Eye movement deficits following ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys II. Pursuit, vestibular, and optokinetic responses.
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The eyes are moved by a combination of neural commands that code eye velocity and eye position. The eye position signal is supposed to be derived from velocity-coded command signals by mathematical integration via a single oculomotor neural integrator. For horizontal eye movements, the neural integrator is thought to reside in the rostral nucleus prepositus hypoglossi (nph) and project directly to the abducens nuclei. In a previous study, permanent, serial ibotenic acid lesions of the nph in three rhesus macaques compromised the neural integrator for fixation but saccades were not affected. In the present study, to determine further whether the nph is the neural substrate for a single oculomotor neural integrator, the effects of those lesions on smooth pursuit, the vestibulo-ocular reflex (VOR), vestibular nystagmus (VN), and optokinetic nystagmus (OKN) are documented. The lesions were correlated with long-lasting deficits in eye movements, indicated most clearly by the animals' inability to maintain steady gaze in the dark. However, smooth pursuit and sinusoidal VOR in the dark, like the saccades in the previous study, were affected minimally. The gain of horizontal smooth pursuit (eye movement/target movement) decreased slightly (<25%) and phase lead increased slightly for all frequencies (0.3-1.0 Hz, +/-10 degrees target tracking), most noticeably for higher frequencies (0.8-0.7 and approximately 20 degrees for 1.0-Hz tracking). Vertical smooth pursuit was not affected significantly. Surprisingly, horizontal sinusoidal VOR gain and phase also were not affected significantly. Lesions had complex effects on both VN and OKN. The plateau of per- and postrotatory VN was shortened substantially ( approximately 50%), whereas the initial response and the time constant of decay decreased slightly. The initial OKN response also decreased slightly, and the charging phase was prolonged transiently then recovered to below normal levels like the VN time constant. Maximum steady-state, slow eye velocity of OKN decreased progressively by approximately 30% over the course of the lesions. These results support the previous conclusion that the oculomotor neural integrator is not a single neural entity and that the mathematical integrative function for different oculomotor subsystems is most likely distributed among a number of nuclei. They also show that the nph apparently is not involved in integrating smooth pursuit signals and that lesions of the nph can fractionate the VOR and nystagmic responses to adequate stimuli. (+info)
Short-latency vergence eye movements induced by radial optic flow in humans: dependence on ambient vergence level.
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Radial patterns of optic flow, such as those experienced by moving observers who look in the direction of heading, evoke vergence eye movements at short latency. We have investigated the dependence of these responses on the ambient vergence level. Human subjects faced a large tangent screen onto which two identical random-dot patterns were back-projected. A system of crossed polarizers ensured that each eye saw only one of the patterns, with mirror galvanometers to control the horizontal positions of the images and hence the vergence angle between the two eyes. After converging the subject's eyes at one of several distances ranging from 16.7 cm to infinity, both patterns were replaced with new ones (using a system of shutters and two additional projectors) so as to simulate the radial flow associated with a sudden 4% change in viewing distance with the focus of expansion/contraction imaged in or very near both foveas. Radial-flow steps induced transient vergence at latencies of 80-100 ms, expansions causing increases in convergence and contractions the converse. Based on the change in vergence 90-140 ms after the onset of the steps, responses were proportional to the preexisting vergence angle (and hence would be expected to be inversely proportional to viewing distance under normal conditions). We suggest that this property assists the observer who wants to fixate ahead while passing through a visually cluttered area (e.g., a forest) and so wants to avoid making vergence responses to the optic flow created by the nearby objects in the periphery. (+info)
Short- and long-term consequences of canal plugging on gaze shifts in the rhesus monkey. I. Effects on gaze stabilization.
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Short- and long-term consequences of canal plugging on gaze shifts in the rhesus monkey. I. Effects on gaze stabilization. To study the contribution of the vestibular system to the coordinated eye and head movements of a gaze shift, we plugged the lumens of just the horizontal (n = 2) or all six semicircular canals (n = 1) in monkeys trained to make horizontal head-unrestrained gaze shifts to visual targets. After the initial eye saccade of a gaze shift, normal monkeys exhibit a compensatory eye counterrotation that stabilizes gaze as the head movement continues. This counterrotation, which has a gain (eye velocity/head velocity) near one has been attributed to the vestibuloocular reflex (VOR). One day after horizontal canal plugging, the gain of the passive horizontal VOR at frequencies between 0.1 and 1.0 Hz was <0.10 in the horizontal-canal-plugged animals and zero in the all-canal-plugged animal. One day after surgery, counterrotation gain was approximately 0.3 in the animals with horizontal canals plugged and absent in the animal with all canals plugged. As the time after plugging increased, so too did counterrotation gain. In all three animals, counterrotation gain recovered to between 0.56 and 0.75 within 80-100 days. The initial loss of compensatory counterrotation after plugging resulted in a gaze shift that ended long after the eye saccade and just before the end of the head movement. With recovery, the length of time between the end of the eye saccade and the end of the gaze movement decreased. This shortening of the duration of reduced gain counterrotation occurred both because head movements ended sooner and counterrotation gain returned to 1.0 more rapidly relative to the end of the eye saccade. Eye counterrotation was not due to activation of pursuit eye movements as it persisted when gaze shifts were executed to extinguished targets. Also counterrotation was not due simply to activation of neck receptors because counterrotation persisted after head movements were arrested in midflight. We suggest that the neural signal that is used to cause counterrotation in the absence of vestibular input is an internal copy of the intended head movement. (+info)
Effects of tilt of the gravito-inertial acceleration vector on the angular vestibuloocular reflex during centrifugation.
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Effects of tilt of the gravito-inertial acceleration vector on the angular vestibuloocular reflex during centrifugation. Interaction of the horizontal linear and angular vestibuloocular reflexes (lVOR and aVOR) was studied in rhesus and cynomolgus monkeys during centered rotation and off-center rotation at a constant velocity (centrifugation). During centered rotation, the eye velocity vector was aligned with the axis of rotation, which was coincident with the direction of gravity. Facing and back to motion centrifugation tilted the resultant of gravity and linear acceleration, gravito-inertial acceleration (GIA), inducing cross-coupled vertical components of eye velocity. These components were upward when facing motion and downward when back to motion and caused the axis of eye velocity to reorient from alignment with the body yaw axis toward the tilted GIA. A major finding was that horizontal time constants were asymmetric in each monkey, generally being longer when associated with downward than upward cross coupling. Because of these asymmetries, accurate estimates of the contribution of the horizontal lVOR could not be obtained by simply subtracting horizontal eye velocity profiles during facing and back to motion centrifugation. Instead, it was necessary to consider the effects of GIA tilts on velocity storage before attempting to estimate the horizontal lVOR. In each monkey, the horizontal time constant of optokinetic after-nystagmus (OKAN) was reduced as a function of increasing head tilt with respect to gravity. When variations in horizontal time constant as a function of GIA tilt were included in the aVOR model, the rising and falling phases of horizontal eye velocity during facing and back to motion centrifugation were closely predicted, and the estimated contribution of the compensatory lVOR was negligible. Beating fields of horizontal eye position were unaffected by the presence or magnitude of linear acceleration during centrifugation. These conclusions were evaluated in animals in which the low-frequency aVOR was abolished by canal plugging, isolating the contribution of the lVOR. Postoperatively, the animals had normal ocular counterrolling and horizontal eye velocity modulation during off-vertical axis rotation (OVAR), suggesting that the otoliths were intact. No measurable horizontal eye velocity was elicited by centrifugation with angular accelerations +info)
Vertical eye position-dependence of the human vestibuloocular reflex during passive and active yaw head rotations.
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Vertical eye position-dependence of the human vestibuloocular reflex during passive and active yaw head rotations. The effect of vertical eye-in-head position on the compensatory eye rotation response to passive and active high acceleration yaw head rotations was examined in eight normal human subjects. The stimuli consisted of brief, low amplitude (15-25 degrees ), high acceleration (4,000-6,000 degrees /s2) yaw head rotations with respect to the trunk (peak velocity was 150-350 degrees /s). Eye and head rotations were recorded in three-dimensional space using the magnetic search coil technique. The input-output kinematics of the three-dimensional vestibuloocular reflex (VOR) were assessed by finding the difference between the inverted eye velocity vector and the head velocity vector (both referenced to a head-fixed coordinate system) as a time series. During passive head impulses, the head and eye velocity axes aligned well with each other for the first 47 ms after the onset of the stimulus, regardless of vertical eye-in-head position. After the initial 47-ms period, the degree of alignment of the eye and head velocity axes was modulated by vertical eye-in-head position. When fixation was on a target 20 degrees up, the eye and head velocity axes remained well aligned with each other. However, when fixation was on targets at 0 and 20 degrees down, the eye velocity axis tilted forward relative to the head velocity axis. During active head impulses, the axis tilt became apparent within 5 ms of the onset of the stimulus. When fixation was on a target at 0 degrees, the velocity axes remained well aligned with each other. When fixation was on a target 20 degrees up, the eye velocity axis tilted backward, when fixation was on a target 20 degrees down, the eye velocity axis tilted forward. The findings show that the VOR compensates very well for head motion in the early part of the response to unpredictable high acceleration stimuli-the eye position- dependence of the VOR does not become apparent until 47 ms after the onset of the stimulus. In contrast, the response to active high acceleration stimuli shows eye position-dependence from within 5 ms of the onset of the stimulus. A model using a VOR-Listing's law compromise strategy did not accurately predict the patterns observed in the data, raising questions about how the eye position-dependence of the VOR is generated. We suggest, in view of recent findings, that the phenomenon could arise due to the effects of fibromuscular pulleys on the functional pulling directions of the rectus muscles. (+info)
Effects of viewing distance on the responses of horizontal canal-related secondary vestibular neurons during angular head rotation.
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Effects of viewing distance on the responses of horizontal canal-related secondary vestibular neurons during angular head rotation. The eye movements generated by the horizontal canal-related angular vestibuloocular reflex (AVOR) depend on the distance of the image from the head and the axis of head rotation. The effects of viewing distance on the responses of 105 horizontal canal-related central vestibular neurons were examined in two squirrel monkeys that were trained to fixate small, earth-stationary targets at different distances (10 and 150 cm) from their eyes. The majority of these cells (77/105) were identified as secondary vestibular neurons by synaptic activation following electrical stimulation of the vestibular nerve. All of the viewing distance-sensitive units were also sensitive to eye movements in the absence of head movements. Some classes of eye movement-related vestibular units were more sensitive to viewing distance than others. For example, the average increase in rotational gain (discharge rate/head velocity) of position-vestibular-pause units was 20%, whereas the gain increase of eye-head-velocity units was 44%. The concomitant change in gain of the AVOR was 11%. Near viewing responses of units phase lagged the responses they generated during far target viewing by 6-25 degrees. A similar phase lag was not observed in either the near AVOR eye movements or in the firing behavior of burst-position units in the vestibular nuclei whose firing behavior was only related to eye movements. The viewing distance-related increase in the evoked eye movements and in the rotational gain of all unit classes declined progressively as stimulus frequency increased from 0.7 to 4.0 Hz. When monkeys canceled their VOR by fixating head-stationary targets, the responses recorded during near and far target viewing were comparable. However, the viewing distance-related response changes exhibited by central units were not directly attributable to the eye movement signals they generated. Subtraction of static eye position signals reduced, but did not abolish viewing distance gain changes in most units. Smooth pursuit eye velocity sensitivity and viewing distance sensitivity were not well correlated. We conclude that the central premotor pathways that mediate the AVOR also mediate viewing distance-related changes in the reflex. Because irregular vestibular nerve afferents are necessary for viewing distance-related gain changes in the AVOR, we suggest that a central estimate of viewing distance is used to parametrically modify vestibular afferent inputs to secondary vestibuloocular reflex pathways. (+info)
Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation.
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Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation. The firing behavior of 59 horizontal canal-related secondary vestibular neurons was studied in alert squirrel monkeys during the combined angular and linear vestibuloocular reflex (CVOR). The CVOR was evoked by positioning the animal's head 20 cm in front of, or behind, the axis of rotation during whole body rotation (0.7, 1.9, and 4.0 Hz). The effect of viewing distance was studied by having the monkeys fixate small targets that were either near (10 cm) or far (1.3-1.7 m) from the eyes. Most units (50/59) were sensitive to eye movements and were monosynaptically activated after electrical stimulation of the vestibular nerve (51/56 tested). The responses of eye movement-related units were significantly affected by viewing distance. The viewing distance-related change in response gain of many eye-head-velocity and burst-position units was comparable with the change in eye movement gain. On the other hand, position-vestibular-pause units were approximately half as sensitive to changes in viewing distance as were eye movements. The sensitivity of units to the linear vestibuloocular reflex (LVOR) was estimated by subtraction of angular vestibuloocular reflex (AVOR)-related responses recorded with the head in the center of the axis of rotation from CVOR responses. During far target viewing, unit sensitivity to linear translation was small, but during near target viewing the firing rate of many units was strongly modulated. The LVOR responses and viewing distance-related LVOR responses of most units were nearly in phase with linear head velocity. The signals generated by secondary vestibular units during voluntary cancellation of the AVOR and CVOR were comparable. However, unit sensitivity to linear translation and angular rotation were not well correlated either during far or near target viewing. Unit LVOR responses were also not well correlated with their sensitivity to smooth pursuit eye movements or their sensitivity to viewing distance during the AVOR. On the other hand there was a significant correlation between static eye position sensitivity and sensitivity to viewing distance. We conclude that secondary horizontal canal-related vestibuloocular pathways are an important part of the premotor neural substrate that produces the LVOR. The otolith sensory signals that appear on these pathways have been spatially and temporally transformed to match the angular eye movement commands required to stabilize images at different distances. We suggest that this transformation may be performed by the circuits related to temporal integration of the LVOR. (+info)
Influence of gaze rotation on the visual response of primate MSTd neurons.
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When we move forward, the visual image on our retina expands. Humans rely on the focus, or center, of this expansion to estimate their direction of heading and, as long as the eyes are still, the retinal focus corresponds to the heading. However, smooth rotation of the eyes adds nearly uniform visual motion to the expanding retinal image and causes a displacement of the retinal focus. In spite of this, humans accurately judge their heading during pursuit eye movements and during active, smooth head rotations even though the retinal focus no longer corresponds to the heading. Recent studies in macaque suggest that correction for pursuit may occur in the dorsal aspect of the medial superior temporal area (MSTd) because these neurons are tuned to the retinal position of the focus and they modify their tuning during pursuit to compensate partially for the focus shift. However, the question remains whether these neurons also shift focus tuning to compensate for smooth head rotations that commonly occur during gaze tracking. To investigate this question, we recorded from 80 MSTd neurons while monkeys tracked a visual target either by pursuing with their eyes or by vestibulo-ocular reflex cancellation (VORC; whole-body rotation with eyes fixed in head and head fixed on body). VORC is a passive, smooth head rotation condition that selectively activates the vestibular canals. We found that neurons shift their focus tuning in a similar way whether focus displacement is caused by pursuit or by VORC. Across the population, compensation averaged 88 and 77% during pursuit and VORC, respectively (tuning shift divided by the retinal focus to true heading difference). Moreover the degree of compensation during pursuit and VORC was correlated in individual cells (P < 0.001). Finally neurons that did not compensate appreciably tended to be gain-modulated during pursuit and VORC and may constitute an intermediate stage in the compensation process. These results indicate that many MSTd cells compensate for general gaze rotation, whether produced by eye-in-head or head-in-world rotation, and further implicate MSTd as a critical stage in the computation of heading. Interestingly vestibular cues present during VORC allow many cells to compensate even though humans do not accurately judge their heading in this condition. This suggests that MSTd may use vestibular information to create a compensated heading representation within at least a subpopulation of cells, which is accessed perceptually only when additional cues related to active head rotations are also present. (+info)