Curing benign positional vertigo in a 3D flight simulator.
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Biomedical subjects
Publications and source records attributed to A M Bronstein.
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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.
We examined the question of whether the position of the eyes in the head and of the head on the trunk influence the direction of visually elicited postural reactions. Normal subjects stood on a force platform viewing a large disc, rotating in the roll plane, always maintained orthogonal to the line of sight. The disc was presented at 0 degree, 30 degrees and 90 degrees to the right or left with respect to the mid-frontal plane of the subject's body and was viewed with various combinations of horizontal eye-in-orbit and head-on-trunk deviations. It was found that the main direction of body sway was always reoriented to be parallel to the disc (e.g. viewing the disc at 30 degrees oriented sway responses at a mean angle of 33 degrees). The largest sway responses were obtained when the disc was parallel to the sagittal plane of the body and was viewed with an ipsilateral eye-neck deviation totalling 90 degrees (head-on-trunk 60 degrees+eye-in-orbit 30 degrees). When eye and head deviations cancelled each other (i.e. eye-in-orbit +30 degrees combined with head-on-trunk -30 degrees), directional effects on sway also cancelled each other out. This result demonstrates that signals of eye-in-orbit and head-on-trunk position have the capability to redirect visuo-motor commands to the appropriate postural muscles. This allows vision to regulate postural balance whatever the position of the eyes in space. We speculate that this function is mediated by eye and neck proprioceptive signals (or alternatively by efference copy) with access to gain control mechanisms in the visuo-postural system.
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.
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.
The possibility of synergistic interaction between the canal and otolith components of the horizontal vestibulo-ocular reflex (VOR) was evaluated in human subjects by subtracting the response to pure angular rotation (AVOR) from the response to combined angular and translational motion (ALVOR) and comparing this difference with the VOR to isolated linear motion (LVOR). Assessments were made with target fixation at 60 cm and in darkness. Linear stimuli were acceleration steps attaining 0.25 g in less than 80 ms. To elicit responses to combined translational and angular head movements, the subjects were seated on a Barany chair with the head displaced forwards 40 cm from the axis of rotation. The chair was accelerated at approximately 300 deg/s2 to 127 deg/s peak angular velocity, the tangential acceleration of the head being comparable with that of isolated translation. Estimates of the contribution of smooth pursuit to responses in the light were made from comparisons of isolated pursuit of similar target trajectories. In the dark the slow phase eye movements evoked by combined canal-otolith stimuli were higher in magnitude by approximately a third than the sum of those produced by translation and rotation alone. In the light, the relative target displacement during isolated linear motion was similar to the difference in relative target displacements during eccentric and centred rotation. However, the gain of the translational component of compensatory eye movement during combined translational and angular motion was approximately unity, in contrast to the gain of the response to isolated linear motion, which was approximately a half. Pursuit performance was always poorer than target following during self-motion. The LVOR responses in the light were greater than the sum of the LVOR responses in the dark with pursuit eye movements. We conclude that, in response to transient motion, there is a synergistic enhancement of the translational VOR with concurrent canal stimulation and that the enhancement of the LVOR in the light is not due solely to pursuit.
To clarify the directional sensitivity of a single utricle with respect to the transaural linear vestibulo-ocular reflex (L-VOR) we studied seven patients before and after vestibular neurectomy. Patients were seated upright in an electrically powered car running on a linear track. Transaural acceleration steps of 0.24 g were applied randomly to the left and right in the dark. The slow phase velocity of the L-VOR was measured from the average of the induced compensatory eye movements. L-VOR asymmetry was calculated as (R-L/R + L x 100) and is < 13% in normals. Before surgery, responses were mostly symmetrical. One week after surgery, however, all patients had diminished or absent responses with medial acceleration of the remaining utricle. Asymmetries averaged 65% after correction for spontaneous nystagmus. Our findings indicate that afferents for the L-VOR originate from the lateral region of the macula where hair cells with ipsilateral on-directions are located.
Three interrelated experiments on visually evoked postural responses (VEPR) are presented to investigate the effect of lack of coplanarity between retinal and body coordinates (Experiment I) and the effect of directionally conflicting information in the visual stimulus. Experiment I showed that the direction of VEPR is modified by eye-in-orbit and head-on-trunk position signals, presumably of proprioceptive origin. Experiments II and III showed that VEPR can be critically suppressed by the presence of conflict within the visual stimulus (Experiment II: a linear, tangential component of visual motion acting in the opposite direction to the main angular component of a roll-motion display; Experiment III: a non congruent "improbable" visual motion parallax linear motion stimulus). A conceptual model of the postural system is presented, incorporating a gain control unit for the visuo-postural loop with inputs from the ocular/cervical proprioceptive system and from intra- and inter-sensory conflict detectors (comparators).
Object motion perception was assessed in avestibular patients and normal controls. Two experiments were conducted, in which subjects were required to assess the motion of a visual stimulus with respect to earth. In the first experiment, we measured the velocity at which a briefly presented (200 ms) grating was perceived as earth fixed, while the subject maintained fixation on a visual target fixed relative to the body, during whole-body yaw rotation (VOR suppression). In this experimental setup, the influence of the semicircular canal signals on object motion perception was evaluated. The avestibular patients judged the grating to be stationary with respect to earth, when it was moving at the same velocity as their body, whereas for normal controls, the grating was perceived as stationary when it moved at a velocity slower than their body motion, but greater than zero. The difference between the two subject groups was significant, and showed the strong contribution of the vestibular system to object motion perception. Similarly, a measurement of the velocity at which a grating was perceived as stationary was obtained during smooth pursuit eye movements. In this experiment the contribution of the efference copy of the oculomotor signal and proprioceptive signals to object motion perception were assessed. As with the first experiment, the normal controls displayed a more veridical sense of object motion perception than the patients, although the difference was only just significant. We suggest that the difference could be an adaptive change in the patients perception of motion, which allows them to reduce the effects of oscillopsia.
Clinical and MRI investigations were carried out on 27 patients with acquired pendular nystagmus in an attempt to delineate possible sites of lesions responsible for pendular nystagmus and mechanisms underlying the frequent ocular disconjugacy of this nystagmus. The aetiologies were multiple sclerosis (n = 21), brainstem stroke (n = 3) and other neurological conditions. In at least 59% of the patients, pendular nystagmus appeared > 1 year after the first symptom of the disease. Patients MRIs were characterized by multiple areas of abnormal signal and were analysed statistically to identify areas where lesions overlapped significantly between patients. Statistically significant overlap occurred in areas containing the red nucleus, the central tegmental tract, the medial vestibular nucleus and the inferior olive. Patients with horizontal pendular nystagmus showed predominantly pontine lesions whereas patients with torsional pendular nystagmus showed predominantly medullary involvement. The nystagmus was conjugate in 15 patients and disconjugate in amplitude or direction in 12. Internuclear ophthalmoplegia or asymmetrical visual acuity occurred in similar proportions in both groups. Patients with conjugate pendular nystagmus had a higher incidence of symmetrical, "mirror image' lesions on MRI than patients with disconjugate nystagmus. The abundance of abnormal MRI signals in our sample suggests that large or multiple structural lesions may be required to elicit pendular nystagmus, predominantly in the pons but also in the midbrain and medulla. The involvement of structures projecting to the inferior olive supports the hypothesis that oscillatory properties of olivary neurons causes the rhythm of pendular nystagmus. The delay observed between the onset of the underlying disease and the pendular nystagmus supports a mechanism operating via neural deafferentation. Disconjugancies in pendular nystagmus cannot be explained on the basis of the associated internuclear ophthalmoplegias nor on the basis of asymmetrical visual acuity. The association between symmetrical MRI lesions and conjugate nystagmus suggests that asymmetrical damage to brainstem structures concerned with binocular alignment may underlie disconjugate pendular nystagmus.
The perception of body verticality (subjective postural vertical, SPV) was assessed in normal subjects and in patients with peripheral and central vestibular lesions and the data were compared with conventional neuro-otological assessments. Subjects were seated with eyes closed in a motorized gimbal which executed cycles of tilt at low constant speed (1.5 degrees s-1), both in the frontal (roll) and sagittal (pitch) planes. Subjects indicated with a joystick when they entered and left verticality, thus defining a sector of subjective uprightness in each plane. The mean angle of tilt (identifying a bias of the SPV) and the width of the sector (defining sensitivity of the SPV) were then determined. In normal subjects, the angle of the "verticality' sector was 5.9 degrees for pitch and roll. Patients with bilateral absence of vestibular function, patients with vertigo, i.e. acute unilateral lesions, benign paroxysmal positional vertigo (BPPV) and Ménière's disease, and patients with positionally modulated up-/downbeat nystagmus all had enlarged sectors (i.e. loss in sensitivity). Mean sector angle in these groups ranged from 7.8 to 11 degrees and the abnormality was present both in pitch and roll, regardless of the direction of nystagmus or body sway. Patients with chronic unilateral peripheral vestibular lesions and those with position-independent vertical nystagmus had normal sensitivities. No significant bias of the SPV was found in any patient group, not even those with acute unilateral vestibular lesions who had marked tilts of the subjective visual vertical (SVV). Complementary experiments in normal subjects tested under galvanic vestibular or roll-plane optokinetic stimulation also failed to show biases of the SPV. In contrast, a significant bias in the SPV could be induced in normal subjects by asymmetric cycles of gimbals tilt, presumably by proprioceptive adaptation. The following conclusions can be drawn. (i) The perception of body verticality whilst seated is mainly dependent on proprioceptive/contact cues but these are susceptible to tilt-mediated adaptation. (ii) Vestibular input improves the sensitivity of the SPV, even in vestibular disorders, as long as the abnormality is stable. (iii) There can be marked dissociation between vestibulo-motor (ocular and postural) phenomena and the perception of body verticality, and between the SPV and SVV. (iv) The postural sway asymmetries in patients with peripheral and central vestibular lesions, like those induced by galvanic or optokinetic stimulation in normal subjects, are not consequences of changes of the SPV.
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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.
We tested 24 normal subjects, 24 patients with idiopathic Parkinson's disease (PD), and eight patients with bilateral absence of vestibular function (labyrinthine defective [LD] subjects) in their ability to set a straight line to the perceived gravitational vertical (visual vertical). Measurements were taken in static conditions, sitting upright, and lying down on the right side, and during visual background motion at constant angular velocities around the line of sight (roll-motion) in both sitting upright and sideways position. Aims of the study were to determine if the reported increased "visual dependence" in PD was present in a psychophysical task that is independent of motor performance, and to examine the interaction between visual motion and proprioceptive cues in the perception of verticality, in the absence of vestibular function. LD patients showed abnormally large deviations of the visual vertical induced both by lateral body tilt and by visual roll-motion. This suggests that vestibular cues play a significant part in counterbalancing visually and proprioceptive mediated biases on the perception of verticality. In contrast, PD patients were normal in all these tasks indicating that visual dependence in PD is not present at an afferent/perceptual level.
1. Head movement responses to discrete, unpredictable tilts of the trunk from earth upright were studied in normal and labyrinthine-defective (LD) subjects. Tilts of the seated, restrained trunk, were delivered in pitch and roll about head-centred axes and approximated raised cosine displacements with peak amplitudes of 20-30 deg and durations of 1.5-2 s. Subjects performed mental arithmetic with eyes closed or read earth-fixed text. 2. At the onset of tilt the head momentarily lagged behind the trunk because of inertia. Subsequently, head control varied widely with three broad types: (i) head relatively fixed to the trunk (in normal subjects and some patients); (ii) head unstable, falling in the direction of gimbal tilt (typical of acute patients for pitch motion); (iii) compensatory head movement in the opposite direction to gimbal tilt (observed consistently in normal subjects and in well-adapted patients). 3. EMG was well developed in subjects with compensatory head movement and consisted of an initial burst of activity at minimum latencies of 25-50 ms (means 72-108 ms), followed by a prolonged peak; both occurring in the 'side up' neck muscles, appropriate for righting the head. These muscles are shortened during the initial head lag so the responses cannot be stretch reflexes. In normal subjects their origin is predominantly labyrinthine but in patients they may be an 'unloading response' of the neck. 4. Head stability in space was superior with the visual task for all subjects but vision only partially compensated for labyrinthine signals in unstable patients. 5. Modelling the responses to tilt suggests that, in LD subjects, the short-latency burst could be driven by signals from the neck of the relative acceleration between head and trunk tilt. The longer latency EMG could be driven by a signal of head tilt in space. Normally, this signal is probably otolithic. In patients it could be synthesized from summing proprioceptive signals of position of head on trunk with trunk tilt.
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The detection of horizontal angular displacement of the head or trunk was assessed in 13 normal subjects and three labyrinthine defective patients. Discrete rotational displacements to the whole body (vestibular stimulus, VS), the trunk whilst keeping the head earth-stationary (cervical stimulus, CS) or the head upon the stationary trunk (combined VS+CS in passive and active mode) were delivered. Amplitudes ranged from 10 degrees to 40 degrees with peak velocities from 5 degrees to 40 degrees/s. Response was quantified as saccadic gain (final position of the eye/amplitude of the rotational stimulus) in a 'remembered saccade' task. it was found that normal subjects show different accuracy according to the sensory channel investigated. If stimulus amplitude was limited (20-30 degrees), gain dropped as rotational velocity decreased during VS but not in conditions including cervical stimulation (CS or VS+CS). Responses combining cervical and vestibular stimuli (VS+CS) were closer to unity gain and showed less scatter than isolated VS and CS. In the labyrinthine-defective patients, VS yielded no structured response but all responses involving cervical stimulation were identical to those of normal subjects when analysed both as a function of stimulus amplitude and velocity. Neither in normal nor in labyrinthine-defective subjects were there significant differences in the ability to detect head angular displacement between passive or active head turns (passive or active VS+CS). The following conclusions can be made. (i) 'Remembered saccade' techniques can be used to investigate cervico-vestibular perception. (ii) The 'high pass' characteristic of the response during VS agrees with the dynamic sensitivity of the vestibular nerve signals. Cervical experiments confirmed that neck responses are position-driven (i.e. 'tonic'). (iii) The detection of head turns is only slightly more accurate when vestibular and cervical signals are combined, but the main input controlling this perception is provided by neck afferents. No specific function for 'efference copy' was apparent in these experiments. (iv) There is no significant change for detecting head turns (on the trunk) in labyrinthine-defective patients. (v) The lack of detectable changes in cervical tasks in labyrinthine-defective patients does not support the view that the potentiation of the cervico-ocular reflex (COR) observed in these patients is due to enhanced sensitivity of the neck afferent system.