Ian S. Curthoys

Mechanisms of recovery following unilateral labyrinthectomy: a review

This paper reviews the literature on the mechanisms responsible for the behavioural recovery which occurs following unilateral labyrinthectomy (UL), UL causes a syndrome of ocular motor and postural disorders, which diminish over time in a process of behavioural recovery known as vestibular compensation. Electrophysiological studies show that the VIIIth nerve does not undergo a functional recovery, therefore vestibular compensation has been attributed to CNS plasticity. However, the nature of the plasticity responsible for vestibular compensation is not understood. Single-neuron studies have demonstrated that a significant recovery of resting activity has occurred in the vestibular nuclei (VN) ipsilateral to the UL by the time symptoms such as spontaneous nystagmus and roll head tilt (static symptoms) have largely disappeared. However, many of the deficits in the response of VN neurons to head acceleration persist and may be permanent. This lack of recovery in the response of neurons to head acceleration correlates with the incomplete and sometimes poor recovery of the vestibulo-ocular and vestibulo-spinal reflex responses to head movement (dynamic symptoms). The major neuronal change in the VN during vestibular compensation appears to be the recovery of resting activity in the VN ipsilateral to the UL, although this recovery is more pronounced in the medial VN than in the lateral VN. The mechanism responsible for the regeneration of resting activity in VN neurons is unknown. In frogs, there is evidence to suggest that transcommissural synaptic input to the VN, from the contralateral (intact) labyrinth, increases in efficacy.(ABSTRACT TRUNCATED AT 250 WORDS)

Responses of guinea pig primary vestibular neurons to clicks

Responses of single neurons in the vestibular nerve to high-intensity clicks were studied by extracellular recording in anaesthetised guinea pigs. One hundred and two neurons in the posterior division of the superior branch or in the inferior branch of the vestibular nerve were activated at short latency by intense clicks. The latency of activation was short (median 0.9 ms) and the threshold was high: the click intensity for evoking the response of these cells was around 60 dB above the auditory brainstem response threshold. Animals were tilted and rotated to identify physiologically the sensory region of the labyrinth from which the activated neurons originated. Seventeen neurons responded to static tilt as well as clicks. These results show that vestibular receptors, probably the otoliths, respond to clicks at intensities corresponding to those used in a new clinical test of the vestibulo-collic pathway.

The video head impulse test: Diagnostic accuracy in peripheral vestibulopathy

Background: The head impulse test (HIT) is a useful bedside test to identify peripheral vestibular deficits. However, such a deficit of the vestibulo-ocular reflex (VOR) may not be diagnosed because corrective saccades cannot always be detected by simple observation. The scleral search coil technique is the gold standard for HIT measurements, but it is not practical for routine testing or for acute patients, because they are required to wear an uncomfortable contact lens. Objective: To develop an easy-to-use video HIT system (vHIT) as a clinical tool for identifying peripheral vestibular deficits. To validate the diagnostic accuracy of vHIT by simultaneous measures with video and search coil recordings across healthy subjects and patients with a wide range of previously identified peripheral vestibular deficits. Methods: Horizontal HIT was recorded simultaneously with vHIT (250 Hz) and search coils (1,000 Hz) in 8 normal subjects, 6 patients with vestibular neuritis, 1 patient after unilateral intratympanic gentamicin, and 1 patient with bilateral gentamicin vestibulotoxicity. Results: Simultaneous video and search coil recordings of eye movements were closely comparable (average concordance correlation coefficient rc = 0.930). Mean VOR gains measured with search coils and video were not significantly different in normal (p = 0.107) and patients (p = 0.073). With these groups, the sensitivity and specificity of both the reference and index test were 1.0 (95% confidence interval 0.69–1.0). vHIT measures detected both overt and covert saccades as accurately as coils. Conclusions: The video head impulse test is equivalent to search coils in identifying peripheral vestibular deficits but easier to use in clinics, even in patients with acute vestibular neuritis.

Planar Relationships Of The Semicircular Canals In Man

Principal-component analyses were determined on a series of points measured from the dissected bony labyrinth of ten human skulls, resulting in planar equations for each of the six semicircular canals. Following this, angles were calculated between the ipsilateral canal planes, between opposite synergistically acting canal planes and between each canal and the Reid stereotaxic planes. Results indicated that pairs of ipsilateral canals were nearly perpendicular, with the excpetion of the angle formed between the anterior and horizontal canal (mean = 111 degrees). Pairs of contralateral synergistic canal planes formed angles of 19 degrees between right and left horizontal canal planes and 23-24 degrees between vertical canal pairs. The horizontal canals formed an angle of 25 degrees with the Reid horizontal plane. Mathematical equations of the semicircular canals were used to predict the optimal head position for rotational and caloric stimulation.

Physiological and Anatomical Study of Click-Sensitive Primary Vestibular Afferents in the Guinea Pig

We studied the sensitivity of primary vestibular afferents in anaesthetised guinea pigs to clicks. These vestibular neurons were also tested by their response to pitch and roll tilts and yaw-axis angular acceleration. The click intensity was referred to the threshold for evoking the auditory brainstem responses. Recording sites in the vestibular nerve were confirmed histologically using iontophoretic injection of FCF green dye. To confirm the site of labyrinthine origin of the click-sensitive neurons, we used retrograde tracing with biocytin. In all, 647 out of 2354 neurons in the vestibular nerves of 51 guinea pigs were activated by clicks. Most were irregularly discharging primary neurons, but some were regularly discharging. We studied responses to vestibular stimuli in 188 click-sensitive neurons. Of these, 86% responded to pitch and/or roll tilt, but none responded to yaw angular acceleration. Conversely we also recorded vestibular neurons which did not respond to clicks. None of 300 neurons sensitive to yaw angular acceleration were responsive to 80-90 dB SL clicks (0 dB SL = threshold for auditory brainstem response to clicks). The latencies of click-evoked action potentials of neurons in the vestibular nerve were very short (mean +/- SD = 0.82 +/- 0.22 ms). Changing click polarity caused a heterogeneous pattern of latency change. Thresholds for evoking spikes in primary vestibular neurons were high (62.0 +/- 12.2 dB SL, range 30-90 dB, n = 371). Retrograde tracing of the origin of the click-sensitive afferents using extracellular biocytin showed that most neurons originated in the medial (striola area) of the saccular macula.

A critical review of the neurophysiological evidence underlying clinical vestibular testing using sound, vibration and galvanic stimuli

In addition to activating cochlear receptors, air conducted sound (ACS) and bone conducted vibration (BCV) activate vestibular otolithic receptors, as shown by neurophysiological evidence from animal studies--evidence which is the foundation for using ACS and BCV for clinical vestibular testing by means of vestibular-evoked myogenic potentials (VEMPs). Recent research is elaborating the specificity of ACS and BCV on vestibular receptors. The evidence that saccular afferents can be activated by ACS has been mistakenly interpreted as showing that ACS only activates saccular afferents. That is not correct - ACS activates both saccular and utricular afferents, just as BCV activates both saccular and utricular afferents, although the patterns of activation for ACS and BCV do not appear to be identical. The otolithic input to sternocleidomastoid muscle appears to originate predominantly from the saccular macula. The otolithic input to the inferior oblique appears to originate predominantly from the utricular macula. Galvanic stimulation by surface electrodes on the mastoids very generally activates afferents from all vestibular sense organs. This review summarizes the physiological results, the potential artifacts and errors of logic in this area, reconciles apparent disagreements in this field. The neurophysiological results on BCV have led to a new clinical test of utricular function - the n10 of the oVEMP. The cVEMP tests saccular function while the oVEMP tests utricular function.

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.

Head taps evoke a crossed vestibulo-ocular reflex

Taps to the forehead on the midline, at the hairline (Fz), with a reflex hammer or powerful bone conduction vibrator caused short-latency surface potentials from beneath both eyes in all healthy subjects. The earliest negative responses were invariably absent from the eye contralateral to the side of a previous vestibular nerve section but were preserved despite sensorineural hearing loss. These responses probably reflect vestibular function via crossed otolith–ocular pathways.

Neuronal activity in the ipsilateral medial vestibular nucleus of the guinea pig following unilateral labyrinthectomy

The recovery of normal ocular motor and postural behavior following unilateral labyrinthectomy (vestibular compensation) has been attributed to the return of normal resting activity to neurons in the bilateral vestibular nuclei. However, previous studies in the cat have reported that average resting activity recovers to no more than 50% of the normal value in neurons in the vestibular nucleus ipsilateral to the labyrinthectomy even after 4 months post-operation (post-op.), despite the fact that, for some symptoms, vestibular compensation is complete by this time. The present data demonstrate that in the guinea pig, normal average resting activity is restored to type I neurons in the ipsilateral medial vestibular nucleus (MVN) by 52-60 h post-op., although type I neurons remain scarce compared to normal. This recovery of resting activity correlates with the compensation of spontaneous nystagmus and postural asymmetries by 52 h post-op. which we have previously reported. In addition, the present data further confirm that the recovery of type I resting activity in the ipsilateral MVN is not due to recovery of resting activity in ipsilateral Scarpas ganglion neurons or to input from the dorsal brainstem commissures.

Impulsive Testing of Semicircular-Canal Function Using Video-oculography

The head impulse test (HIT) is a safe, quick way of assessing horizontal semicircular‐canal function in patients with peripheral vestibular loss. At the bedside, the clinician identifies “overt” catch‐up saccades back to the target after brisk passive head rotation as an indirect sign of canal paresis. However, saccades during head rotation (“covert” saccades) may not be detectable by the naked eye, and so lead to incorrect diagnosis. Up to now, the scleral search coil technique has been the standard for HIT measurement, but that technique is not practical for routine diagnostic use. A new lightweight, nonslip, high‐speed video‐oculography system (vHIT) that measures eye velocity during horizontal head impulses has been developed. This system is easy to use in a clinical setting, provides an objective measure of the vestibulo‐ocular reflex (VOR), and detects both overt and covert catch‐up saccades in patients with vestibular loss.