Vestibular function after vestibular neuritis.

OBJECTIVE: To measure horizontal semicircular canal function over days, weeks, and months after an acute attack of vestibular neuritis. DESIGN: The video head impulse test (vHIT) was used to measure the eye movement response to small unpredictable passive head turns at intervals after the attack. STUDY SAMPLE: Two patients diagnosed with acute right unilateral vestibular neuritis. RESULTS: There was full restoration of horizontal canal function in one patient (A) as shown by the return of the slow phase eye velocity response to unpredictable head turns, while in the other patient (B) there was little or no recovery of horizontal canal function. Instead this second patient generated covert saccades during head turns. CONCLUSION: Despite the objective evidence of their very different recovery patterns, both patients reported, at the final test, being happy and feeling well recovered, even though in one of the patients there was clear absence of horizontal canal function. The results indicate covert saccades seem a successful way of compensating for loss of horizontal canal function after unilateral vestibular neuritis. Factors other than recovery of the slow phase eye velocity are significant for patient recovery.

Does unilateral utricular dysfunction cause horizontal spontaneous nystagmus?

The presence of spontaneous nystagmus in darkness with a strong horizontal component has been taken to indicate that there is asymmetrical function of the horizontal semicircular canals. If this horizontal spontaneous nystagmus can be suppressed by vision, then it is regarded as due to peripheral horizontal canal dysfunction. However, we report evidence from one patient (61-year-old male), who visited the MSA ENT Clinic, Cassino (FR) Italy, reporting acute, severe vertigo, postural unsteadiness, nausea and vomiting associated with right sudden hearing loss. The patient received instrumental audiovestibular testing to obtain objective measurements of his inner-ear receptors. At the time of the attack, the patient showed spontaneous nystagmus, mainly with horizontal and vertical components (3D infrared video-oculography). Video head-impulse tests of dynamic horizontal canal function showed that the functional status of both horizontal canals was within the normal range. Cervical VEMPs to 500 Hz bone-conducted vibration at Fz showed normal results; ocular VEMPs to the same stimulus showed a reduced n10 amplitude beneath the left eye, corresponding to the right ear. For this reason, the patient was diagnosed as having right unilateral selective utricular macula lesion due to labyrinthitis. There is considerable evidence of convergence of neural input from the otoliths onto horizontal canal neurons in the vestibular nuclei. The firing of such neurons could reflect either asymmetrical horizontal canal function or asymmetrical utricular function. The problem with this patient was not due to asymmetrical horizontal canal function, but only to asymmetrical utricular function, demonstrated by the results of the oVEMP test.

Ocular and cervical vestibular evoked myogenic potentials in response to bone-conducted vibration in patients with probable inferior vestibular neuritis.

BACKGROUND AND AIMS: Previous evidence shows that the n10 component of the ocular vestibular evoked myogenic potential indicates utricular function, while the p13 component of the cervical vestibular evoked myogenic potential indicates saccular function. This study aimed to assess the possibility of differential utricular and saccular function testing in the clinic, and whether loss of saccular function affects utricular response. METHODS: Following vibration conduction from the mid-forehead at the hairline, the ocular n10 component was recorded by surface electromyograph electrodes beneath both eyes, while the cervical p13-n23 component was recorded by surface electrodes over the tensed sternocleidomastoid muscles. RESULTS: Fifty-nine patients were diagnosed with probable inferior vestibular neuritis, as their cervical p13-n23 component was asymmetrical (i.e. reduced or absent on the ipsilesional side), while their ocular n10 component was symmetrical (i.e. normal beneath the contralesional eye). CONCLUSION: The sense organ responsible for the cervical and the ocular vestibular evoked myogenic potentials cannot be the same, as one response was normal while the other was not. Reduced or absent saccular function has no detectable effect on the ocular n10 component. On vibration stimulation, the ocular n10 component indicates utricular function and the cervical p13-n23 component indicates saccular function.

The basis for using bone-conducted vibration or air-conducted sound to test otolithic function.

Extracellular single neuron recordings of primary vestibular neurons in Scarpa's ganglion in guinea pigs show that low-intensity 500 Hz bone-conducted vibration (BCV) or 500 Hz air-conducted sound (ACS) activate a high proportion of otolith irregular neurons from the utricular and saccular maculae but few semicircular canal neurons. In alert guinea pigs, and humans, 500 Hz BCV elicits otolith-evoked eye movements. In humans, it also elicits a myogenic potential on tensed sternocleidomastoid muscles. Although BCV and ACS activate both utricular and saccular maculae, it is possible to probe the functional status of these two sense organs separately because of their differential neural projections. Saccular neurons have a strong projection to neck muscles and a weak projection to the oculomotor system. Utricular afferents have a strong projection to eye muscles. So measuring oculomotor responses to ACS and BCV predominantly probes utricular function, while measuring neck muscle responses to these stimuli predominantly probes saccular function.

Ocular and cervical vestibular-evoked myogenic potentials to bone conducted vibration in Ménière's disease during quiescence vs during acute attacks.

OBJECTIVE: Two indicators of otolithic function were used to measure dynamic otolith function in the same patients both during an acute attack of Ménière's disease (MD) and in the quiescent period between attacks. METHODS: The early negative component (n10) of the ocular vestibular-evoked myogenic potential (the oVEMP) to brief 500 Hz bone conducted vibration (BCV) stimulation of the forehead, in the midline at the hairline (Fz) was recorded by surface EMG electrodes just beneath both eyes while the patient looked up. It has been proposed that the n10 component of the oVEMP to 500 Hz Fz BCV indicates utricular function. It has been proposed that the early positive component (p13) of the cervical vestibular-evoked myogenic potential (the cVEMP) recorded by surface electrodes on both tensed SCM neck muscles to 500 Hz Fz BCV indicates saccular function. RESULTS: Sixteen healthy control subjects tested on two occasions showed no detectable change in the symmetry of oVEMPs or cVEMPs to 500 Hz Fz BCV. In response to 500 Hz Fz BCV 15 early MD patients tested at both attack and quiescent phases showed a dissociation: there was a significant increase in contralesional of n10 of the oVEMP during the attack compared to quiescence but a significant decrease in the ipsilesional p13 of the cVEMP during the attack compared to quiescence. CONCLUSIONS: During an MD attack, dynamic utricular function in the affected ear as measured by the n10 of the oVEMP to 500 Hz Fz BCV is enhanced, whereas dynamic saccular function in the affected ear as measured by the p13 of the cVEMP to 500 Hz Fz BCV is not similarly affected. SIGNIFICANCE: The MD attack appears to affect different otolithic regions differentially.

Effect of bone-conducted vibration of the midline forehead (Fz) in unilateral vestibular loss (uVL). Evidence for a new indicator of unilateral otolithic function.

Recently, a new indicator of vestibular otolithic function has been reported: it is a series of negative-positive myogenic potentials recorded by surface electrodes on the skin beneath the eyes in response to bone-conducted vibration (BCV) delivered to the forehead at the hairline in the midline (Fz). The potential is called the ocular vestibular-evoked myogenic potential (oVEMP) and the first component of this (n10) is a small (approximately 8 microV), short latency (~ 10 ms), negative potential. In healthy subjects, who are looking up, the n10 responses to Fz bone-conducted vibration are symmetrical beneath the two eyes. In the present investigation, in 17 patients with unilateral surgical vestibular loss, marked asymmetries were observed between the n10 beneath the two eyes: n10 is small or absent beneath the eye on the side opposite the operated ear, confirming previous evidence that n10 is a crossed vestibulo-ocular response unlike p13 of bone-conducted vibration cervical VEMPs (cVEMPs) is a ipsilateral vestibular response and also it is absent in this type of subjects. These results, together with evidence from patients with superior vestibular neuritis allow us to conclude: the asymmetry of the n10 response to Fz bone-conducted vibration is an indicator of utricular macula/superior vestibular nerve dysfunction on the operated side in patients with unilateral vestibular loss.

Testing human otolith function using bone-conducted vibration.

Bone-conducted vibration of the forehead, in the midline at the hairline (Fz) causes linear acceleration stimulation of both mastoids and results in an ocular vestibular-evoked myogenic potential (oVEMP), recorded by surface electromyogram (EMG) electrodes just beneath the eyes. The early n10 component of the oVEMP is symmetrical in healthy subjects, absent in patients with bilateral vestibular loss, and in patients after unilateral vestibular loss (uVL) n10 is small or absent on the side contralateral to the uVL, but of normal amplitude on the side contralateral to the healthy ear. The n10 component probably reflects mainly otolithic function, since in the guinea pig, primary otolith irregular neurons are selectively activated by bone-conducted vibration (BCV) at low intensities (0.1 g), whereas semicircular canal primary afferents are not activated even at high intensities (10 g).

The n10 component of the ocular vestibular-evoked myogenic potential (oVEMP) is distinct from the R1 component of the blink reflex.

OBJECTIVE: Bone-conducted vibration (BCV) in the midline at the hairline (Fz), results in short latency potentials recorded by surface electrodes beneath the eyes - the ocular vestibular-evoked myogenic potential (oVEMP). The early negative component of the oVEMP, n10, is due to vestibular stimulation, however it is similar to the early R1 component of the blink reflex. Here we seek to dissociate n10 from R1. METHODS: Surface potentials were recorded from the infraorbital electromyogram of 10 healthy subjects, 6 patients with bilateral vestibular loss, 2 with unilateral vestibular loss, 4 with facial palsy and 3 with facial and vestibular nerve lesions on the same side. BCV was delivered at Fz, the inion, the glabella or the supraorbital ridge using a tendon hammer or a bone-conduction vibrator. RESULTS: Onset latencies of the n10 evoked by taps at Fz or inion were significantly shorter than the R1 components of blink responses to supraorbital and glabellar stimuli. Upward gaze increased the amplitude of n10 but not R1. The n10 was absent bilaterally in patients with bilateral vestibular loss and beneath the contralesional eye in patients with unilateral vestibular loss, but in both these groups of patients R1 was preserved. In severe facial palsy the R1 component was absent or delayed and attenuated ipsilesionally, but n10 was preserved bilaterally. In subjects with unilateral facial and vestibular nerve lesions (Herpes Zoster of the facial and vestibulocochlear nerves) the dissociation was complete - the ipsilesional R1 was absent or attenuated whereas the ipsilesional n10 was preserved. CONCLUSIONS: n10 is distinguished from R1 by its earlier onset, laterality, modulation by gaze position and dissociation in patient groups. SIGNIFICANCE: The n10 component evoked by BCV at Fz is not the R1 component of the blink reflex.

The role of the superior vestibular nerve in generating ocular vestibular-evoked myogenic potentials to bone conducted vibration at Fz.

OBJECTIVE: The n10 component (n10) of the ocular vestibular evoked myogenic potential (oVEMP) to brief bone conducted vibration (BCV) of the forehead at Fz is probably caused by the vibration selectively activating vestibular otolithic receptors. If the n10 is due primarily to utricular activation then diseases which affect only the superior division of the vestibular nerve (SVN) should reduce or eliminate n10. METHODS: The n10 component of the oVEMP was measured in 13 patients with unilateral SVN but with inferior vestibular nerve function preserved. RESULTS: We compared the n10 to BCV of these 13 SVN patients to previously published data for healthy subjects and patients after complete unilateral vestibular loss. We found that in 12 out of the 13 patients with SVN, n10 was markedly reduced or absent under the contralesional eye. CONCLUSION: Since all utricular afferents course in the superior vestibular nerve and in 12/13 of these patients the n10 was reduced we conclude that the n10 component of the oVEMP to BCV is probably mediated by the superior vestibular nerve and probably due to activation of mainly utricular receptors. SIGNIFICANCE: The n10 appears to be a simple new test of superior vestibular nerve and probably mainly utricular function.

A review of the scientific basis and practical application of a new test of utricular function--ocular vestibular-evoked myogenic potentials to bone-conducted vibration.

This is a review of recently published papers showing that bone-conducted vibration of the head causes linear acceleration stimulation of both inner ears and this linear acceleration is an effective way of selectively activating otolithic afferent neurons. This simple stimulus is used in a new test to evaluate clinically the function of the otoliths of the human inner ear. Single neuron studies in animals have shown that semicircular canal neurons are rarely activated by levels of bone-conducted vibration at 500 Hz which generate vigorous firing in otolithic irregular neurons and which result in a variety of vestibulo-spinal and vestibulo-ocular responses, and the latter is the focus of this review. In humans, 500 Hz bone-conducted vibration, delivered at the midline of the forehead, at the hairline (Fz), causes simultaneous and approximately equal amplitude linear acceleration stimulation at both mastoids and results in ocular-evoked myogenic potentials (oVEMPs) beneath both eyes. The first component of this myogenic potential, at a latency to peak of about 10 ms is a negative potential and is called n10 and, in healthy subjects, is equal in amplitude beneath both eyes, but after unilateral vestibular loss, the n10 potential beneath the eye opposite to the lesioned ear is greatly reduced or totally absent. n10 is a myogenic potential due to a crossed otolith-ocular pathway. In patients with total unilateral superior vestibular neuritis, in whom saccular function is largely intact (as shown by the presence of cervical vestibular evoked myogenic potentials (cVEMPs), but utricular function is probably compromised, there is a reduced n10 response beneath the contralesional eye, strongly indicating that n10 is due to utricular otolithic function.

Ocular vestibular evoked myogenic potentials in response to bone-conducted vibration of the midline forehead at Fz. A new indicator of unilateral otolithic loss.

If a patient, who is lying supine and looking upward, is given bone-conducted vibration (BCV) of the forehead at the hairline in the midline (Fz) with a clinical reflex hammer or a powerful bone conduction vibrator, short-latency surface potentials called ocular vestibular evoked myogenic potentials (oVEMP) can be recorded from just beneath the eyes. The early negative (excitatory) component (n10) is approximately equal in amplitude for both eyes in healthy subjects, but in patients with unilateral vestibular loss, the n10 component is significantly asymmetrical under the 2 eyes - the n10 component is small or absent under the eye on the side contralateral to the prior unilateral vestibular nerve removal, but of normal amplitude under the eye on the side contralateral to the healthy ear. The n10 component of the oVEMP response to BCV at Fz stimuli reflects vestibular and probably mainly otolithic function via crossed otolithic-ocular pathways, and so n10 asymmetry is a new way of identifying the affected side in patients with unilateral otolithic loss.

Ocular vestibular evoked myogenic potentials to bone conducted vibration of the midline forehead at Fz in healthy subjects.

OBJECTIVE: To provide the empirical basis for using ocular vestibular evoked myogenic potentials (oVEMPS) in response to Fz bone conducted vibration (BCV) stimulation to indicate vestibular function in human subjects. To show the generality of the response by testing a large number of unselected healthy subjects across a wide age range and the repeatability of the response within subjects. To provide evidence that the response depends on otolithic function. METHODS: The early negative component (n10) of the oVEMP to brief BCV of the forehead, in the midline at the hairline (Fz) is recorded by surface EMG electrodes just beneath the eyes. We used a Bruel and Kjaer 4810 Mini-Shaker or a light tap with a tendon hammer to provide adequate BCV stimuli to test a large number (67) of unselected healthy people to quantify the individual differences in n10 magnitude, latency and symmetry to Fz BCV. A Radioear B-71 bone oscillator at Fz is not adequate to elicit a reliable n10 response. RESULTS: The n10 oVEMP response showed substantial differences in amplitude between subjects, but is repeatable within subjects. n10 is of equal magnitude in both eyes with an average asymmetry around 11%. The average n10 amplitude for Mini Tone Burst BCV is 8.47microV+/-4.02 (sd), the average latency is 10.35ms+/-0.63 (sd). The amplitude of n10 decreases and its latency increases with age. CONCLUSIONS: oVEMPs are a new reliable, repeatable test to indicate vestibular and probably otolithic function. SIGNIFICANCE: This study shows the optimum conditions for recording oVEMPs and provides baseline values for individual differences and asymmetry. oVEMPs can be measured in senior subjects without difficulty.

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.

Psychophysiological correlates of the inter-individual variability of head movement control in seated humans.

We recently conducted experiments where 24 seated participants were subjected (with eyes closed) to small amplitude, high-jerk impulses of linear acceleration. Responses were distributed as a continuum between two extremes. The "stiff" participants showed little movement of the head relative to the trunk, whereas the "floppy" participants showed a large head rotation in the direction opposite the sled movement. We hypothesized that the stiff behavior resulted from the spontaneous use of an imagined visual frame of reference and undertook this larger-scale study to test that idea. The distribution along the "stiff-floppy" continuum was compared with the scores on psychophysiological tests measuring vividness of imagery, visual field-dependence and motion sickness susceptibility. Multivariate regression analysis revealed that the "stiffness" of individuals was loosely, but significantly related to the vividness of their imagery. However, "stiffness" was not linked to visual field-dependence or motion sickness susceptibility. Even if it explains only 20% of the variance of the data, the increase of "stiffness" with vividness of imagery fits our hypothesis. With eyes closed, stiff people may use imagined external visual cues to stabilize their head and trunk. Floppy people, who are poorer imagers, may rely more on "egocentric", proprioceptive and vestibular inputs.

Patient and normal three-dimensional eye-movement responses to maintained (DC) surface galvanic vestibular stimulation.

HYPOTHESIS: That disease or dysfunction of vestibular end organs in human patients will reduce or eliminate the contribution of the affected end organs to the total eye-movement response to DC surface galvanic vestibular stimulation (GVS). BACKGROUND: It was assumed that DC GVS (at current of 5 mA) stimulates all vestibular end organs, an assumption that is strongly supported by physiological evidence, including the activation of primary vestibular afferent neurons by galvanic stimulation. Previous studies also have described the oculomotor responses to vestibular activation. Stimulation of individual semicircular canals results in eye movements parallel to the plane of the stimulated canal, and stimulation of the utricular macula produces changes in ocular torsional position. It was also assumed that the total three-dimensional eye-movement response to GVS is the sum of the contributions of the oculomotor drive of all the vestibular end organs. If a particular vestibular end organ were to be diseased or dysfunctional, it was reasoned that its contribution to the GVS-induced oculomotor response would be reduced or absent and that patients thus affected would have a systematic difference in their GVS-induced oculomotor response compared with the response of normal healthy individuals. METHODS: Three-dimensional video eye-movement recording was carried out in complete darkness on normal healthy subjects and patients with various types of vestibular dysfunction, as diagnosed by independent vestibular clinical tests. The eye-movement response to long-duration bilateral and unilateral surface GVS was measured. RESULTS: The pattern of horizontal, vertical, and torsional eye velocity and eye position during GVS of patients independently diagnosed with bilateral vestibular dysfunction, unilateral vestibular dysfunction, CHARGE syndrome (semicircular canal hypoplasia), semicircular canal occlusion, or inferior vestibular neuritis differed systematically from the responses of normal healthy subjects in ways that corresponded to the expectations from the conceptual approach of the study. CONCLUSION: The study reports the first data on the differences between the normal response to GVS and those of patients with a number of clinical vestibular conditions including unilateral vestibular loss, canal block, and vestibular neuritis. The GVS-induced eye-movement patterns of patients with vestibular dysfunction are consistent with the reduction or absence of oculomotor contribution from the end organs implicated in their particular disease condition.

Convergence reduces ocular counterroll (OCR) during static roll-tilt.

When humans are roll-tilted around the naso-occipital axis, both eyes roll or tort in the opposite direction to roll-tilt, a phenomenon known as ocular counterroll (OCR). While the magnitude of OCR is primarily determined by vestibular, somatosensory, and proprioceptive input, direction of gaze also plays a major role. The aim of this study was to measure the interaction between some of these factors in the control of OCR. Videooculography was used to measure 3D eye position during maintained whole body (en bloc) static roll-tilt in darkness, while subjects fixated first on a distant (at 130 cm) and then a near (at 30 cm) head-fixed target aligned with the subject's midline. We found that while converging on the near target, human subjects displayed a significant reduction in OCR for both directions of roll-tilt--i.e. the interaction between OCR and vergence was not simple addition or subtraction of torsion induced by vergence with torsion induced by roll-tilt. To remove the possibility that the OCR reduction may be associated with the changed horizontal position of the eye in the orbit during symmetric convergence, we ran an experiment using asymmetric convergence in which the distant and near targets were aligned directly in front of one eye. We found the magnitude of OCR in this asymmetric convergence case was also reduced for near viewing by about the same amount as in the symmetric vergence condition, confirming that the convergence command rather than horizontal position of the eye underlies the OCR reduction, since there was no horizontal movement of the aligned eye in the orbit between fixation on the distant and near targets. Increasing vergence from 130 to 30 cm reduced OCR gain by around 35% on average. That reduction was equal in both eyes and occurred in both the symmetric and asymmetric convergence conditions. These results demonstrate the important role vergence plays in determining ocular counterroll during roll-tilt and may support the contention that vergence acts to reduce the conflict facing a stereopsis-generating mechanism.

Variability in the control of head movements in seated humans: a link with whiplash injuries?

The aim of this study was to determine how context and on-line sensory information are combined to control posture in seated subjects submitted to high-jerk, passive linear accelerations. Subjects were seated with eyes closed on a servo-controlled linear sled. They were asked to relax and received brief accelerations either sideways or in the fore-aft direction. The stimuli had an abrupt onset, comparable to the jerk experienced during a minor car collision. Rotation and translation of the head and body were measured using an Optotrak system. In some of the subjects, surface electromyographic (EMG) responses of selected neck and/or back muscles were recorded simultaneously. For each subject, responses were highly stereotyped from the first trial, and showed little sign of habituation or sensitisation. Comparable results were obtained with sideways and fore-aft accelerations. During each impulse, the head lagged behind the trunk for several tens of milliseconds. The subjects' head movement responses were distributed as a continuum in between two extreme categories. The 'stiff' subjects showed little rotation or translation of the head relative to the trunk for the whole duration of the impulse. In contrast, the 'floppy' subjects showed a large roll or pitch of the head relative to the trunk in the direction opposite to the sled movement. This response appeared as an exaggerated 'inertial' response to the impulse. Surface EMG recordings showed that most of the stiff subjects were not contracting their superficial neck or back muscles. We think they relied on bilateral contractions of their deep, axial musculature to keep the head-neck ensemble in line with the trunk during the movement. About half of the floppy subjects displayed reflex activation of the neck muscles on the side opposite to the direction of acceleration, which occurred before or during the head movement and tended to exaggerate it. The other floppy subjects seemed to rely on only the passive biomechanical properties of their head-neck ensemble to compensate for the perturbation. In our study, proprioception was the sole source of sensory information as long as the head did not move. We therefore presume that the EMG responses and head movements we observed were mainly triggered by the activation of stretch receptors in the hips, trunk and/or neck. The visualisation of an imaginary reference in space during sideways impulses significantly reduced the head roll exhibited by floppy subjects. This suggests that the adoption by the central nervous system of an extrinsic, 'allocentric' frame of reference instead of an intrinsic, 'egocentric' one may be instrumental for the selection of the stiff strategy. The response of floppy subjects appeared to be maladaptive and likely to increase the risk of whiplash injury during motor vehicle accidents. Evolution of postural control may not have taken into account the implications of passive, high-acceleration perturbations affecting seated subjects.

Semicircular canal occlusion causes permanent VOR changes.

We measured the guinea pig horizontal vestibulo-ocular reflex (hVOR) to high acceleration impulsive head rotations following a unilateral lateral semicircular canal (LSCC) occlusion. We found a significant hVOR deficit for rotations toward the side of the occluded LSCC and this deficit did not show systematic changes over 3 months. We considered the LSCC nerve was still functional as shown by the normal appearance of the crista of the LSCC ampulla and also electrical stimulation of the LSCC. We conclude that the VOR during angular acceleration in response to high acceleration shows no adaptive plasticity following a unilateral LSCC occlusion.