Oculomotor abnormalities related to otolith function: discussion paper.
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Biomedical subjects
Publications and source records attributed to M Gresty.
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Head movement-dependent oscillopsia (HMDO) with peripheral vestibular, brainstem and cerebellar lesions is reviewed. The differentiation of this kind of oscillopsia is based mainly on clinical grounds. HMDO with bilateral abolition of caloric responses, and in the absence of disease of the central nervous system, is due to bilateral vestibular disease. HMDO in patients with internuclear ophthalmoplegia and other brainstem signs is probably due to a lesion of VOR pathways in or near the medial longitudinal fasciculus. The occurrence of HMDO with ataxia of gait and cerebellar eye movement disorders (rebound nystagmus, flutter-like oscillations), in the absence of brainstem lesions (medial longitudinal fasciculus), is clinical evidence for HMDO due to a cerebellar lesion. An attempt is made to associate the different kinds of oscillopsia with current knowledge of the vestibulo-ocular reflexes.
Head shaking and congenital nystagmus were recorded in a patient presented with visual tasks. When she was at rest the nystagmus took a 6 cycles per second saw-tooth wave-form. When she was attentive the nystagmus beat at a 2 to 2.6 cycles per second with a saddle-shaped deformation which permitted foveation. The head shaking occurred occasionally when the patient was attentive and was phase-locked to the nystagmus with resemblances in wave form and direction. Deceleration of the head shaking to zero velocity and peak displacement (to the left) coincided with the onset of the saddle of the nystagmus and hence assisted foveation; all other parts of the head-shaking cycle were detrimental to vision. It is proposed that the head shaking has a common pathological origin with the nystagmus and that, just as an isolated congenital nystagmus wave form becomes altered with attention to permit periods of foveal fixation, the pattern of combined head and eye nodding in this patient provided similar peroids of fixation.
Three abnormalities of eye movement in man are described which are indicative of cerebellar system disorder, namely, centripetally beating nystagmus, failure to maintain lateral gaze either in darkness or with eye closure, and slow drifting movements of the eyes in the absence of fixation. Similar eye movement signs follow cerebellectomy in the primate and the cat. These abnormalities of eye movement, together with other signs of cerebellar disease, such as rebound alternating, and gaze paretic nystagmus, are explained by the hypothesis that the cerebellum helps to maintain lateral gaze and that brain stem mechanisms which monitor gaze position generate compensatory biases in the absence of normal cerebellar function.
The effect of head position on conjugate horizontal gaze was studied in healthy adults, in patients with multiple sclerosis without eye movement signs, and in patients with downbeat nystagmus indicative of low brain stem lesions. Displacements of gaze from primary position to 30 degrees left and right were recorded using the electro-oculogram, with the head in the primary position, and turned voluntarily to the left and right (in yaw). The quality of eye movements was noted and peak velocities of saccades were measured. The head turning test trebled the incidence of abnormal eye movements found in the multiple sclerosis patients and increased it by tenfold in the patients with downbeat nystagmus. Disorders of eye movement were also found in approximately 20--30% of healthy subjects tested. Weakness of abduction was the most common eye movement defect and appeared to be posterior internuclear ophthalmoplegia. A hypothesis is made which unifies the theoretical explanations of anterior and posterior internuclear ophthalmoplegia. The most likely cause of the disorders of eye movement observed is vertebrobasilar ischaemia induced by stretching and compression of the vertebral arteries during eccentric head posture.
Subjects were required to use their head and eyes in pursuit of visual targets which moved randomly or sinusoidally in the horizontal plane. All subjects disliked moving their heads to pursue the random motion, apparently because the motion broke fixation which resulted in a predominance of the vestibulo-ocular compensatory reflex over the smooth pursuit reflex. As a consequence gaze (head plus eye movement) was at times in the opposite direction to the motion of the target. In steady state pursuit of sinusoidal targets, eye movement consisted of a combination of pursuit and vestibulo-ocular reflex eye movements. At frequencies below 0.8 HZ, the vestibular reflex was used at times of minimum target velocity to stabilize fixation whereas during maximum target velocity the head movement was slowed and the smooth pursuit reflex predominated. At 1 HZ and over, there was a failure to suppress the compensatory vestibulo-ocular reflex; however, the saccades of vestibular nystagmus were used to "catch up" the target. There was a preference not to use the head in predictable pursuit.
The experiment was performed to establish the accuracy with which visual targets perceived during saccadic eye movement are localised. Subjects were presented with the task of executing saccades of 30 degrees plus amplitude, passing through primary gaze, about the time of peak velocity a 5 ms red flash was presented at some random position (up to 30 degrees left or right of centre) on a horizontal visual display. Subjects were required to indicate the direction in which they thought the flash was localised by fixating in that direction. Observations were made under conditions of prolonged total darkness and in the presence of a contrasting background. Measurement was made of saccade velocity and eye displacement as an index of target positions. Eye displacement was linearly scaled with respect to true target direction. Targets were localised with an average error of 5 degrees-6 degrees although the variance was high. No systematic differences were found between conditions or subjects. Error was unrelated to saccade velocity. It is concluded that during saccadic eye movements the appreciation of target position is maintained with an acceptable degree of accuracy.
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A case of spasmus nutans was studied using objective recordings of head and eye displacement in order to generate a precise description of the ocular oscillations and head nodding and to investigate their interrelationships. The ocularoscillations consisted of 11-Hz sinusoidal convergence movements. The head nodding consisted of a 3-Hz, 3 degrees peak to peak, sinusoidal oscillation in the horizontal plane. The occurrence of the nodding always abolished the ocular oscillation which was replaced by normal compensatory eye movements which assisted visual acuity. The hypothesis is made that the head nodding is not pathological; it is a learned behavioural pattern which permits the patient to nullify the pathological eye movements. In order to test this hypothesis further, objective evidence is required to determine the precise order of appearance of the abnormal head and eye movements in spasmus nutans.
Subjects were required to execute saccadic eye movements in the horizontal plane which passed through primary gaze. During the saccades, visual images were projected onto a screen which subtended 40 degrees horizontaloy and 26 degrees vertically and was centered on primary gaze. Content, contrast, and intensity of the stimulus patterns and level of illumination of the laboratory background were manipulated to maximise pattern recognition. Little or no detail of the projected images could be discerned under any conditions. Only horizontal laminations were perceived as blurs of appropriate colour. It is concluded that there is no useful perception of the everyday environment during saccades.
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Following responses to constant velocity and sinusoidally oscillating movements of the whole visual environment were examined in normal subjects wearing blinkers to obscure central vision or subjected to a photo flash to induce a central scotoma, in patients with central scotomas of pathological origin and in one patient with a central scotoma in an immobile eye which provided open loop testing. Good following and brisk nystagmus were produced in patients with central scotomas and subjects with flash scotomas; it was subjectively evident that the scotoma itself could be used as a target to generate open loop pursuit and augment peripherally induced following responses. Following responses in subjects with blinkers were weak, possibly reflecting that, in everyday life, eye movements induced by movements of the visual background have to be suppressed. Open loop responses were strong, suggesting that the periphery has the latent potential to mediate good following. The findings provide a unified explanation for the various patterns of optokinetic nystagmus.
The assumption that the CNS regulates head stability during human balance corrections is explored in this review (an outgrowth of discussions initiated during the Head/Neck meeting held in Vail, Colorado, USA, July 1995). Two major questions were considered. First, how do the vestibulocollic (VCR) and cervicocollic (CCR) reflexes interact with intrinsic mechanical properties of the head neck system to control head position during balance corrections? Second, how is this interaction affected by factors such as vestibular loss, aging, and changes in behavioral goals or central set? The authors conclude that head velocities observed during balance corrections depend to a large extent on the movements of the head-neck mass-viscoelastic system whose properties could be altered by cocontracting the neck muscles. For experiments involving stance perturbations, much of the corrective response in neck muscles appeared to be triggered by trunk and leg proprioceptive signals, and a major role for the VCR was not established. Evidence consistent with a role for the vestibular system was found in other experimental paradigms in which the head was perturbed directly. In these paradigms the VCR modulates the amplitude of functionally stabilizing responses and damps mechanically induced instability of the head and neck.