Otolith-ocular Reflex Research Articles

Off-vertical axis rotational responses in patients with unilateral peripheral vestibular lesions.

Off-vertical axis rotation (OVAR) stimulates the otolith organs in a manner that is suitable for assessment of the otolith-ocular reflex. To further assess the potential clinical usefulness of OVAR, the eye movement responses of seven patients with surgically confirmed unilateral peripheral vestibular lesions were compared with the eye movement responses of a group of age-matched, healthy, asymptomatic control subjects. Patients and controls were tested with constant velocity rotations that followed a brief period of angular acceleration (velocity trapezoid) using either earth-vertical axis (EVA) rotation or OVAR. Both EVA and OVAR sinusoidal velocity profiles were also performed. Results indicated that each patient had 1) an asymmetric OVAR response, ie, a bias component whose direction was opposite normal when rotating toward the lesioned ear, and 2) a normal modulation component. Population data suggested that patients had 1) a more rapid decay of response than normal subjects during OVAR velocity trapezoids, 2) an increased phase lead as compared to normal subjects during sinusoidal OVAR, and 3) like normal subjects, a less rapid decay of response during OVAR velocity trapezoids than during EVA rotational velocity trapezoids. Taken together, these findings suggest that patients with unilateral peripheral vestibular deficits have abnormal otolith-ocular and semicircular canal-ocular reflexes but that a single labyrinth appears to provide an otolithic signal sufficient for qualitatively normal semicircular canal-otolith interaction.

Off-vertical axis rotation: a test of the otolith-ocular reflex.

The vestibulo-ocular reflex was studied via off-vertical axis rotation (OVAR) in the dark. The axis of the turntable could be tilted from vertical by up to 30 degrees. Eye movements were measured with electro-oculography. Results from healthy asymptomatic subjects indicated that 1) a reliable otolith-induced response could be obtained during constant velocity OVAR using a velocity of 60 degrees/s with a tilt of 30 degrees; 2) constant velocity OVAR rotation was nausea-producing and, especially if subjects were rotated in the dark about an earth-vertical axis prior to being tilted, disorienting; and 3) sinusoidal OVAR produced minimal nausea; the eye movement response appeared to be the result of a combination of semicircular canal and otolith components. We conclude that OVAR has the potential of becoming a useful method for clinically assessing both the otolith-ocular reflex and semicircular canal-otolith interaction.

Preservation of the electrical-evoked vestibuloocular reflex and otolith-ocular reflex in two patients with markedly impaired canal-ocular reflexes.

Preservation of the electrical-evoked vestibuloocular reflex and otolith-ocular reflex in two patients with markedly impaired canal-ocular reflexes.

Ocular torsion produced by unilateral chemical inactivation of the interstitial nucleus of Cajal in chronically labyrinthectomized cats

Unilateral lesions of the rostral midbrain involving the interstitial nucleus of Cajal (INC) have been known to produce ocular torsion in alert animals including humans, which has been assumed to be the result of an impaired otolith-ocular reflex. We examined the effects of chemical deactivation of the INC using a gamma-aminobutyric acid (GABA) agonist (muscimol) in cats that had received bilateral labyrinthectomy, and compared the results with those in normal cats. Ocular torsion with a magnitude similar to that observed in normal cats appeared in chronically labyrinthectomized cats after unilateral muscimol infusion into the INC, indicating that ocular torsion following unilateral INC deactivation can be produced by a mechanism independent of the otolith-ocular reflex.

Otolith-ocular testing in human subjects.

Assessment of the otolith-ocular reflex of human subjects involves linear acceleration and/or changes in the orientation of the head with respect to gravity. Several such stimuli are currently under investigation regarding their applicability to the evaluation of patients with dizziness and balance disorders. Discussed in this paper are off-vertical axis rotation, eccentric rotation, pitch and roll rotation, and linear acceleration. For each of these stimuli, basic principles, normative human data, and patient data are described. Although none of these methods are currently established for clinical use, each of them, especially off-vertical axis rotation and linear acceleration, have the potential for developing into a clinically useful method for assessing otolith function in man.

Plasticity of the Human Otolith-ocular Reflex

The eye movement response to earth vertical axis rotation in the dark, a semicircular canal stimulus, can be altered by prior exposure to combined visual-vestibular stimuli. Such plasticity of the vestibulo-ocular reflex has not been described for earth horizontal axis rotation, a dynamic otolith stimulus. Twenty normal human subjects underwent one of two types of adaptation paradigms designed either to attenuate or enhance the gain of the semicircular canal-ocular reflex prior to undergoing otolith-ocular reflex testing with horizontal axis rotation. The adaptation paradigm paired a 0.2 Hz sinusoidal rotation about a vertical axis with a 0.2 Hz optokinetic stripe pattern that was deliberately mismatched in peak velocity. Pre- and post-adaptation horizontal axis rotations were at 60 degrees/s in the dark and produced a modulation in the slow component velocity of nystagmus having a frequency of 0.17 Hz due to putative stimulation of the otolith organs. Results showed that the magnitude of this modulation component response was altered in a manner similar to the alteration in semicircular canal-ocular responses. These results suggest that physiologic alteration of the vestibulo-ocular reflex using deliberately mismatched visual and semicircular canal stimuli induces changes in both canal-ocular and otolith-ocular responses. We postulate, therefore, that central nervous system pathways responsible for controlling the gains of canal-ocular and otolith-ocular reflexes are shared.

Testing otolith function.

Otolithic signals contribute to; (1) perception of orientation and linear motion, (2) generate compensatory eye movements in response to linear acceleration of the head and (3) participate in the co-ordination of movement and balance. Tests of these functions shown to be useful in identifying clinical disorders have been reviewed: (1) Evaluation of orientation to gravity, as estimated by adjustment of the visual vertical, indicates deranged otolith function at a peripheral or central level and the sensitivity of this test can be enhanced by performing estimates during centrifugation on a motorised turntable. Estimation of thresholds of self motion on a parallel swing identifies global reduction or unilateral loss of peripheral function, with central disorders awaiting study. (2) Otolith ocular reflexes to linear head translation can be used to demonstrate overall integrity of peripheral function and reveal central abnormalities. Counter-rolling responses to head roll-tilt and measurements of cyclodeviation of the eyes demonstrate functional asymmetries, with some lateralising value, particularly in central lesions. Global function and asymmetries may also be evaluated by 'head eccentric' rotational testing, which adds a tangential linear acceleration to the angular stimulus. The linear acceleration enhances the canal response by adding an otolith component. (3) Latency and amplitude of surface electro-myography (EMG) responses in the limbs to sudden falls, which can be recorded with the subject suspended on a hinged bed, indicate gross peripheral abnormality of function and can lateralize disorders of CNS motor pathways. It is concluded that some tests of otolith function can be of use in indicating global loss of peripheral otolith function, others are capable of lateralizing a marked loss of function and all have the potential to give information about central disorders. They all have to be interpreted within the clinical context and, unfortunately, none have yet been shown to be sensitive to partial, particularly unilateral, dysfunction.

Optokinetic nystagmus in response to different stimulus modalities

Eye movements were recorded in 42 patients with CNS and labyrinthine lesions during optokinetic (OK) stimulation with a small drum, a full field angular drum and a large linear screen. Gain (slow phase eye velocity/stimulus velocity) and symmetry of the response were measured. In the whole patient group the asymmetry of optokinetic nystagmus (OKN) with the small drum was larger than that elicited with the large field OK stimuli; this indicates that the small drum is a more sensitive stimulus for eliciting abnormal OKN asymmetry (directional preponderance). In some patients with parietal and cerebellar lesions, there was slow build-up of the nystagmic response which was selective to the full field angular OK stimulus. This finding suggests that the ‘old subcortical OKN system, responsible for slow build-up of the response, is specifically related to angular motion. Linear OKN may be coupled to otolith-ocular reflexes.

Upbeat nystagmus: Clinicopathological and pathophysiological considerations

We describe an electro-oculographic study of upbeat nystagmus in 4 patients, with neuropathological correlation in one. All patients had lesions in the pontine tegmentum. The electro-oculographic data may be explained by imbalanced vertical vestibular or smooth pursuit eye movement control. The nystagmus stopped or reversed direction during convergence or in supine head positions. We propose that changes in the intensity or direction of upbeat nystagmus that are induced by convergence or changes in head position, are caused by vertical imbalance in the otolithic-ocular reflex, when superimposed on an imbalanced vestibulo-ocular reflex (VOR). Imbalance of the otolithic-ocular reflex and the vertical VOR are caused by damage in the pontomedullary tegmentum.

Compensatory eye movements in the presence of conflicting canal and otolith signals

Orbital motion of the head with the face directed towards the axis of rotation is a stimulus to the otolith organs which is in the opposite rightwards-left-wards sense to the rotational stimulus to the semicircular canals. This can be experienced, for example, by a child held at arms length "en face' and swung from side to side. As one swings, say to the right, the child's head rotates to its right yet moves linearly to its left. Eye movement responses to a transient orbital movement were observed whilst subjects fixated earth-fixed targets. i) a "near target" placed between the head and the axis whose relative displacement is in the same direction as head rotation, and ii) a "far target" placed beyond the axis whose relative motion is in the opposite direction to head rotation. The motion stimuli evoked slow phase eye movements at 45 ms latency, always in the opposite direction to head rotation, thus compensating for the motion of the far target but in the wrong direction for fixating the near target. Theoretically, fixating the near target demands a predominance of the otolith ocular-reflex, which would give an eye movement in the correct direction. However, despite visual cues, it seems that if the canal and otolith-ocular reflexes are evoked in opposing directions, the otolith reflex fails to operate at a sensitivity sufficiently high to reverse the direction of the canal-reflex.

Objektivierung visueller Wahrnehmungsstörungen nach einseitigem Vestibularisausfall*

Visual ability and compensatory eye movements during defined vertical oscillation were investigated in 20 patients with unilateral lesions of labyrinthine function and in 20 normal subjects. Oscillation frequencies were performed at the rate of 1 to 1.5 Hz with an amplitude of 5 cm, comparative to head locomotions of a running person. In synchronism with this, the visual function was tested with Landolt rings. Patients complaining of subjective visual disturbance during walking and running, also presented a measurable blur of vision under test conditions. In addition, eye movements were recorded and classified into three types. However, these eye movements showed no relation to gaze function. Our results suggest that the otolith-ocular reflex may participate in adjusting the vertical eye position during vertical stimulations at low frequencies. The effect of visual disturbances in patients with labyrinthine lesions is explained by the "efference-copy" initially described by von Holst. The efference-copy is responsible for the neutralisation of provoked retinal perceptions.

Primary Position Upbeat Nystagmus:Clinicopathologic Study of Four Patients

We report an electro-oculographic study (EOG) of upbeat nystagmus and neuroradiological correlations in 4 patients and neuropathological findings in 1 patient. All 4 patients revealed responsible lesions in the lower pontine tegmentum. The EOG data suggest that our patients had a deficit in vertical smooth eye movement balance. The nystagmus stopped or reversed direction during convergence or changes of head position. These EOG findings might be caused by vertical imbalance in the otolithic ocular reflex, superimposed on an imbalanced vestibulo-ocular reflex (VOR), secondary to a damage to the pontomedullary tegmentum.

Influence of Gravity Vector on Eye Movement Elicited by Linear Acceleration

When the body/head motion is sensed by otolith organs, they respond not only to the resultant acceleration of the motion but also to the gravitational force. We investigated the influence of the gravity vector on the otolithic-ocular reflex caused by motion in normal subjects. The sled type linear accelerator, moving back and forth with a frequency of 0.25 Hz and an amplitude of 2 m, generated right-left linear acceleration with a maximum magnitude of 0.5 g. We tested every subject under seven different postures: 1) 135 degrees forward tilted (F.T.), 2) 90 degrees F.T., 3) 45 degrees F.T., 4) upright sitting, 5) 45 degrees backward tilted (B.T.), 6) 90 degrees B.T., and 7) 135 degrees B.T. Horizontal eye movements with nystagmic pattern were elicited by these stimulations and were recorded by EOG. The eye movement data were analyzed by using a computer with the following procedure. After extraction of saccadic components from the data, the remaining parts were connected smoothly. The waves reconstructed in this manner, considered to be primary otolithic-ocular responses, were processed with the FFT method for calculating the amplitude of the component at 0.25 Hz. As a result, the responses were larger in the forward tilted postures than in the backward tilted postures.

Congenital ocular motor apraxia: a neurodevelopmental and neuroradiological study

Upbeating nystagmus has been described in lesions of the posterior fossa. We report a case of upbeating nystagmus accompanying a focal hemorrhagic lesion of the left brachium conjunctivum, the anterior vermis, and the anterior superior left cerebellar hemisphere. The nystagmus was suppressed by a contralateral head tilt. We postulate that in this instance, acquired central nystagmus was inhibited by the otolith-ocular reflex.

Recovery of the Otolith-ocular Reflex after Unilateral Deafferentation of the Otolith Organs in Squirrel Monkeys

The enhancement of the vestibulo-ocular reflex (VOR) gain in the eccentric rotation is mediated by the otolith organs. Functional recovery of the otolith-ocular reflex after deafferentation of the otolith organs was examined in squirrel monkeys, using the enhancement of the eccentric VOR gain as an indicator of the reflex. After unilateral deafferentation of the otolith organs, the enhancement of the eccentric VOR gain decreased and then recovered completely within eight weeks. However, the eccentric VOR gain was not enhanced after contralateral side lesions. These findings demonstrate that functional recovery of the otolith-ocular reflex is achieved after unilateral deafferentation of the otolith organs, and that afferents from the remaining otolith organs are necessary for the functional compensation.

VESTIBULAR FUNCTION IN PERIODIC ALTERNATING NYSTAGMUS

The vestibulo-ocular reflex of 4 patients with periodic alternating nystagmus (PAN) was studied in detail. Rotational testing was used to investigate the horizontal semicircular canal-ocular reflex, canal-otolith interaction, and the dynamic otolith-ocular reflex. Results indicated abnormal gain and phase of the horizontal semicircular canal-ocular reflex during sinusoidal rotation and a variable rate of decay of postrotatory responses. Each patient had abnormal canal-otolith interaction. An enlarged modulation component of the dynamic otolith-ocular response was observed in each patient. This study supports the idea that PAN is caused by an instability in the velocity storage element, a hypothetical neural circuit that perseverates the eye movement response to both vestibular and optokinetic stimulation. Further, we postulate that PAN may be caused by lesions of the cerebellar uvula and nodulus or their connections with the brainstem vestibular nuclei.

Contribution of the otoliths to the calculation of linear displacement.

1. The present work is a quantitative study of the eye movements induced by linear translation when the subject is instructed to stabilize his gaze on a memorized earth-fixed target. These experiments may allow a better understanding of the central processing of otolithic signals. 2. Human subjects were submitted to either sinusoidal or step-like horizontal linear displacements along the interaural (Y)-axis in darkness, seated in a cart moving along a linear track. Each subject's head was fixed by a helmet secured to the cart. They were asked to keep their eyes on an earth-fixed memorized target at 63 cm from them on the X-axis. 3. During sinusoidal motion, a combination of low smooth compensatory eye movements and of compensatory saccades allowed the subjects to track the memorized target. The linear model of the responses of five subjects (seven sessions) exhibited a near-ideal slope of 1.14 (range 0.84-1.58). Two subjects did not compensate properly for their displacement. The mean "vestibular-saccadic" (VS) gain (ratio of overall eye movement peak-peak amplitude versus head displacement amplitude) was 1.52 +/- 0.80 (SD), showing an overestimation of head displacement. 4. The otolith-ocular reflex (OOR) mean gain values (ratio of slow phase cumulated peak-peak amplitude versus head displacement amplitude) were about 0.13 degrees/cm. This value is 5 times higher than what has been reported in the literature, probably due to the fact that the target was at a short distance. 5. The number of saccades occurring during sinusoidal stimulations varied according to the different subjects. They were obviously compensatory saccades and not quick phases. They indicate that although the gain of the OOR was small, the brain has computed the adequate desired eye position. 6. During steplike head displacements in darkness, although the OOR gain was also small, seven of the eight subjects could stabilize their gaze with a mean VS gain of 1.01 +/- 0.70. The linear model for the pooled responses of these subjects exhibited a slope of 0.82. 7. When subjects were instructed not to move their eyes during the translation, three of the five examined could still correctly reproduce the head movement amplitude with saccades, even as late as 50 s after motion had stopped. This indicates that head displacement was stored with the adequate metrics and could be used to drive the saccadic system. 8. Bilabyrinthectomized patients could not perform any adequate gaze stabilization. This shows that the observed performance was of vestibular origin.

Earth horizontal axis rotational responses in patients with unilateral peripheral vestibular deficits.

We evaluated the vestibulo-ocular reflex (VOR) of five patients with surgically confirmed unilateral peripheral vestibular lesions. Testing used both earth vertical axis (EVA) and earth horizontal axis (EHA) yaw rotation. Results indicated that the patients had short VOR time constants, asymmetric responses to both EVA and EHA rotation, and normal EHA modulation components. These findings suggest that unilateral peripheral vestibular loss causes a shortened VOR time constant even with the addition of dynamic otolithic stimulation and causes an asymmetry in semicircular canal-ocular reflexes and one aspect of otolith-ocular reflexes.

Counter-rolling after regional destruction of the saccule by laser spot irradiation in the guinea pig.

Destruction of the anterior one-third of the right saccule in the guinea pig resulted in a marked eye deviation simultaneously towards the ear and downward on the operated side and a marked upward eye deviation on the non-operated side in the standard head position. During head inclination towards the operated side, both eyes showed a disturbed ocular counter-rolling (OCR). The disturbance of OCR was more severe in the eye on the operated side than in the eye on the non-operated side. Brief interpretation about eye position in the standard head position in the regional destructive group showed that the eye ball on the operated side showed a marked deviation simultaneously upward and towards the ear, while the eye ball on the non-operated side showed an upward deviation on the 1st and 3rd days after the operation. OCR after regional destruction was seen as follows: During head inclination towards the operated side, both eyes showed disturbed OCR. The disturbance of OCR was more severe in the eye on the operated side. Most animals in our experiment showed this disturbed OCR which was compensated and normalized by the third postoperative week; relatively shorter (faster) than the total destruction. These results suggest that when the head is inclined around its longer axis, the saccule on the side of head inclination plays a principal role in the otolith-ocular reflex.

Nystagmus responses in a group of normal humans during earth-horizontal axis rotation.

Horizontal eye movement responses to earth-horizontal yaw axis rotation were evaluated in 50 normal human subjects who were uniformly distributed in age (20-69 years) and equally divided by gender for each decade. The subjects were rotated with eyes open in the dark, using clockwise and counterclockwise 60 degree/s velocity trapezoids. The nystagmus slow component velocity (SCV) was analysed using four parameters: Amp, Bias, Mod and Tau. Amp and Tau characterize the canal-ocular reflex to constant velocity steps, while Mod and Bias characterize the "AC" and "DC" components of the otolith-ocular reflex. Results indicated that intersubject variability was larger than that seen in earth-vertical axis data. Tau depended significantly (p less than 0.05) upon subject gender, while Mod increased monotonically with age decade. Linear regression showed a positive correlation between pairs of SCV magnitude parameters (Amp, Bias and Mod), suggesting a common scaling effect. In addition, there was a negative correlation between the value of the decay time constant Tau and each of the three magnitude parameters. Thus, despite large intersubject variability, parameters that describe earth-horizontal yaw axis responses are loosely interrelated and some of them vary significantly with gender and age.