Michael J. Todd

Head impulse test in unilateral vestibular loss: vestibulo-ocular reflex and catch-up saccades.

Background: Quantitative head impulse test (HIT) measures the gain of the angular vestibulo-ocular reflex (VOR) during head rotation as the ratio of eye to head acceleration. Bedside HIT identifies subsequent catch-up saccades after the head rotation as indirect signs of VOR deficit. Objective: To determine the VOR deficit and catch-up saccade characteristics in unilateral vestibular disease in response to HIT of varying accelerations. Methods: Eye and head rotations were measured with search coils during manually applied horizontal HITs of varying accelerations in patients after vestibular neuritis (VN, n = 13) and unilateral vestibular deafferentation (UVD, n = 15) compared to normal subjects (n = 12). Results: Normal VOR gain was close to unity and symmetric over the entire head-acceleration range. Patients with VN and UVD showed VOR gain asymmetry, with larger ipsilesional than contralesional deficits. As accelerations increased from 750 to 6,000 °/sec2, ipsilesional gains decreased from 0.59 to 0.29 in VN and from 0.47 to 0.13 in UVD producing increasing asymmetry. Initial catch-up saccades can occur during or after head rotation. Covert saccades during head rotation are most likely imperceptible, while overt saccades after head rotation are detectable by clinicians. With increasing acceleration, the amplitude of overt saccades in patients became larger; however, initial covert saccades also became increasingly common, occurring in up to about 70% of trials. Conclusions: Head impulse test (HIT) with high acceleration reveals vestibulo-ocular reflex deficits better and elicits larger overt catch-up saccades in unilateral vestibular patients. Covert saccades during head rotation, however, occur more frequently with higher acceleration and may be missed by clinicians. To avoid false-negative results, bedside HIT should be repeated to improve chances of detection.

Inferior vestibular neuritis.

Abstract: Sudden, spontaneous, unilateral loss of vestibular function without simultaneous hearing loss or brain stem signs is generally attributed to a viral infection involving the vestibular nerve and is called acute vestibular neuritis. The clinical hallmarks of acute vestibular neuritis are vertigo, spontaneous nystagmus, and unilateral loss of lateral semicircular function as shown by impulsive and caloric testing. In some patients with vestibular neuritis the process appears to involve only anterior and lateral semicircular function, and these patients are considered to have selective superior vestibular neuritis. Here we report on two patients with acute vertigo, normal lateral semicircular canal function as shown by both impulsive and caloric testing, but selective loss of posterior semicircular canal function as shown by impulsive testing and of saccular function as shown by vestibular evoked myogenic potential testing. We suggest that these patients had selective inferior vestibular neuritis and that contrary to conventional teaching, in a patient with acute spontaneous vertigo, unilateral loss of lateral semicircular canal function is not essential for a diagnosis of acute vestibular neuritis.

Benign positional nystagmus A study of its three-dimensional spatio-temporal characteristics

Objective: To describe the spatial and temporal characteristics of benign positional nystagmus (BPN) subtypes in benign positional vertigo (BPV) due to vestibular lithiasis affecting one or more semicircular canals (SCCs). Background: Activation of SCC receptors by sequestered otoconia, either freely moving (canalithiasis) or cupula-adherent (cupulolithiasis) during head position changes with respect to gravity, is the accepted cause of BPV. Although accurate identification and interpretation of BPN is critical to BPV therapy, no rigorous, kinematically correct three-dimensional spatio-temporal analysis of BPN in all its forms exists. Methods: Using dual-search scleral coils, the authors recorded BPN provoked by Dix–Hallpike or supine ear-down test in a two-axis whole-body rotator in 44 patients with refractory BPV. To localize the SCC affected, BPN rotation axes were compared to SCC axes, axes orthogonal to average SCC planes. Results: Sixteen patients had upbeat, geotropic-torsional BPN in the Dix–Hallpike test to one side and five to both sides, with BPN rotation axes clustered around the lowermost posterior SCC axis. Seven had direction-changing horizontal BPN, three geotropic (canalithiasis) and four apogeotropic (cupulolithiasis), with rotation axes around the lowermost and uppermost horizontal SCC axis. Seven had predominantly downbeating BPN with rotation axes clustered around one superior SCC axis. Nine had upbeat, horizontal-torsional BPN with rotation axes located between posterior and horizontal SCC axes of the lowermost ear suggesting simultaneous lithiasis in both SCCs. BPN vector-guided repositioning therapy was successful in 43 patients. Conclusion: Benign positional vertigo can affect one or more semicircular canals and three-dimensional recording with vector analysis of the benign positional nystagmus (BPN) can guide canalith repositioning therapy especially in refractory cases with atypical BPN.

Superior semicircular canal dehiscence simulating otosclerosis

This is a report of a patient with an air-bone gap, thought 10 years ago to be a conductive hearing loss due to otosclerosis and treated with a stapedectomy. It now transpires that the patient actually had a conductive hearing gain due to superior semicircular canal dehiscence. In retrospect for as long as he could remember the patient had experienced cochlear hypersensitivity to bone-conducted sounds so that he could hear his own heart beat and joints move, as well as a tuning fork placed at his ankle. He also had vestibular hypersensitivity to air-conducted sounds with sound-induced eye movements (Tullio phenomenon), pressure-induced nystagmus and low-threshold, high-amplitude vestibular-evoked myogenic potentials. Furthermore some of his acoustic reflexes were preserved even after stapedectomy and two revisions. This case shows that if acoustic reflexes are preserved in a patient with an air-bone gap then the patient needs to be checked for sound- and pressure-induced nystagmus and needs to have vestibular-evoked myogenic potential testing. If there is sound- or pressure-induced nystagmus and if the vestibular-evoked myogenic potentials are also preserved, the problem is most likely in the floor of the middle fossa and not in the middle ear, and the patient needs a high-resolution spiral computed tomography (CT) of the temporal bones to show this.

Vestibular, saccadic and fixation abnormalities in genetically confirmed Friedreich ataxia

Friedreich ataxia (FRDA), the commonest of the inherited ataxias, is a multisystem neurodegenerative condition that affects ocular motor function. We assessed eye movement abnormalities in 20 individuals with genetically confirmed FRDA and compared these results to clinical measures. All subjects were assessed with infrared oculography. Fifteen individuals underwent a full protocol of eye movement recordings. Ten subjects were analysed using two-dimensional scleral coil equipment and five using three-dimensional scleral coil recording equipment. We also recorded visual quality of life, Sloan low contrast letter acuity and Friedreich Ataxia Rating Scale scores to compare to the visual measures. Whilst saccadic velocity was essentially normal, saccadic latency was prolonged. The latency correlated with clinical measures of disease severity, including the scores for the Friedreich Ataxia Rating Scale and the Sloan low contrast letter acuity tests. Fixation abnormalities consisting of square wave jerks and ocular flutter were common, and included rare examples of vertical square wave jerks. Vestibular abnormalities were also evident in the group, with markedly reduced vestibulo-ocular reflex gain and prolonged latency. The range of eye movement abnormalities suggest that neurological dysfunction in FRDA includes brainstem, cortical and vestibular pathways. Severe vestibulopathy with essentially normal saccadic velocity are hallmarks of FRDA and differentiate it from a number of the dominant spinocerebellar ataxias. The correlation of saccadic latency with FARS score raises the possibility of its use as a biomarker for FRDA clinical trials.

Horizontal head impulse test detects gentamicin vestibulotoxicity

Background: Parenteral antibiotic therapy with gentamicin, even in accepted therapeutic doses, can occasionally cause bilateral vestibular loss (BVL) due to hair cell toxicity. Objective: To quantify in patients with gentamicin vestibulotoxicity (GVT) the extent of acceleration gain deficit of the horizontal vestibulo-ocular reflex at different accelerations with a graded head impulse test (HIT) in comparison with standard caloric and rotational testing. To characterize the corresponding HIT catch-up saccade pattern to provide the basis for its salience to clinicians. Methods: Horizontal HIT of graded acceleration (750°–6,000°/sec2) was measured with binocular dual search coils in 14 patients with GVT and compared with 14 normal subjects and a control subject with total surgical BVL. Results: Patients showed mostly symmetric HIT gain deficits with a continuous spectrum from almost normal to complete BVL. Gain deficits were present even at the lowest head accelerations. HIT gain correlated better with caloric (Spearman ρ = 0.85, p = 0.0001) than rotational testing (ρ = 0.55, p = 0.046). Cumulative amplitude of overt saccades after head impulses was 5.6 times larger in patients than in normal subjects. Compared with previously published patients after unilateral vestibular deafferentation, GVT patients with BVL generated only approximately half the percentage of covert saccades during head rotation (23% at 750°/sec2 to 46% at 6,000°/sec2). Conclusions: Head impulse testing is useful for early bedside detection of gentamicin vestibulotoxicity because most patients, even those with partial bilateral vestibular loss (BVL), have large overt saccades. Covert saccades, which can conceal the extent of BVL, are only approximately half as frequent as in unilateral patients, but may be present even in total BVL.

Impulsive Testing of Individual Semicircular Canal Function

Abstract: In order to test the human angular vestibulo‐ocular reflex in the dynamic range of normal head movements, we measured 3‐dimensional compensatory eye‐movement responses to low‐amplitude (10–12°), high‐acceleration (3000–4000°/s/s), passive, manually delivered head rotations (head “impulses”) in the three planes of the semicircular canals in normal subjects, in subjects who had recovered from surgical unilateral vestibular deafferentation, and in patients after acute unilateral peripheral vestibulopathy, that is, from vestibular “neuritis.” We found that canal‐plane head impulses away from an intact semicircular canal, that is, toward a lesioned semicircular canal, invariably produce a vestibulo‐ocular reflex with permanently low gain, typically less that 0.4 if the lesion is complete. These results are a necessary consequence of primary semicircular canal afferents being driven into inhibitory saturation by rapid angular accelerations. With practice, clinicians can learn to recognize the telltale compensatory saccades that patients with unilateral loss of semicircular canal function will make if asked to look at an earth‐fixed target during head impulses in any one of the three semicircular canal planes.

A Mathematical Model of Human Semicircular Canal Geometry: A New Basis for Interpreting Vestibular Physiology

We report a precise, simple, and accessible method of mathematically measuring and modeling the three-dimensional (3D) geometry of semicircular canals (SCCs) in living humans. Knowledge of this geometry helps understand the development and physiology of SCC stimulation. We developed a framework of robust techniques that automatically and accurately reconstruct SCC geometry from computed tomography (CT) images and are directly validated using micro-CT as ground truth. This framework measures the 3D centroid paths of the bony SCCs allowing direct comparison and analysis between ears within and between subjects. An average set of SCC morphology is calculated from 34 human ears, within which other geometrical attributes such as nonplanarity, radius of curvature, and inter-SCC angle are examined, with a focus on physiological implications. These measurements have also been used to critically evaluate plane fitting techniques that reconcile many of the discrepancies in current SCC plane studies. Finally, we mathematically model SCC geometry using Fourier series equations. This work has the potential to reinterpret physiology and pathophysiology in terms of real individual 3D morphology.

The click-evoked vestibulo-ocular reflex in superior semicircular canal dehiscence

The authors studied eye movement responses to loud (110dB) clicks in 4 patients with Tullio effect due to superior semicircular canal dehiscence and in 9 normal subjects, by averaging the electro-oculogram. All 4 patients had small (0.1–0.3 deg) but easily reproducible vertical vestibulo-ocular reflex eye movement responses to the clicks. Normal subjects had responses that were at least 10 times smaller. The click-evoked vestibulo-ocular reflex test is a simple, robust way to screen dizzy patients for symptomatic superior semicircular dehiscence.

Head impulse gain and saccade analysis in pontine-cerebellar stroke and vestibular neuritis.

Objective: We sought to quantify and compare angular vestibulo-ocular reflex (aVOR) gain and compensatory saccade properties elicited by the head impulse test (HIT) in pontine-cerebellar stroke (PCS) and vestibular neuritis (VN). Methods: Horizontal HIT was recorded ≤7 days from vertigo onset with dual-search coils in 33 PCS involving the anterior inferior, posterior inferior, and superior cerebellar arteries (13 AICA, 17 PICA, 3 SCA) confirmed by MRI and 20 VN. We determined the aVOR gain and asymmetry, and compensatory overt saccade properties including amplitude asymmetry and cumulative amplitude (ipsilesional trials [I]; contralesional trials [C]). Results: The aVOR gain (normal: 0.96; asymmetry = 2%) was bilaterally reduced, greater in AICA (I = 0.39, C = 0.57; asymmetry = 20%) than in PICA/SCA strokes (I = 0.75, C = 0.74; asymmetry = 7%), in contrast to the unilateral deficit in VN (I = 0.22, C = 0.76; asymmetry = 54%). Cumulative amplitude (normal: 1.1°) was smaller in AICA (I = 4.2°, C = 3.0°) and PICA/SCA strokes (I = 2.1°, C = 3.0°) compared with VN (I = 8.5°, C = 1.3°). Amplitude asymmetry in AICA and PICA/SCA strokes was comparable, but favored the contralesional side in PICA/SCA strokes and the ipsilesional side in VN. Saccade asymmetry <61% was found in 97% of PCS and none of VN. Gain asymmetry <40% was found in 94% of PCS and 10% of VN. Conclusion: HIT gains and compensatory saccades differ between PCS and VN. VN was characterized by unilateral gain deficits with asymmetric large saccades, AICA stroke by more symmetric bilateral gain reduction with smaller saccades, and PICA stroke by contralesional gain bias with the smallest saccades. Saccade and gain asymmetry should be investigated further in future diagnostic accuracy studies. Classification of evidence: This study provides Class II evidence that aVOR testing accurately distinguishes patients with PCS from VN (sensitivity 94%–97%, specificity 90%–100%).