F. A. Miles

Vergence eye movements in response to binocular disparity without depth perception

Primates use vergence eye movements to align their two eyes on the same object and can correct misalignments by sensing the difference in the positions of the two retinal images of the object (binocular disparity). When large random-dot patterns are viewed dichoptically and small binocular misalignments are suddenly imposed (disparity steps), corrective vergence eye movements are elicited at ultrashort latencies. Here we show that the same steps applied to dense anticorrelated patterns, in which each black dot in one eye is matched to a white dot in the other eye, initiate vergence responses that are very similar, except that they are in the opposite direction. This sensitivity to the disparity of anticorrelated patterns is shared by many disparity-selective neurons in cortical area V1 (ref. 3), despite the fact that human subjects fail to perceive depth in such stimuli. These dataindicate that the vergence eye movements initiated at ultrashort latencies result solely from locally matched binocular features, and derive their visual input from an early stage of cortical processing before the level at which depth percepts are elaborated.

Short latency ocular-following responses in man.

The ocular-following responses elicited by brief unexpected movements of the visual scene were studied in human subjects. Response latencies varied with the type of stimulus and decreased systematically with increasing stimulus speed but, unlike those of monkeys, were not solely determined by the temporal frequency generated by sine-wave stimuli. Minimum latencies (70-75 ms) were considerably shorter than those reported for other visually driven eye movements. The magnitude of the responses to sine-wave stimuli changed markedly with stimulus speed and only slightly with spatial frequency over the ranges used. When normalized with respect to spatial frequency, all responses shared the same dependence on temporal frequency (band-pass characteristics with a peak at 16 Hz), indicating that temporal frequency, rather than speed per se, was the limiting factor over the entire range examined. This suggests that the underlying motion detectors respond to the local changes in luminance associated with the motion of the scene. Movements of the scene in the immediate wake of a saccadic eye movement were on average twice as effective as movements 600 ms later: post-saccadic enhancement. Less enhancement was seen in the wake of saccade-like shifts of the scene, which themselves elicited weak ocular following, something not seen in the wake of real saccades. We suggest that there are central mechanisms that, on the one hand, prevent the ocular-following system from tracking the visual disturbances created by saccades but, on the other, promote tracking of any subsequent disturbance and thereby help to suppress post-saccadic drift. Partitioning the visual scene into central and peripheral regions revealed that motion in the periphery can exert a weak modulatory influence on ocular-following responses resulting from motion at the center. We suggest that this may help the moving observer to stabilize his/her eyes on nearby stationary objects.

Human ocular responses to translation of the observer and of the scene: dependence on viewing distance

Recent experiments on monkeys have indicated that the eye movements induced by brief translation of either the observer or the visual scene are a linear function of the inverse of the viewing distance. For the movements of the observer, the room was dark and responses were attributed to a translational vestibulo-ocular reflex (TVOR) that senses the motion through the otolith organs; for the movements of the scene, which elicit ocular following, the scene was projected and adjusted in size and speed so that the retinal stimulation was the same at all distances. The shared dependence on viewing distance was consistent with the hypothesis that the TVOR and ocular following are synergistic and share central pathways. The present experiments looked for such dependencies on viewing distance in human subjects. When briefly accelerated along the interaural axis in the dark, human subjects generated compensatory eye movements that were also a linear function of the inverse of the viewing distance to a previously fixated target. These responses, which were attributed to the TVOR, were somewhat weaker than those previously recorded from monkeys using similar methods. When human subjects faced a tangent screen onto which patterned images were projected, brief motion of those images evoked ocular following responses that showed statistically significant dependence on viewing distance only with low-speed stimuli (10°/s). This dependence was at best weak and in the reverse direction of that seen with the TVOR, i.e., responses increased as viewing distance increased. We suggest that in generating an internal estimate of viewing distance subjects may have used a confounding cue in the ocular-following paradigm the size of the projected scene -which was varied directly with the viewing distance in these experiments (in order to preserve the size of the retinal image). When movements of the subject were randomly interleaved with the movements of the scene to encourage the expectation of ego-motion -the dependence of ocular following on viewing distance altered significantly: with higher speed stimuli (40°/s) many responses (63%) now increased significantly as viewing distance decreased, though less vigorously than the TVOR. We suggest that the expectation of motion results in the subject placing greater weight on cues such as vergence and accommodation that provide veridical distance information in our experimental situation: cue selection is context specific.

Radial optic flow induces vergence eye movements with ultra-short latencies

An observer moving forwards through the environment experiences a radial pattern of image motion on each retina. Such patterns of optic flow are a potential source of information about the observers rate of progress, direction of heading and time to reach objects that lie ahead. As the viewing distance changes there must be changes in the vergence angle between the two eyes so that both foveas remain aligned on the object of interest in the scene ahead. Here we show that radial optic flow can elicit appropriately directed (horizontal) vergence eye movements with ultra-short latencies (roughly 80 ms) in human subjects. Centrifugal flow, signalling forwards motion, increases the vergence angle, whereas centripetal flow decreases the vergence angle. These vergence eye movements are still evident when the observers view of the flow pattern is restricted to the temporal hemifield of one eye, indicating that these responses do not result from anisotropies in motion processing but from a mechanism that senses the radial pattern of flow. We hypothesize that flow-induced vergence is but one of a family of rapid ocular reflexes, mediated by the medial superior temporal cortex, compensating for translational disturbance of the observer.

Floccular lesions abolish adaptive control of post-saccadic ocular drift in primates

SummaryAfter several days of exposure to optically-imposed post-saccadic retinal slip, the saccades of normal monkeys acquire an exponential ocular drift. This drift is in the direction of the imposed image motion, and persists in the dark. It has been argued that these changes result from the operation of a visually mediated adaptive mechanism that normally functions to minimize post-saccadic ocular drift. Adaptation to persistent post-saccadic retinal slip was assessed in two rhesus monkeys before and after bilateral ablations of the flocculi and portions of the paraflocculi (“flocculectomy”). After flocculectomy, both monkeys showed some post-saccadic ocular drift. Flocculectomized animals also failed to adapt to optically-imposed post-saccadic slip. We infer from this that the flocculi and/or paraflocculi are necessary for the successful suppression of postsaccadic ocular drift.

Deficits in Short-Latency Tracking Eye Movements after Chemical Lesions in Monkey Cortical Areas MT and MST

Past work has suggested that the medial superior temporal area (MST) is involved in the initiation of three kinds of eye movements at short latency by large-field visual stimuli. These eye movements consist of (1) version elicited by linear motion (the ocular following response), (2) vergence elicited by binocular parallax (the disparity vergence response), and (3) vergence elicited by global motion toward or away from the fovea (the radial-flow vergence response). We investigated this hypothesis by recording the effects of ibotenic acid injections in the superior temporal sulcus (STS) of both hemispheres in five monkeys. After the injections, all three kinds of eye movements were significantly impaired, with the magnitude of the impairments often showing a strong correlation with the extent of the morphological damage in the three subregions of the STS: dorsal MST on the anterior bank, lateral MST and middle temporal area on the posterior bank. However, the extent of the lesions in the three subregions often covaried, rendering it difficult to assess their relative contributions to the various deficits. The effects of the lesions on other aspects of oculomotor behavior that are known to be important for the normal functioning of the three tracking mechanisms (e.g., ocular stability, fixation disparity) were judged to be generally minor and to contribute little to the impairments. We conclude that, insofar as MST sustained significant damage in all injected hemispheres, our findings are consistent with the hypothesis that MST is a primary site for initiating all three visual tracking eye movements at ultra-short latencies.

Short-latency compensatory eye movements associated with a brief period of free fall

The vertical eye movements induced by a brief period of free fall were recorded from three monkeys (Macaca mulatta) using the electromagnetic search coil technique. Free fall was initiated in total darkness immediately following binocular fixation of one of six target lights located at viewing distances ranging from 20 to 107 cm. Responses consisted of an initial transient downward eye movement (anticompensatory direction) with a latency of a few milliseconds at most followed by a sustained upward (compensatory) eye movement. The early transient was independent of viewing distance and attributed to an artifact, whereas the later component was a linear function of the inverse of the prior viewing distance and attributed to the translational vestibulo-ocular reflex (TVOR). Response latencies for the four nearer viewing distances were determined from the individual eye velocity traces using a computerized algorithm: after removing the initial transient by subtracting the mean response obtained with the most distant viewing, a regression line was fitted to the initial rising phase of the residual response and then extrapolated back to the baseline to determine the onset. When so determined, median latencies for the nearest viewing ranged from 16.4 to 18.5 ms, values appreciably shorter than any in the literature.

Changes in the coupling between accommodation and vergence eye movements induced in human subjects by altering the effective interocular separation.

It has usually been thought that the coupling between accommodation and convergence of the eyes is fixed and not modifiable by experience. Experiments are reported which show that the ratio of accommodative vergence to the accommodation stimulus, the stimulus AC/A ratio (one measure of the coupling), is elevated by brief periods (∼30 min) of experience of viewing the world through periscopic spectacles which increase the effective interocular separation. Experience of viewing through ‘cyclopean’ spectacles, which superimpose the line of sight of the two eyes, reduced the stimulus AC/A ratio in one subject and increased it in another, while it remained hardly affected in a third.

Short-latency ocular following in humans: sensitivity to binocular disparity

We show that the initial ocular following responses elicited by motion of a large pattern are modestly attenuated when that pattern is shifted out of the plane of fixation by altering its binocular disparity. If the motion is applied to only restricted regions of the pattern, however, then altering the disparity of those regions severely attenuates their ability to generate ocular following. This sensitivity of the ocular tracking mechanism to local binocular disparity would help the observer who moves through a cluttered 3-D world to stabilize objects in the plane of fixation and ignore all others.

Visual stabilization of the eyes in primates.

Observers moving through a textured three-dimensional world experience potentially confusing patterns of optic flow. Recent experiments on monkeys and humans have revealed the existence of rapid, yet cortically mediated, reflex eye movements that automatically single out images in the plane of fixation for stabilization and ignore images that are nearer or further.