Coordination of eye and head movements during smooth pursuit in patients with vestibular failure.

During pursuit of smoothly moving targets with combined eye and head movements in normal subjects, accurate gaze control depends on successful interaction of the vestibular and head movement signals with the ocular pursuit mechanisms. To investigate compensation for loss of the vestibulo-ocular reflex during head-free pursuit in labyrinthine-deficient patients, pursuit performance was assessed and compared under head-fixed and head-free conditions in five patients with isolated bilateral loss of vestibular function. Target motion consisted of predictable and unpredictable pseudo-random waveforms containing the sum of three or four sinusoids. Comparison of slow-phase gaze velocity gains under head-free and head-fixed conditions revealed no significant differences during pursuit of any of the three pseudo-random waveforms. The finding of significant compensatory eye movement during active head movements in darkness in labyrinthine-deficient patients, which were comparable in character and gain to the vestibular eye movement elicited in normal subjects, probably explains the similarity of the head-fixed and head-free responses. In two additional patients with cerebellar degeneration and vestibular failure, no compensatory eye movement response was observed, implying that the cerebellum is necessary for the generation of such responses in labyrinthine-deficient patients.     

Bone conducted vibration activates the vestibulo-ocular reflex in the guinea pig

The aim of the study was: (a) to test whether short duration (6 ms) 500 Hz bone-conducted vibration (BCV) of the skull in alert head free guinea pigs would elicit eye movements; (b) to test whether these eye movements were vestibular in origin; and (c) to determine whether they corresponded to human eye movements to such stimuli. In this way we sought to establish the guinea pig as an acceptable model for testing the mechanism of the effect BCV on the vestibulo-ocular reflex. Consistent short-latency stimulus-locked responses to BCV were observed. The magnitude of eye displacement was directly related to stimulus intensity as recorded by accelerometers cemented onto the animal's skull. The strongest and most consistent response component was intorsion of both eyes. In lateral-eyed animals intorsion is produced by the combined contraction of the inferior rectus and superior oblique muscles. In humans the same pair of muscles acts to cause depression of the eye. To test whether the movements were vestibular we selectively ablated the vestibular endorgans: 3 of the 8 animals underwent a bilateral intratympanic injection of gentamicin, an ototoxic aminoglycoside antibiotic, to ablate their vestibular receptors. After ablation there was an overall reduction in the magnitude of eye displacement, as well as a reduction in the effectiveness of the BCV stimulus to elicit eye movements. The animals' hearing, as measured by the threshold for auditory brainstem responses, remained unchanged after gentamicin, confirming that the cochlea was not affected. The reduced magnitude of responses after vestibular receptor ablation demonstrates that the eye-movement responses to BCV are probably caused by the stimulation of vestibular receptors, which in turn activate the vestibulo-ocular reflex.     

Vestibular compensation and substitution

This is a very brief update on the major papers since August 1998. Unilateral vestibular loss causes oculomotor, postural and sensory symptoms, all of which would be appropriate responses in a healthy person to a strong maintained angular and linear acceleration stimulus directed towards the healthy side. Within hours or days these static symptoms (so called because they are present without any externally imposed vestibular stimulation) reduce, and their progressive disappearance is called 'vestibular compensation'. However, careful testing with natural vestibular stimuli shows that the dynamic vestibular response after unilateral vestibular loss to passively imposed vestibular stimuli does not recover; it is usually asymmetric and functionally ineffective. Major recent developments are: (1) the permanent asymmetrical and functionally ineffective dynamic rotational vestibulo-ocular reflex responses to passive natural vestibular stimulation after unilateral vestibular loss and canal blocks in human patients; (2) evidence for the substitution of other sensory input and responses during vestibular compensation; (3) perceptual testing using visual perception of a horizontal line to confirm permanent otolith dysfunction; (4) the clear and substantial differences in post-unilateral vestibular loss vestibulo-ocular reflex responses between passive and active head turning; and (5) new results in brainstem physiology explaining the disappearance of static symptoms.     

Sensory-to-motor transformations in the vestibular system

The vestibulo-ocular reflex is a compensatory reflex that results in eye movements that are 180 degrees out of phase with movements of the head but that match head velocity. Because of these reflex eye movements that are equal, but opposite to head movement, the viewed object remains on the fovea of the retina during head movement, thus resulting in visual acuity that is not degraded by visual image slip on the retina. This reflex is compensatory over a large spectrum of head movements in any plane of space. This is accomplished by a spatial and temporal transformation of the input from the vestibular semicircular canals to the motoneurons that innervate the extraocular muscles. The reflex is a three-neuron arc. The middle leg of the reflex is accomplished by secondary vestibular neurons whose axons branch to innervate more than one extraocular muscle. These secondary neurons thus program an eye movement rather than the contraction of a single extraocular muscle. These programmed eye movements that match the plane of the particular semicircular canal that is the input to the reflex constitute the spatial transformation. Primary vestibular afferents innervating the semicircular canals have a broad range of response dynamics that either lead, lag or are in phase with head velocity. The predominant vestibular primary afferent input to the middle leg of the reflex, the same secondary neurons as mentioned above, is parcellated so that afferents more in phase with head velocity predominate.(ABSTRACT TRUNCATED AT 250 WORDS)     

Potentiation by vestibular stimulation of the immobility reflex elicited by clamping in developing and adult rats

We have previously described (Exp. Neurol., 97: 315-326, 1987) that clamping of the neck elicits a profound immobility with flexion of limbs and ventroflexion of head and neck ('carrying posture'). We also observed that when a clamped rat pup is carried by the experimenter's hand, such carrying posture was potentiated. In the present paper we observed that in adult rats vestibular stimulation by circular acceleration potentiates the duration of immobility reflex by clamping and intensifies the limb flexion. In rat pups from 10 to 20 days, vestibular stimulation potentiated only the carrying posture but not the duration of the immobility reflex by clamping.     

Head deviation in progressive supranuclear palsy: enhanced vestibulo-collic reflex or loss of resetting head movements?

It is unclear how the torticollis occasionally observed in patients with progressive supranuclear palsy (PSP) relates to vestibulo-collic reflex mechanisms. We report here the results of vestibular evoked myogenic potentials (VEMPs) in a PSP patient with forced head deviation in the opposite direction of turning, leading to torticollis for a few seconds. As VEMPs were normal bilaterally we conclude that an enhanced vestibulo-collic reflex per se is not the cause of the torticollis in our patient. The abnormal head deviation induced by turning in some PSP patients is best explained by damage to reticular nuclei responsible for resetting eye and head saccades. When such mechanisms are defective, unopposed vestibulo-collic reflexes can lead to eye and head deviations in the opposite direction of body turns.     

Individual semicircular canal function in superior and inferior vestibular neuritis

OBJECTIVE: To examine the concept of selective superior and inferior vestibular nerve involvement in vestibular neuritis by studying the distribution of semicircular canal (SCC) involvement in such patients. BACKGROUND: Vestibular neuritis was traditionally thought to involve the superior and inferior vestibular nerves. Recent work suggests that in some patients, only the superior nerve is involved. So far there are no reported cases of selective involvement of the inferior vestibular nerve. METHODS: The authors measured the vestibuloocular reflex from individual SCC at natural head accelerations using the head impulse test. The authors studied 33 patients with acute unilateral peripheral vestibulopathy, including 29 with classic vestibular neuritis and 4 with simultaneous ipsilateral hearing loss, 18 healthy subjects and 15 surgical unilateral vestibular deafferented patients. RESULTS: In patients with preserved hearing, eight had deficits in all three SCC, suggesting involvement of the superior and inferior vestibular nerves. Twenty-one had a lateral SCC deficit or a combined lateral and anterior SCC deficit consistent with selective involvement of the superior vestibular nerve. Two patients with ipsilateral hearing loss had normal caloric responses and an isolated posterior SCC deficit on impulsive testing. The authors propose that these two patients had a selective loss of inferior vestibular nerve function. CONCLUSION: Vestibular neuritis can affect the superior and inferior vestibular nerves together or can selectively affect the superior vestibular nerve.     

Ocular vestibular evoked myogenic potentials (OVEMPs) produced by impulsive transmastoid accelerations.

OBJECTIVE: Recent work has demonstrated the existence of ocular vestibular evoked myogenic potentials (OVEMPs), which likely reflect projections underlying the translational vestibular ocular reflex (TVOR). We examined extraocular muscle activity associated with impulsive acceleration of the head in the transmastoid plane. METHODS: Accelerometry was measured in 4 subjects in response to acceleration impulses produced by a gamma function delivered with a Minishaker (4810, Bruel & Kjaer). This stimulus produced peak head accelerations of 0.13-0.14 g occurring at between 3.1 and 4.0 ms at the mastoids for both right and left head movement. OVEMPs were recorded in 10 normal subjects with 5 directions of gaze, using electrode pairs placed lateral to, above and below the eyes. RESULTS: OVEMPs occurred at short latency, with initial peaks between 10.3 ms (p10) and 15.3 ms (n15). For a given recording site and gaze direction, the responses were determined solely by the direction of imposed acceleration. CONCLUSIONS: We propose that, given the transtemporal nature of the stimuli, utricular afferents are likely to be powerfully activated. The OVEMPs evoked may be generated by the lateral recti and oblique muscles. SIGNIFICANCE: Sudden lateral accelerations of the head evoke the translational VOR and ocular counter rolling reflex and the pattern of muscle activations indicated by the OVEMPs appear to be a manifestation of these reflexes.     

Reflex responses of masseter muscles to sound

Acoustic stimuli can evoke reflex EMG responses (acoustic jaw reflex) in the masseter muscle. Although these were previously ascribed to activation of cochlear receptors, high intensity sound can also activate vestibular receptors. Since anatomical and physiological studies, both in animals and humans, have shown that masseter muscles are a target for vestibular inputs we have recently reassessed the vestibular contribution to masseter reflexes. We found that high intensity sound evokes two bilateral and symmetrical short-latency responses in active unrectified masseter EMG of healthy subjects: a high threshold, early p11/n15 wave and a lower threshold, later p16/n21 wave. Both of these reflexes are inhibitory but differ in their threshold, latency and appearance in the rectified EMG average. Experiments in healthy subjects and in patients with selective lesions showed that vestibular receptors were responsible for the p11/n15 wave (vestibulo-masseteric reflex) whereas cochlear receptors were responsible for the p16/n21 wave (acoustic masseteric reflex). The possible functional significance of the double vestibular control over masseter muscles is discussed.     

Vestibulo-ocular abnormalities in spasmodic torticollis before and after botulinum toxin injections.

In order to establish whether vestibular abnormalities often found in spasmodic torticollis are secondary to the abnormal head posture, the vestibulo-ocular reflex (VOR) was studied in eight patients before and after correction of head posture with botulinum toxin. Eye movements were recorded in the dark during sinusoidal and velocity step rotation. Four patients showed a significantly asymmetric response, with the slow phase of the VOR more active ipsilateral to the torticollis (chin). Despite significant improvement of the head posture in all patients for up to 10 weeks following treatment, no correction of the vestibular asymmetry occurred. This suggests that the VOR abnormalities are not caused by the head posture itself. We interpret the findings as evidence of primary involvement of the vestibular system in torticollis and we postulate a widespread derangement of the sensory-motor mechanisms controlling head posture in this disease.     

Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys

The vestibulo-ocular reflex (VOR) is subject to long-term adaptive changes that minimize retinal image slip and keep eye movement equal to and opposite head movement. As a step toward identifying the site of neural changes, we have used a transient vestibular stimulus to study the dynamic response properties of the vestibular signals carried by the modifiable pathways. In normal monkeys, "rapid changes in head velocity" (30 degrees/sec in 50 msec) evoke a VOR that has a slight overshoot and reaches a steady-state gain (eye velocity divided by head velocity) of 1.0. Adaptation to magnifying spectacles causes changes in both the steady-state gain and the degree of overshoot in the eye velocity of the VOR. When the steady-state gain is decreased, the transient overshoot increases, so that peak eye velocity is twice steady-state. When the steady-state gain is increased, the overshoot decreases, so that peak eye velocity is nearly equal to steady-state. The discharge of vestibular primary afferents suggests an explanation for the inverse relationship between the transient overshoot and the steady-state gain of the VOR. In normal monkeys, 73 afferents showed a range of transient responses during rapid changes in head velocity. The afferents with the most regular spontaneous discharge had little overshoot in firing rate. Afferents with less regular discharge had large overshoots in firing; the peak change in firing was 2-6 X the steady-state change. We suggest that the large overshoot in eye velocity when VOR gain is low represents the contribution of vestibular signals from afferents with large transient responses.(ABSTRACT TRUNCATED AT 250 WORDS)     

Bedside Evaluation of Dizzy Patients

In recent decades there has been marked progress in the imaging and laboratory evaluation of dizzy patients. However, detailed history taking and comprehensive bedside neurotological evaluation remain crucial for a diagnosis of dizziness. Bedside neurotological evaluation should include examinations for ocular alignment, spontaneous and gaze-evoked nystagmus, the vestibulo-ocular reflex, saccades, smooth pursuit, and balance. In patients with acute spontaneous vertigo, negative head impulse test, direction-changing nystagmus, and skew deviation mostly indicate central vestibular disorders. In contrast, patients with unilateral peripheral deafferentation invariably have a positive head impulse test and mixed horizontal-torsional nystagmus beating away from the lesion side. Since suppression by visual fixation is the rule in peripheral nystagmus and is frequent even in central nystagmus, removal of visual fixation using Frenzel glasses is required for the proper evaluation of central as well as peripheral nystagmus. Head-shaking, cranial vibration, hyperventilation, pressure to the external auditory canal, and loud sounds may disclose underlying vestibular dysfunction by inducing nystagmus or modulating the spontaneous nystagmus. In patients with positional vertigo, the diagnosis can be made by determining patterns of the nystagmus induced during various positional maneuvers that include straight head hanging, the Dix-Hallpike maneuver, supine head roll, and head turning and bending while sitting. Abnormal smooth pursuit and saccades, and severe imbalance also indicate central pathologies. Physicians should be familiar with bedside neurotological examinations and be aware of the clinical implications of the findings when evaluating dizzy patients.     

Are Covert Saccade Functionally Relevant in Vestibular Hypofunction?

The vestibulo-ocular reflex maintains gaze stabilization during angular or linear head accelerations, allowing adequate dynamic visual acuity. In case of bilateral vestibular hypofunction, patients use saccades to compensate for the reduced vestibulo-ocular reflex function, with covert saccades occurring even during the head displacement. In this study, we questioned whether covert saccades help maintain dynamic visual acuity, and evaluated which characteristic of these saccades are the most relevant to improve visual function. We prospectively included 18 patients with chronic bilateral vestibular hypofunction. Subjects underwent evaluation of dynamic visual acuity in the horizontal plane as well as video recording of their head and eye positions during horizontal head impulse tests in both directions (36 ears tested). Frequency, latency, consistency of covert saccade initiation, and gain of covert saccades as well as residual vestibulo-ocular reflex gain were calculated. We found no correlation between residual vestibulo-ocular reflex gain and dynamic visual acuity. Dynamic visual acuity performance was however positively correlated with the frequency and gain of covert saccades and negatively correlated with covert saccade latency. There was no correlation between consistency of covert saccade initiation and dynamic visual acuity. Even though gaze stabilization in space during covert saccades might be of very short duration, these refixation saccades seem to improve vision in patients with bilateral vestibular hypofunction during angular head impulses. These findings emphasize the need for specific rehabilitation technics that favor the triggering of covert saccades. The physiological origin of covert saccades is discussed.     

Reversed Corrective Saccades during Head Impulse Test in Acute Cerebellar Dysfunction

Patients with cerebellar lesions may show horizontal (positive)- or downward (perverted)-corrective saccades during horizontal head impulse test (HIT). However, corrective saccades in the direction of head rotation (reversed corrective saccades) have not been reported during HIT. We present two patients who showed reversed corrective saccades during horizontal HIT as an initial sign of acute cerebellitis. In contrast to the corrective saccades mostly observed in peripheral vestibular paresis, this paradoxical response indicates abnormally increased vestibulo-ocular responses due to cerebellar disinhibition over the vestibulo-ocular reflex. This paradoxical response should be considered an additional bedside cerebellar sign.     

The effects of the cerebral,cerebellar and vestibular systems on the head stabilization reflex

The head stabilization reflex (HSR) is a brain stem reflex which appears in the neck muscles in response to sudden head position changes and brings the head to its previous position. The reflex mechanism has not been understood. The afferent fibers come from cervical muscle spindles, vestibular structures, and the accessory nerve, the efferents from the accessory nerve. In this study, we aim to investigate the roles of supraspinal neural structures and the vestibular system on the HSR. The patient group consisted of 86 patients (33 cerebral cortical lesion, 14 cerebellar syndrome and 39 vestibular inexcitability or hypoexcitability); the control group was composed of 32 healthy volunteers. Concentric needle electrodes were inserted into the sternocleidomastoid muscle (SCM) and the accessory nerves were stimulated with the electrical stimulator. A reflex response of about 45–55 ms was obtained from the contralateral SCM muscle. 50 % of cases had bilateral loss whereas 37 % of cases with unilateral cerebellar lesions had an ipsilateral reflex loss. Bilateral HSR loss was detected in 84 % of cases with bilateral cerebellar lesions. Bilateral reflex loss was observed in 70 % of patients with unilateral cortical lesions and 94 % of those with bilateral vestibular dysfunction. Ipsilateral HSR loss was observed in 55 % of cases with unilateral vestibular dysfunction. It was discovered that supraspinal structures and the vestibular system may have an excitatory effect on HSR. This effect may be lost in supra-segmental and vestibular dysfunctions. The localization value of HSR was found to be rather poor in our study.     

Vestibular responses in Wernicke's encephalopathy

Two patients with Wernicke's encephalopathy were evaluated with quantitative vestibulo-ocular reflex and ocular motor testing. Vestibulo-ocular reflex testing included caloric irrigation, earth vertical axis rotational sinusoids, and rotational impulses. Both patients demonstrated hypoactive vestibular responses to both caloric and rotational stimuli at the time of presentation. One patient had unbeating nystagmus that diminished with upgaze, downgaze, or convergence. Following treatment with thiamine, both patients' vestibular responses improved but remained abnormal, with a short vestibulo-ocular reflex time constant and increased low-frequency rotational phase lead. Impairment of the velocity storage element attributable to damage to the vestibular nucleus and nucleus prepositus hypoglossi may account for this permanent effect on the vestibulo-ocular reflex.     

Cervical nystagmus due to loss of cerebellar inhibition on the cervico-ocular reflex: a case report.

Studies of the cervico-ocular reflex and the vestibulo-ocular reflex have been carried out separately and in combination on a patient with gait ataxia due to a cerebellar tumour. With the head fixed in space, body rotation to the right (left neck torsion) induced marked nystagmus to the left in darkness. Vestibulo-ocular responses to sinusoidal rotation were symmetrical while the neck was immobilised and asymmetric when it moved freely. It is suggested that the cervical nystagmus seen in this case was the result of removal of cerebellar inhibition upon the cervico-ocular reflex and that abnormal interaction of cervical and vestibular inputs could have played a role in the patient's unsteadiness.     

Vestibular contribution to the orientation of cervico-ocular reflex in rabbit

In the rabbit the cervico-ocular reflex (COR) helps to maintain the gaze stability during passive head displacements, by increasing the gain and decreasing the phase lead of low frequency vestibular responses and by diminishing in amplitude the anticompensatory vestibular fast phases. These cervical influences appear only for horizontal stimulations, while they are scarce or absent in the vertical and sagittal planes. Ocular responses to horizontal body displacements are oriented in the horizontal plane and remain in the same plane when the head is statically pitched at various degrees, in spite of the directional changes in the extraocular muscle (EOM) lines of force with respect to space. Tension recordings from the EOMs show that the oculomotor system is differently activated depending upon the degree of head inclination. This change in the EOM activation is not observed when the body, instead of the head, is pitched. Furthermore, after bilateral labyrinthectomy (BL) the cervico-ocular responses lose their appropriate directionality. It is concluded that the information for determining the plane of the eye movements during cervical stimulations does not originate from the neck proprioception but is provided by the otolithic receptors.     

Vestibular contribution to the orientration of cervico-ocular reflex in rabbit

In the rabbit the cervico-ocular reflex (COR) helps to maintain the gaze stability during passive head displacements, by increasing the gain and decreasing the phase lead of low frequency vestibular responses and by diminishing in amplitude the anticompensatory vestibular fast phases. These cervical influences appear only for horizontal stimulations, while they are scarce or absent in the vertical and sagittal planes. Ocular responses to horizontal body displacements are oriented in the horizontal plane and remain in the same plane when the head is statically pitched at various degrees, in spite of the directional changes in the extraocular muscle (EOM) lines of force with respect to space. Tension recordings from the EOMs show that the oculomotor system is differently activated depending upon the degree of head inclination. This change in the EOM activation is not observed when the body, instead of the head, is pitched. Furthermore, after bilateral labyrinthectomy (BL) the cervico-ocular responses lose their appropriate directionality. It is concluded that the information for determining the plane of the eye movements during cervical stimulations does not originate from the neck proprioception but is provided by the otolithic receptors.     

Oculomotor related interaction of vestibular and visual stimulation in vestibular nucleus cells in alert monkey

The activity of single cells in the vestibular nuclei in alert, behaving monkey was studied by extracellular recording. A majority of the neurons found in the superior and the rostral medial vestibular nuclei can be divided into two classes on the basis of their discharge relationship to eye movements evoked during head rotation, visual target pursuit, or visual suppression of the vestibulo-ocular reflex. The firing rate of the first unit type is proportional to head rotational velocity (and the resulting compensatory eye velocity) but is not modulated during slow eye movements of pure visual origin. During visual suppression of the vestibulo-ocular reflex, the relationship of this type of unit discharge to head velocity remains unchanged, although the eye velocity is now zero. The second type of unit more closely resembles oculomotor neurons in that its discharge pattern is proportional to eye position and velocity during eye movements of both visual and vestibular origin. However during suppression of the vestibuloocular reflex this type of unit continues to show a greatly reduced but consistent modulation of discharge rate proportional to head velocity. Thus the direct projection of vestibular neurons to oculomotor neurons cannot by itself account for the ability of the monkey to completely suppress its vestibulo-ocular reflex.