Benjamin T. Crane

The human horizontal vestibulo-ocular reflex during combined linear and angular acceleration.

Abstract We employed binocular magnetic search coils to study the vestibulo-ocular reflex (VOR) and visually enhanced vestibulo-ocular reflex (VVOR) of 15 human subjects undergoing passive, whole-body rotations about a vertical (yaw) axis delivered as a series of pseudorandom transients and sinusoidal oscillations at frequencies from 0.8 to 2.0 Hz. Rotations were about a series of five axes ranging from 20 cm posterior to the eyes to 10 cm anterior to the eyes. Subjects were asked to regard visible or remembered targets 10 cm, 25 cm, and 600 cm distant from the right eye. During sinusoidal rotations, the gain and phase of the VOR and VVOR were found to be highly dependent on target distance and eccentricity of the rotational axis. For axes midway between or anterior to the eyes, sinusoidal gain decreased progressively with increasing target proximity, while, for axes posterior to the otolith organs, gain increased progressively with target proximity. These effects were large and highly significant. When targets were remote, rotational axis eccentricity nevertheless had a small but significant effect on sinusoidal gain. For sinusoidal rotational axes midway between or anterior to the eyes, a phase lead was present that increased with rotational frequency, while for axes posterior to the otolith organs phase lag increased with rotational frequency. Transient trials were analyzed during the first 25 ms and from 25 to 80 ms after the onset of the head rotation. During the initial 25 ms of transient head rotations, VOR and VVOR gains were not significantly influenced by rotational eccentricity or target distance. Later in the transient responses, 25–80 ms from movement onset, both target distance and eccentricity significantly influenced gain in a manner similar to the behavior during sinusoidal rotation. Vergence angle generally remained near the theoretically ideal value during illuminated test conditions (VVOR), while in darkness vergence often varied modestly from the ideal value. Regression analysis of instantaneous VOR gain as a function of vergence demonstrated only a weak correlation, indicating that instantaneous gain is not likely to be directly dependent on vergence. A model was proposed in which linear acceleration as sensed by the otoliths is scaled by target distance and summed with angular acceleration as sensed by the semicircular canals to control eye movements. The model was fit to the sinusoidal VOR data collected in darkness and was found to describe the major trends observed in the data. The results of the model suggest that a linear interaction exists between the canal and otolithic inputs to the VOR.

Magnetic resonance imaging at 1.5 T after cochlear implantation.

Objective: To assess the safety of 1.5 T magnetic resonance imaging (MRI) in patients with cochlear implants (CIs) with internal magnets. Study Design: Retrospective review of CI patients who underwent an MRI at Johns Hopkins. Patients: Sixteen patients with a mean age of 43 ± 22 years with a CI underwent a total of 22 clinically indicated 1.5 T MRI. Devices from 3 major CI manufactures were represented. Interventions: Binding of CI with mold material and gauze was performed before MRI. Some patients were also administered a sedative. Intravenous gadolinium contrast was used in all but 1 patient. Main Outcome Measures: Patients were assessed with regard to the ability to complete the MRI, the size of the artifact caused by the device, the ability to make a diagnosis from the studies, the post-MRI CI function, and the magnets position. Results: No CI malfunction, displacement, or magnet displacement was observed after MRI. One patient was unable to tolerate the procedure because of pressure at the site of the device. One patient required intravenous sedation to complete the study. The CI generally produced an artifact on brain MRI, with a mean maximal anterior-posterior dimension of 6.6 cm and a lateral dimension of 4.8 cm around the site of the device. The contralateral internal auditory canal was visualized in all patients, and the ipsilateral internal auditory canal was at least party visible in all but 1 patient. Conclusion: Patients can safely undergo 1.5 T MRI after CI if the device is tightly bound before scanning. Magnet displacement was not observed, and we think the risk to be minimal compared with the risk and inconvenience of removing the magnet before the study.

Superior canal dehiscence plugging reduces dizziness handicap.

Objectives/Hypothesis: To compare dizziness handicap inventory (DHI) scores before and after surgery for plugging of superior canal dehiscence (SCD). The size of the dehiscence as measured during surgery, subject age, vestibular‐evoked myogenic potentials threshold, and degree of conductive hearing loss (CHL) were also considered.

Three-dimensional computed tomography of superior canal dehiscence syndrome.

Objective: To compare 3-dimensional (3-D) surface reconstructions of the temporal bone with presently used multiplanar reconstructions (MPRs) from high-resolution computed tomographic (HRCT) data sets in patients with superior canal dehisence syndrome (SCDS). Results of audiometry, vestibular evoked myopotentials (VEMPs), and clinical testing are also considered. Patients: Twenty-one adults with unilateral or bilateral SCD. Interventions: High-resolution computed tomographic scans, audiograms, VEMP testing. Main Outcome Measure: Comparison of findings on 3-D surface reconstructions with MPRs; predictive values of different tests. Results: High-resolution computed tomographic scans were performed on 6 subjects with bilateral SCD and 15 with unilateral SCD. High-resolution computed tomographic scans were examined as MPRs in the plane of the SC and in perpendicular radial cuts through the SC. High-resolution computed tomographic scans were also analyzed as 3-D surface reconstructions. Compared with the MPRs, 3-D surface reconstructions for patients who had at least 1 objective finding suggestive of SCDS had a 68% positive predictive value, 91% sensitivity, and 47% specificity. None of those temporal bones that had intact SCs on MPRs had other objective findings suggestive of SCDS. Three-dimensional surface reconstructions often made SCs covered with thin bone seem dehiscent, exposed air cells can be mistaken for SCDS, and a large dehiscence can sometimes be missed. Nystagmus evoked by 110-dB relative-to-normal-hearing-level tones was 100% specific for SCDS when present but only 67% sensitive. Decreased click evoked VEMP threshold was 80% sensitive and 80% specific for SCDS. Conductive hearing loss of 10 dB or greater had an 83% sensitivity and 95% specificity. Conclusion: Multiplanar reconstructions of HRCT data are the most sensitive test for diagnosis of SCD. False SCD and missed SCD can occur with 3-D surface reconstructions of the temporal bone. Determination of SCD should be based on MPRs of an HRCT data instead of 3-D surface reconstructions, but the latter remain valuable for surgical planning. The decision for surgery in SCDS should not be based on imaging results alone but also on the physiologic findings and the frequency and severity of symptoms.

Middle ear exploration in patients with Ménière's disease who have failed outpatient intratympanic gentamicin therapy

Objective: Treatment of medically refractory Ménières disease (MD) with intratympanic (IT) gentamicin has now become a standard therapy. This procedure is effective in controlling vertigo attacks, but approximately 10% of patients do not have an adequate response. The objective of the current study was to evaluate the option of middle ear exploration with direct application of gentamicin to the round window (MEE-G) in patients with persistent MD after transtympanic injection of gentamicin. Study Design: A retrospective chart review of 191 patients with MD treated with IT gentamicin revealed 16 who failed to have symptomatic relief after transtympanic injection. Options discussed with these patients included labyrinthectomy, vestibular nerve section, and MEE-G. Setting: Tertiary referral center. Patients: Eight patients opted for MEE-G. Intervention: Patients were taken to the operating room for MEE-G. After removal of the round window obstruction, gentamicin-soaked pledgets were placed for at least 30 minutes. Main Outcome Measures: Control of MD-related vertigo and need for additional therapy. Results: At the time of MEE-G, all 8 patients were found to have adhesions, bone dust blocking the round window, or a thickened round window membrane. In 6 of these patients, vertigo symptoms due to MD either resolved with no further therapy (4 patients) or with subsequent IT gentamicin injections in clinic (2 patients). The remaining 2 patients underwent a vestibular nerve section, which resolved MD symptoms in each case. Conclusion: Anatomic barriers to the round window membrane may be a significant cause of IT gentamicin failure, and MEE-G can be considered before ablative therapy in this subset of patients with Ménières disease.

A linear canal-otolith interaction model to describe the human vestibulo-ocular reflex

Abstract. A control systems model of the vestibulo-ocular reflex (VOR) originally derived for yaw rotation about an eccentric axis (Crane et al. 1997) was applied to data collected during ambulation and dynamic posturography. The model incorporates a linear summation of an otolith response due to head translation scaled by target distance, adding to a semi-circular canal response that depends only on angular head rotation. The results of the model were compared with human experimental data by supplying head angular velocity as determined by magnetic search coil recording as the input for the canal branch of the model and supplying linear acceleration as determined by flux gate magnetometer measurements of otolith position. The model was fit to data by determining otolith weighting that enabled the model to best fit the data. We fit to the model experimental data from normal subjects who were: standing quietly, walking, running, or making active sinusoidal head movements. We also fit data obtained during dynamic posturography tasks of: standing on a platform sliding in a horizontal plane at 0.2 Hz, standing directly on a platform tilting at 0.1 Hz, and standing on the tilting platform buffered by a 5-cm thick foam rubber cushion. Each task was done with the subject attending a target approximately 500, 100, or 50 cm distant, both in light and darkness. The model accurately predicted the observed VOR response during each test. Greater otolith weighting was required for near targets for nearly all activities, consistent with weights for the otolith component found in previous studies employing imposed rotations. The only exceptions were for vertical axis motion during standing, sliding, and tilting when the platform was buffered with foam rubber. In the horizontal axis, the model always fit near target data better with a higher otolith component. Otolith weights were similar with the target visible and in darkness. The model predicts eye movement during both passive whole-body rotation and free head movement in space implying that the VOR is controlled by a similar mechanism during both situations. Factors such as vision, proprioception, and efference copy that are available during head free motion but not during whole-body rotation are probably not important to gaze stabilization during ambulation and postural stabilizing movement. The linearity of the canal-otolith interaction was tested by re-analysis of the whole body rotation data on which the model is based (Crane et al. 1997). Normalized otolith-mediated gain enhancement was determined for each axis of rotation. This analysis uncovered minor non-linearities in the canal-otolith interaction at frequencies above 1.6 Hz and when the axis of rotation was posterior to the head.

Direction Specific Biases in Human Visual and Vestibular Heading Perception

Heading direction is determined from visual and vestibular cues. Both sensory modalities have been shown to have better direction discrimination for headings near straight ahead. Previous studies of visual heading estimation have not used the full range of stimuli, and vestibular heading estimation has not previously been reported. The current experiments measure human heading estimation in the horizontal plane to vestibular, visual, and spoken stimuli. The vestibular and visual tasks involved 16 cm of platform or visual motion. The spoken stimulus was a voice command speaking a heading angle. All conditions demonstrated direction dependent biases in perceived headings such that biases increased with headings further from the fore-aft axis. The bias was larger with the visual stimulus when compared with the vestibular stimulus in all 10 subjects. For the visual and vestibular tasks precision was best for headings near fore-aft. The spoken headings had the least bias, and the variation in precision was less dependent on direction. In a separate experiment when headings were limited to ±45°, the biases were much less, demonstrating the range of headings influences perception. There was a strong and highly significant correlation between the bias curves for visual and spoken stimuli in every subject. The correlation between visual-vestibular and vestibular-spoken biases were weaker but remained significant. The observed biases in both visual and vestibular heading perception qualitatively resembled predictions of a recent population vector decoder model (Gu et al., 2010) based on the known distribution of neuronal sensitivities.

Gaze stabilization during dynamic posturography in normal and vestibulopathic humans

Abstract Dynamic posturography by measurement of center of pressure (COP) is a widely employed technique for evaluating the vestibular system. However, the relationship of COP motion to vestibulo-ocular reflex (VOR) function and image stability on the retina has not been determined previously. To assess these relationships, we report gaze, head, and trunk stability during dynamic posturography in 11 normal volunteers, 7 subjects with unilateral vestibular lesions, and 3 subjects with bilateral vestibular lesions. Posturographic tasks consisted of standing still and standing on a platform that was sliding (0.2 Hz), tilting (0.1 Hz), or covered with a foam cushion 6 cm thick while tilting (0.1 Hz). Each perturbation was imposed in the anterior-posterior and repeated in the medial-lateral direction, in both light and darkness. Subjects viewed (or in darkness remembered) a target located 50, 100, or 500 cm distant. COP, angular eye position, and angular and linear orbit and trunk positions were measured using magnetic search coils and flux gate magnetometer sensors. With the target visible, the velocity of image motion on the retina was on average always less than 1°/s, well within the range consistent with high visual acuity. In darkness, gaze velocity increased for normal and vestibulopathic subjects. During tilt, vestibulopathic subjects had a significantly greater gaze velocity than controls. Gain of the angular VOR (eye velocity/head velocity) was significantly lower in darkness than in light and in vestibulopathic as compared to control subjects. Gain of the VOR was significantly correlated with gaze instability, but variation in VOR gain accounted for only 20–40% of the variance. In darkness, the velocity of the COP was significantly greater in vestibulopathic than control subjects for every condition tested. In light, this difference was small and often not significant. Although spectral analysis of the COP indicated frequencies above 1 Hz that were not observed in motion of the trunk and orbit, root mean square (RMS) velocities of the trunk and orbit in the horizontal plane were higher in darkness and in vestibulopathic subjects, mirroring COP findings. Only in vestibulopathic subjects tested in darkness was there a correlation between COP velocity and gaze velocity; COP velocity was otherwise uncorrelated with gaze. Gaze velocity was greater with near than with distant targets. Vertical VOR gain was higher with near targets. No other significant effects of target distance were found. Head movement strategy, VOR gain, and COP were all unaffected by target proximity. These data show that gaze velocity measurements during dynamic posturography in darkness are sensitive to vestibular loss. With a visible target, both COP and gaze stability of vestibulopathic subjects are difficult to distinguish from normal. During visual feedback, it is likely that image stabilization over the range of frequencies tested is achieved through better head stability and through visual tracking, allowing vestibulopathic subjects to maintain adequate visual acuity.

New Tests of Vestibular Function

Abstract: The vestibulo‐ocular reflex (VOR) is the only drive for short‐latency eye movements stabilizing the retina during externally imposed, sudden, high‐head accelerations. New strategies can exploit this unique VOR feature to study it under conditions relevant to the daily lives of patients, and to exclude the contributions from confounding nonvestibular mechanisms. Testing of the yaw vestibulo‐ocular reflex (VOR) during random, whole‐body rotational transients at ≤2800°/s2 delivered about centered and eccentric axes enables measurement of gains and millisecond latencies of the canal and otolith VORs in humans. Repeated measurements in acute unilateral deafferentation show sequential recovery of canal and otolith VORs to contralesional rotation, but severe and permanent deficits to ipsilesional rotation. Patients with bilateral loss of caloric responses show severe bilateral loss of VORs to transient rotation, suggesting that the apparent preservation of their VORs during sinusoidal rotations at moderate frequencies may be due instead to somatosensory inputs.

Vestibular function in severe bilateral vestibulopathy

OBJECTIVES To assess residual vestibular function in patients with severe bilateral vestibulopathy comparing low frequency sinusoidal rotation with the novel technique of random, high acceleration rotation of the whole body. METHODS Eye movements were recorded by electro-oculography in darkness during passive, whole body sinusoidal yaw rotations at frequencies between 0.05 and 1.6 Hz in four patients who had absent caloric vestibular responses. These were compared with recordings using magnetic search coils during the first 100 ms after onset of whole body yaw rotation at peak accelerations of 2800°/s2. Off centre rotations added novel information about otolithic function. RESULTS Sinusoidal yaw rotations at 0.05 Hz, peak veocity 240°/s yielded minimal responses, with gain (eye velocity/head velocity)<0.02, but gain increased and phase decreased at frequencies between 0.2 and 1.6 Hz in a manner resembling the vestibulo-ocular reflex. By contrast, the patients had profoundly attenuated responses to both centred and eccentric high acceleration transients, representing virtually absent responses to this powerful vestibular stimulus. CONCLUSION The analysis of the early ocular response to random, high acceleration rotation of the whole body disclosed a profound deficit of semicircular canal and otolith function in patients for whom higher frequency sinusoidal testing was only modestly abnormal. This suggests that the high frequency responses during sinusoidal rotation were of extravestibular origin. Contributions from the somatosensory or central predictor mechanisms, might account for the generation of these responses. Random, transient rotation is better suited than steady state rotation for quantifying vestibular function in vestibulopathic patients.