A new device to quantify ocular counterroll using retinal afterimages.

BACKGROUND: The integrity of vertical semicircular canal and otolith function remains difficult to assess in the clinical setting, partly due to difficulties in recording ocular counterroll. Here, we quantify static ocular counterroll from head tilt using a new head-mounted device. METHODS: The device consists of an LED positioned 42 cm in front of one eye and a striated lens which produces a streak of light on the retina. The LED is illuminated at full intensity (80 cd) to generate a retinal afterimage. Subsequently, in darkness, the subject's head is tilted in the roll plane. Finally, the LED is illuminated dimly (0.2 cd) and the subject rotates the striated lens to superimpose the dim light streak onto the afterimage. An angular scale indicates the angle through which the lens is rotated, giving a measure of the ocular counterroll. To validate the device, we recorded binocular counterroll simultaneously with 3D computerised video-oculography of the other eye in 16 normal subjects; 2 patients with acquired bilateral loss of vestibular function were also tested. RESULTS: In the normal subjects, there was no significant difference between the two techniques (p=0.24) when recording ocular counterroll and the correlation between the two techniques was R2=0.78. The 2 avestibular patients essentially showed no ocular counterroll with both techniques. CONCLUSIONS: We have devised a non-invasive, quick and reliable test of ocular counterroll. The lack of response in the 2 avestibular patients indicates that this device is clinically applicable to assess otolith function.

Visual dependence and BPPV.

The increased visual dependence noted in some vestibular patients may be secondary to their vertigo. We examine whether a single, brief vertigo attack, such as in benign paroxysmal positional vertigo (BPPV), modifies visual dependency. Visual dependency was measured before and after the Hallpike manoeuvre with (a) the Rod and Frame and the Rod and Disc techniques whilst seated and (b) the postural sway induced by visual roll-motion stimulation. Three subject groups were studied: 20 patients with BPPV (history and positive Hallpike manoeuvre; PosH group), 20 control patients (history of BPPV but negative Hallpike manoeuvre; NegH group) and 20 normal controls. Our findings show that while both patient groups showed enhanced visual dependency, the PosH and the normal control group decreased visual dependency on repetition of the visual tasks after the Hallpike manoeuvre. NegH patients differed from PosH patients in that their high visual dependency did not diminish on repetition of the visual stimuli; they scored higher on the situational characteristic questionnaire ('visual vertigo' symptoms) and showed higher incidence of migraine. We conclude that long term vestibular symptoms increase visual dependence but a single BPPV attack does not increase it further. Repetitive visual motion stimulation induces adaptation in visual dependence in peripheral vestibular disorders such as BPPV. A positional form of vestibular migraine may underlie the symptoms of some patients with a history of BPPV but negative Hallpike manoeuvre. The finding that they have non adaptable increased visual dependency may explain visuo-vestibular symptoms in this group and, perhaps more widely, in patients with migraine.

Head accelerations during particle repositioning manoeuvres.

Benign paroxysmal positional vertigo (BPPV) due to canalithiasis can be treated with particle repositioning manoeuvres, which aim to evacuate trapped particles from the semicircular canals (SCC). The movement of particles within the SCC is affected by gravity as well as by the accelerations of the head during the manoeuvres. Moreover, as experienced by the particles, gravity is indistinguishable from an upward acceleration of the SCC in free space. We used a set of three orthogonal linear accelerometers to measure the net three-dimensional linear acceleration vector acting on the head during the Hallpike manoeuvre and Epley and Semont particle repositioning manoeuvres (which are used to treat posterior canal BPPV). The projection of the net acceleration vector onto the SCC planes showed that both the Epley and Semont manoeuvres approximated to stepwise, 360 degrees , backward rotations in the plane of the targeted posterior canal. Angular velocity measurements however showed that the rotational component during the central stages of these two manoeuvres is opposite in direction. A simple model of head rotations during particle repositioning manoeuvres was created which showed good agreement to the linear acceleration measurements. Analysis of modelled and measured data identified that speed of movement during the Semont manoeuvre should be critical to its clinical success.

Influence of pitch tilts on the perception of gravity-referenced eye level in labyrinthine defective subjects.

We investigate the role of vestibular information in judging the gravity-referenced eye level (i.e., earth-referenced horizon or GREL) during sagittal body tilt whilst seated. Ten bilateral labyrinthine-defective subjects (LDS) and 10 age-matched controls set a luminous dot to their perception of GREL in darkness, with and without arm pointing. Although judgements were linearly influenced by the magnitude of whole-body tilt, results showed no significant difference between LDS and age-matched controls in the subjective GREL accuracy or in the intra-subject variability of judgement. However, LDS performance without arm pointing was related to the degree of vestibular compensation inferred from another postural study performed with the same patients. LDS did not utilize upper limb input during arm pointing movements as a source of graviceptive information to compensate for the vestibular loss. The data suggest that vestibular cues are not of prime importance in GREL estimates in static conditions. The absence of difference between controls and LDS GREL performance, and the correlation between the postural task and GREL accuracy, indicate that somatosensory input may convey as much graviceptive information required for GREL judgements as the vestibular system.

Influence of whole-body pitch tilt and kinesthetic cues on the perceived gravity-referenced eye level.

We investigated the effects of whole body tilt and lifting the arm against gravity on perceptual estimates of the Gravity-Referenced Eye Level (GREL), which corresponds to the subjective earth-referenced horizon. The results showed that the perceived GREL was influenced by body tilt, that is, lowered with forward tilt and elevated with backward tilt of the body. GREL estimates obtained by arm movements without vision were more biased by whole-body tilt than purely visual estimates. Strikingly, visual GREL estimates became more dependent on whole-body tilt when the indication of level was obtained by arm lifting. These findings indicate that active motor involvement and/or the addition of kinesthetic information increases the body tilt-induced bias when making GREL judgements. The introduction of motor/kinaesthetic cues may induce a switch from a semi-geocentric to a more egocentric frame of reference. This result challenges the assumption that combining non-conflicting multiple sensory inputs and/or using intermodal information provided during action should improve perceptual performance.

Vestibular perception in patients with acquired ophthalmoplegia.

Using a perceptual technique it is shown that patients with chronic external ophthalmoplegia have shortened vestibular responses. It is postulated that this is secondary to the retinal image slip experienced by these patients during head movements and a useful compensatory mechanism to suppress motion-induced sickness and spatial disorientation.

Paroxysmal alternating skew deviation and nystagmus after partial destruction of the uvula.

A patient with suspected brain stem glioma involving the area of the left vestibular nuclei and cerebellar peduncle, developed paroxysmal alternating skew deviation and direction changing nystagmus after biopsy of the inferior cerebellar vermis resulting in destruction of the uvula. Between attacks she had right over left skew deviation with asymptomatic right beating horizontal nystagmus. Slow phases of the resting nystagmus showed increasing velocity, similar to congenital nystagmus. At intervals of 40-50 seconds, paroxysmal reversal of her skew deviation occurred, accompanied by violent left beating horizontal torsional nystagmus lasting 10-12 seconds and causing severe oscillopsia. It is proposed that this complex paroxysmal eye movement disorder results from (1) a lesion in the left vestibular nuclei causing right over left skew and right beating resting nystagmus and (2) a disruption of cerebellar inhibition of vestibular nuclei, causing alternating activity in the vestibular system with intermittent reversal of the skew deviation and paroxysmal nystagmus towards the side of the lesion.

Horizontal ocular vergence and the three-dimensional response to whole-body roll motion.

We evaluated the human binocular response to roll motion in the dark and during visual fixation with horizontal convergence. Six normal human subjects were exposed to manually driven, whole-body rotation about an earth-vertical, naso-occipital axis, under two conditions: (I) oscillation at 0.4 Hz (peak velocity 69+/-3.8 degree/s) in the dark, and whilst fixating an axial light-emitting diode at 48 cm ('near') and at 206 cm ('far'); (II) constant velocity rotation (56.5+/-3.1 degree/s) for 40 s, clockwise and counter-clockwise, in the dark, and sudden stops. Eye and head movements were monitored using scleral search coils. In head-fixed, angular velocity coordinates roll motion always evoked conjugate ocular torsion, with small conjugate horizontal and disconjugate vertical components. The resultant binocular eye responses were rotations about convergent axes. During oscillation with target fixation the convergence of the rotation axes was larger than that predicted by target geometry, producing disconjugate oscillations of vertical gaze about the target ('skewing'). Fast-phase eye movements were primarily resetting rotations about the same convergent rotation axes as the slow phases, but the small vertical velocity components had oscillatory, asymmetrical profiles. In response to velocity steps the slow-phase eye velocity decayed exponentially with time constants of 4.5+/-1.5 s for the torsional component and 5.8+/-1.9 s for the 'vertical vergence' component (right eye-left eye recordings). We conclude that in normal human subjects dynamic vertical canal stimulation with horizontal gaze convergence evokes rotation of the eyes about convergent axes and a small skewing of the eyes.

The incidence and waveform characteristics of periodic alternating nystagmus in congenital nystagmus.

PURPOSE: To investigate the incidence and waveform characteristics of periodic alternating nystagmus, (PAN) in congenital nystagmus (CN). METHODS: In a prospective study, 18 patients with CN without associated sensory defects agreed to undergo eye movement documentation using binocular infrared oculography. Two of the 18 had a diagnosis of suspected PAN before entering the study. The patients sat in a dimly lit room and viewed an LED (4 min in diameter) located in the primary position, at a distance of 100 cm. During an 8-minute recording, patients were read a story of neutral interest to hold attention at a constant level. PAN was defined as a left-beating nystagmus, a transition phase, a right-beating nystagmus, and a final transition phase; the sequence was then repeated. RESULTS: Seven of the 18 patients had PAN (median cycle: 223 seconds, range 180-307 seconds). The periodicity of the cycles for each adult patient was regular, although the phases within a cycle were often asymmetric. Six of the seven patients had an anomalous head posture (AHP), and in five the AHP was in only one direction. Except for one patient, the PAN waveforms had an increasing slow-phase velocity in at least one phase of the cycle; in the other phase they were linear. CONCLUSIONS: The occurrence of PAN in CN is not as rare as previously thought and can be missed because of the long cycles and the use of only one AHP. The AHP was dependent on, and could be predicted from, the waveforms containing the longest foveation times. Although the waveforms and foveation times may differ among the phases of the PAN cycle, the periodicity of the cycle was usually regular and therefore predictable. Identification of PAN is essential in cases in which surgical treatment is considered for correction of AHPs.

Visual and oculomotor responses induced by neck vibration in normal subjects and labyrinthine-defective patients.

Three-dimensional scleral search coil eye movement recordings were obtained in five normal subjects and four patients with absent vestibular function, during unilateral vibration of the neck in the supine position. The purpose of the experiments was to investigate any role played by eye movements in the illusion that a small fixation target, viewed in an otherwise dark room, moves when vibration is applied to the neck (propriogyral illusion). Vibration was applied to the right dorsal neck muscles in three visual conditions: total darkness, fixating a light-emitting diode (LED) in an otherwise totally dark room and LED fixation in the normally lit room. Normal subjects reported that during vibration, with LED fixation in an otherwise dark room, the target appeared to move predominantly leftwards and patients reported a predominantly downward movement. Eye movements were consistently elicited in all subjects. In normal subjects there was a slow-phase eye movement predominantly to the right, interrupted by nystagmic quick phases in the opposite direction, whereas in the patients slow phases were predominantly upward with quick phases downward. Eye movements were larger in the dark but the velocity of the initial slow-phase component (<200 ms) did not change with visual conditions. Mean latencies of the eye movements were typically 80 ms but in individual trials could be as short as 40- 60 ms. The eye movements were considerably larger in the patients (e.g. mean cumulative slow-phase displacement in the dark 12 degrees vs 2 degrees; maximum velocity ca. 5 degrees /s vs 1 degrees /s). These results indicate that the propriogyral illusion is secondary to vibration-induced eye movements, presumably mediated by the cervico-ocular reflex (COR). The difference in direction of the illusion and eye movements in the patients may be related to a predominant enhancement of the vertical COR, secondary to the prominent exposure to vertical retinal slippage experienced by these patients during daily activities such as locomotion.

Fast eye movement initiation of ocular torsion in mesodiencephalic lesions.

Three patients with episodic ocular torsion and skew deviation due to mesodiencephalic lesions were studied by using binocular three-dimensional scleral search coils. The conjugate ocular torsion (upper pole of each eye rotating toward the side of the brainstem lesion) was initiated by a torsional fast eye movement. During prolonged episodes, torsional nystagmus was also present. Cessation of the ocular torsion and skew deviation occurred by slow eye movements with exponentially decreasing velocities in 2 patients, and by multiple fast torsional movements in 1 patient. In 1 patient, the abnormal eye movements were temporally linked to dystonic movements in the limbs on the side opposite the brainstem lesion. The occurrence of skew deviation with conjugate ocular torsion in brainstem lesions has been attributed to functional asymmetry in vestibular pathways responsible for the slow-phase compensatory eye movement response to roll. In comparison, the findings in our patients show that in mesodiencephalic lesions conjugate ocular torsion with skew deviation may be generated by torsional fast eye movements, indicating activation of the burst cells of the rostral interstitial nucleus of the medial longitudinal fasciculus.

Otolith and semicircular canal contributions to the human binocular response to roll oscillation.

Three normal human subjects were oscillated about their naso-occipital axis in a supine position at 0.4 Hz and 0.1 Hz, both in darkness and in the light with a structured fixation target. The same subjects were oscillated in roll about an upright position, at the same frequencies, in darkness; and also about axes directed 20 degrees and 40 degrees to the left and to the right of the midsagittal plane, at 0.4 Hz, in darkness. Three-dimensional binocular eye movements were recorded using video-oculography. All stimuli induced a predominantly torsional nystagmus with small disconjugate head-vertical (skew) and conjugate head-horizontal components. For roll oscillation, the torsional slow phase velocity gain was higher in the light and generally increased with the stimulation frequency. In darkness, only one subject had significantly higher torsional gains in the upright compared to the supine position (12% difference), suggesting that the otolith contribution to the roll response is minimal at the frequencies tested. The slow phase velocity gain of the skew increased with fixation in two subjects. but decreased in the third subject; these changes were related to changes in eye vergence. In the upright position, with oblique axes of rotation, the head-vertical eye movements were asymmetrical, with the outermost eye executing a larger amplitude movement. The disconjugate head-vertical eye movements observed can be explained by the pattern of vertical semicircular canal stimulation and their connections to the extraocular muscles. In humans, skewing of the eyes may compensate for the eccentricity of the foveae which lie in the temporal retina and undergo vertical translations in opposite directions when the eyes tort.

Evaluating 3D semicircular canal function by perception of rotation.

OBJECTIVE: We aimed to develop a clinical test of 3D canal dysfunction by perceptual matching of motion stimuli as an alternative to vestibular ocular reflex assessment. STUDY DESIGN: The study was a comparison with age-matched controls. SETTING: The study was performed in a clinical neurophysiology laboratory. PATIENTS: Ten patients with acute unilateral vestibular nerve section and 9 patients in the chronic stage of recovery, 2 acute-stage and 2 chronic-stage patients with posterior canal plugging, and 35 healthy individuals were studied. INTERVENTIONS: Seated on a motorized rotating chair in darkness, subjects were exposed to discrete, raised cosine velocity (60 degrees/s peak) rotations, for random displacements < or = 180 degrees rightward and leftward. They responded by rotating themselves back to the starting position with a joystick control. Horizontal canals were tested with head upright, ipsilateral versus contralateral vertical canal pairs were tested with the head down, face horizontal and co-planar anterior-posterior canal pairs were tested with the head down and turned approximately 45 degrees to the left or right. MAIN OUTCOME MEASURES: These were accuracy and symmetry of responses. RESULTS: Normal responses were approximately accurate returns to start. Nine patients with acute nerve section were hypometric (undershooting start) when displaced toward the lesion but normometric to the intact side. Eight chronic-stage nerve section patients with chronic dysfunction were hypometric to the lesion for vertical canal stimuli, but one third showed normal responses for horizontal canal testing. Patients with posterior canal plugging were hypometric specifically toward the plugged canal. CONCLUSIONS: The method reliably identifies acute and chronic dysfunction of vertical canals and acute dysfunction of horizontal canals. Dysfunction of a single canal can be specified.

Motion detection deficits in infantile esotropia without nystagmus.

PURPOSE: To investigate whether adults with infantile strabismus but without latent nystagmus have abnormalities of horizontal motion detection. METHODS: Eleven adult subjects with infantile esotropia but without latent nystagmus and 15 control subjects were required to detect the onset of motion and drift direction of a sinusoidal, spatial frequency grating that moved with linearly increasing velocity. The grating was presented monocularly in paracentral vision at an eccentricity of 16.5 degrees with a field size of 18 degrees. The contrast of the grating was just above contrast threshold for visibility. RESULTS: The mean velocity threshold for detection of motion was raised significantly in the patient group compared with the control group. Nine of the 11 subjects with infantile esotropia demonstrated directional asymmetry for the detection of motion. Thresholds were elevated more often when the grating was moving nasally in the squinting eye and temporally in the nonsquinting eye, and raised thresholds were more prevalent in the squinting eye. CONCLUSIONS: The findings indicate that in infantile esotropia, the presence of motion perception deficits are not always associated with the development of latent nystagmus. The predominance of nasally directed motion deficits in the squinting eye and temporally directed motion deficits in the nonsquinting eye was unexpected and may have been caused by abnormal development of cortical motion processing.

Skew deviation following vestibular nerve surgery.

Eighteen consecutive patients undergoing vestibular nerve surgery underwent pre- and postoperative examination of ocular motility. Five patients developed a skew deviation following surgery, with the lower eye on the operated side and an incomitant pattern of deviation in all cases. Three patients experienced diplopia lasting from 1 day to 6 months. The magnitude of skew deviation was increased by head tilt away from the operated side in only 1 case. The development of skew deviation was not determined by preoperative ocular alignment or binocular function, or any particular type or pattern of vestibular disease. There was an association with large changes in ocular torsion and subjective visual vertical, which correlated with lesser degrees of canal paresis to preoperative caloric testing on the operated side. No patient developed a head tilt postoperatively. There is a gradation of responses to surgical vestibular deafferentation in humans, skew deviation only occurring in patients suffering marked changes in subjective visual vertical and ocular torsion.

Optically induced plasticity of the cervico-ocular reflex in patients with bilateral absence of vestibular function.

The horizontal cervico-ocular reflex (COR) was examined in five labyrinthine-defictive subjects (LDS), during both passive oscillations of the head on the trunk (HTexam) and of the trunk under the earth-fixed head (THexam) at 0.1-0.5 Hz, peak angular displacement +/- 30 degrees. Subjects were tested in the dark, before and immediately after adaptation to binocular magnifying (x1.9) and reducing (x0.6) lenses. During long-term adaptation, the LDS were exposed to the normal environment for 5 h while wearing lenses. Short-term adaptation experiments (15-20 min) consisted of sustained ocular following of a small LED in an otherwise dark room and in full-room illumination. This LED was either stationary in space whilst the subjects moved their head actively, or fixed on the chair and rotating with the trunk during head-fixed stimulation. In all five patients, magnifying lenses increased COR gain (peak slow-phase eye velocity/peak stimulus velocity), whereas reducing lenses reduced the gain. Under HTexam the gain changes were greater, more consistent and the phases approximately compensatory to head displacement, whereas during THexam the gain decreased and phase increased at higher frequencies. COR adaptation was observed during foveal stimulation alone, but the effects were stronger with added background illumination. Results during an imaginary target task showed that the gain can be influenced strongly by mental set. Our findings indicate a highly modifiable COR in subjects with loss of vestibular function. Both peripheral and foveal retinal information contribute to the plastic changes in COR gain. Somatosensory cues from the trunk as well as cognitive/perceptual factors may be involved in the modification of the COR, by providing information about the relevance of eye movements, and contribute to the stabilisation of gaze in space.

Visual and vestibular factors influencing vestibular "navigation".

In order to elucidate the role of the "starting point" in path integration, normal subjects underwent a self-rotational task in a motor-driven turntable rotating around an earth-vertical axis. They were passively rotated ("stimulus") and had to return to the starting point, controlling the direction and velocity of the turntable by means of a joystick ("response"). The test included conditions with an earth-fixed target (EFT) as starting point, shown before the stimulus, and conditions without EFT presentation. The subject's response always took place in total darkness. Subjects succeeded in returning to the starting point in all conditions but were more precise (i.e. had smaller variability of responses) with the EFT than in the other conditions. The larger data scatter (inaccuracy) in these latter tasks was directly related to the return peak velocity, whereas with EFT there was no relationship between amplitude and velocity of the return motion. These results suggest that the presentation of the starting point (the EFT) allows a real time integration to take place, thereby improving accuracy during self-controlled motion in the dark. Five subjects were also tested with the same rotational paradigm in total darkness throughout, but with the head in a different position during stimulus and response motions. Thus, motion detection was performed by different semicircular canals during stimulus and response. The conditions used were head upright during stimulus, hyper-extended backward during response motion, and head backward during stimulus and upright during response motion. It was found that the accuracy during these tasks did not differ from that during stimulus/response motion without change in the upright or backward head position. These data indicate that estimates of trajectory are, within limits, independent of canal plane.

Abnormalities of torsional fast phase eye movements in unilateral rostral midbrain disease.

In a patient with a unilateral rostral midbrain lesion, three-dimensional scleral search coil eye movement recordings demonstrated slowing of ipsidirectional torsional fast phase eye movements without any abnormalities of torsional slow phases. On high-resolution MRI, the brainstem lesion localized to the area of the efferent pathways from the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF). This supports the experimental finding that unilateral inactivation of the riMLF results in a loss of ipsidirectional torsional fast phase eye movements and the hypothesis that there is lateralization of function throughout the torsional fast eye movement generating system.

Skew deviation of the eyes in normal human subjects induced by semicircular canal stimulation.

Computerised video-oculography and scleral search coils were used to record the horizontal, vertical and torsional binocular eye movements of human subjects exposed to roll oscillation at 0.4 Hz about earth-horizontal and earth-vertical naso-occipital axes in darkness. The stimuli provoked a dominant torsional ('ocular counter-rolling') response with a ratio of peak slow phase eye velocity to stimulus velocity which was not significantly different for earth-horizontal (0.39, SD 0.08) or earth-vertical axis orientations (0.40, SD 0.08). For all conditions the responses also had a head-vertical component which was disconjugate ('skew deviation'). The cumulative, vertical, slow phase divergence was 5.8 degrees, SD 1.3 degrees, about upright and 4.3 degrees, SD 0.6 degrees, when supine. This is the first demonstration that dynamic roll stimuli provoke a skew deviation in normal human subjects. At the frequency tested, the skew was driven by vertical semicircular canal stimulation.

Clinical and electrophysiological findings in the Tullio phenomenon.

A 55 year old female with idiopathic Tullio phenomenon is presented. Binocular, scleral search eye coil recordings demonstrated a predominantly torsional left-beating and vertical down-beating nystagmus in response to sound intensities over 100 dB HL to the left ear, increasing in amplitude and slow phase velocity with sound intensity and removal of visual fixation. The vertical ocular movement was conjugate, i.e. without skew deviation. Neuro-imaging, all other neuro-otological features, including ipsilateral-contralateral stapedius muscle reflexes, and surgical exploration of the middle ear, were normal. Click-evoked vestibulo-collic potentials were normal from the right ear but showed low threshold (70 dB) and increased amplitude from the left. There was no evidence that the Tullio phenomenon in this patient arises from stapes footplate hypermobility. The findings suggest that some cases of the Tullio phenomenon may be due to a hyperexcitability of the normal vestibular response to sound.