of Listing's plane and eye position in the orbit are fixed, the axis of eye rotation during the VOR reflects a compromise between the requirements of Listing's law and a perfectly compensatory VOR.

The effect of binocular eye position and head rotation plane on the human torsional vestibuloocular reflex

We examined how the gain of the torsional vestibulo-ocular reflex (VOR) (defined as the instantaneous eye velocity divided by inverted head velocity) in normal humans is affected by eye position, target distance, and the plane of head rotation. In six normal subjects we measured three-dimensional (3D) eye and head rotation axes using scleral search coils, and 6D head position using a magnetic angular and linear position measurement device, during low-amplitude (∼20°), high-velocity (∼200°/s), high-acceleration (∼4000°/s 2) rapid head rotations or ‘impulses.’ Head impulses were imposed manually and delivered in five planes: yaw (horizontal canal plane), pitch, roll, left anterior-right posterior canal plane (LARP), and right anterior-left posterior canal plane (RALP). Subjects were instructed to fix on one of six targets at eye level. Targets were either straight-ahead, 20° left or 20° right from midline, at distance 15 or 124 cm from the subject. Two subjects also looked at more eccentric targets, 30° left or 30° right from midline. We found that the vertical and horizontal VOR gains increased with the proximity of the target to the subject. Previous studies suggest that the torsional VOR gain should decrease with target proximity. We found, however, that the torsional VOR gain did not change for all planes of head rotation and for both target distances. We also found a dynamic misalignment of the vertical positions of the eyes during the torsional VOR, which was greatest during near viewing with symmetric convergence. This dynamic vertical skew during the torsional VOR arises, in part, because when the eyes are converged, the optical axes are not parallel to the naso-occipital axes around which the eyes are rotating. In five of six subjects, the average skew ranged 0.9°–2.9° and was reduced to <0.4° by a ‘torsional’ quick-phase (around the naso-occipital axis) occurring <110 ms after the onset of the impulse. We propose that the torsional quick-phase mechanism during the torsional VOR could serve at least three functions: (1) resetting the retinal meridians closer to their usual orientation in the head, (2) correcting for the ‘skew’ deviation created by misalignment between the axes around which the eyes are rotating and the line of sight, and (3) taking the eyes back toward Listing’s plane.

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 degrees /s(2) reaching a velocity of 150 degrees /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 degrees /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 > or =4 Hz. For rotational frequencies > or =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.

Phakometric measurement of ocular surface radii of curvature, axial separations and alignment in relaxed and accommodated human eyes.

Measurements (autokeratometry, A-scan ultrasonography and video ophthalmophakometry) of ocular surface radii, axial separations and alignment were made in the horizontal meridian of nine emmetropes (aged 20-38 years) with relaxed (cycloplegia) and active accommodation (mean +/- 95% confidence interval: 3.7 +/- 1.1 D). The anterior chamber depth (-1.5 +/- 0.3 D) and both crystalline lens surfaces (front 3.1 +/- 0.8 D; rear 2.1 +/- 0.6 D) contributed to dioptric vergence changes that accompany accommodation. Accommodation did not alter ocular surface alignment. Ocular misalignment in relaxed eyes is mainly because of eye rotation (5.7 +/- 1.6 degrees temporally) with small amounts of lens tilt (0.2 +/- 0.8 degrees temporally) and decentration (0.1 +/- 0.1 mm nasally) but these results must be viewed with caution as we did not account for corneal asymmetry. Comparison of calculated and empirically derived coefficients (upon which ocular surface alignment calculations depend) revealed that negligible inherent errors arose from neglect of ocular surface asphericity, lens gradient refractive index properties, surface astigmatism, effects of pupil size and centration, assumed eye rotation axis position and use of linear equations for analysing Purkinje image shifts.