Visual motion integration for perception and pursuit

To examine the relationship between visual motion processing for perception and pursuit, we measured the pursuit eye-movement and perceptual responses to the same complex-motion stimuli. We show that humans can both perceive and pursue the motion of line-figure objects, even when partial occlusion makes the resulting image motion vastly different from the underlying object motion. Our results show that both perception and pursuit can perform largely accurate motion integration, i.e. the selective combination of local motion signals across the visual field to derive global object motion. Furthermore, because we manipulated perceived motion while keeping image motion identical, the observed parallel changes in perception and pursuit show that the motion signals driving steady-state pursuit and perception are linked. These findings disprove current pursuit models whose control strategy is to minimize retinal image motion, and suggest a new framework for the interplay between visual cortex and cerebellum in visuomotor control.     

Adaptation in motion perception: Alteration of motion evoked by ocular pursuit

A new perceptual adaptation, an alteration in the perceived direction of motion given by ocular pursuit, is reported. When an object starts to move on a straight path, its displacement is initially given by a shift of its image on the retinas of the stationary eyes; then, after about 200 msec, the eyes start to track the moving object. The perception of motion that results from ocular pursuit was altered by causing ocular pursuit of a moving object to be preceded regularly by a displacement of the object’s image whose direction differed from the direction of the pursuit movement. This was arranged by changing the direction of the given motion at approximately the moment when image displacement changed into tracking. Prolonged exposure to such conditions resulted in a change of the tracked motion’s apparent direction, which became somewhat more like the direction of the preceding motion phase that was given by image displacement.     

The nature of adaptation in distance perception based on oculomotor cues

In previous work by the senior authors, brief adaptation to glasses that changed the accommodation and convergence with which objects were seen resulted in large alterations in size perception. Here, two further effects of such adaptation are reported: alterations in stereoscopic depth perception and a change when distance is represented by a response of S’s arm. We believe that the three effects are manifestations of one primary effect, an alteration of the relation between accommodation and convergence on the one hand and the distance they represent in the nervous system (registered distance) on the other. This view was supported by the results of two experiments, each of which demonstrated that the alterations in stereoscopic depth perception could be obtained after adaptation periods which had provided no opportunity to use stereoscopic vision, and that the adaptation effect was larger for depth perception than for size perception when it was obtained under the same conditions; the latter finding was expected if both effects resulted from the same change in registered distance. In three of the five experiments here reported, the variety of cues that could represent veridical distance during the adaptation period was limited. In one condition of adaptation, only the pattern of growth of the retinal images of objects that S approached and the kinesthetic cues for S’s locomotion served as cues to veridical distance. In two other conditions S remained immobile. In one of these, only the perspective distortion in the projection of the scene that S viewed mediated veridical distance, and in the other one familiar objects of normal size were successively illuminated in an otherwise totally dark field, conditions from which opportunities to use stereoscopic vision were again absent. After exposure to each of these adaptation conditions, adaptive changes in perceived size and larger ones in perceived stereoscopic depth were obtained. Because we found that familiar size may serve as the sole indicator of veridical distance in an adaptation process, we concluded that it can function as a perceptual as distinguished from an inferential cue to distance.     

Eye muscle potentiation does not account for adaptation in distance perception based on oculomotor cues

Ebenholtz and Wolfson have demonstrated an aftereffect of sustained ocular convergence, which they ascribed to eye muscle potentiation. They suggested that this effect can explain an aftereffect of wearing glasses that alter oculomotor cues for distance. Wallach and Frey interpreted this aftereffect as resulting from adaptation. The outcome of two experiments designed to test Ebenholtz and Wolfson’s explanation and a review of previous experiments on adaptation in distance perception based on oculomotor cues show that this explanation is untenable.     

Quantification and analysis of saccadic and smooth pursuit eye movements and fixations to detect oculomotor deficits

Assessment of deficits in oculomotor function may be useful to detect visuomotor impairments due to a closed head injury. Systematic analysis schemes are needed to reliably quantify oculomotor deficits associated with oculomotor impairment via brain trauma. We propose a systematic, automated analysis scheme using various eye-tracking tasks to assess oculomotor function in a cohort of adolescents with acute concussion symptoms and aged-matched healthy controls. From these data we have evidence that these methods reliably detect oculomotor deficits in the concussed group, including reduced spatial accuracy and diminished tracking performance during visually guided prosaccade and self-paced saccade tasks. The accuracy and tracking deficits are consistent with prior studies on oculomotor function, while introducing novel discriminatory measures relative to fixation assessments – methodologically, a less complicated measure of performance – and thus represent a reliable and simple scheme of detection and analysis of oculomotor deficits associated with brain injury.     

The psychophysics of the pursuit oculomotor system

When a fixation point moves under a row of identical targets at a speed of one target for each flash of a strobe, smooth apparent movement of the targets is seen (the "picket-fence illusion"). When the fixation point is removed, the eye continues to pursue the apparent target movement. Pursuit continues through small changes in target configuration, but is interrupted by a change to a very dissimilar target (such as 1 vs. x) in the middle of a row. This new method, the "pursuit-interruption method," showed that large differences in the number of pixels in a line did not interrupt tracking if the end points of the line were preserved. Pursuit interruption by changes in line orientation (such as /vs./) corresponded to the orientation bandwidth of orientation-sensitive cortical neurons. The maximum number of consecutive missing targets that does not interrupt pursuit depends on frequency of target presentation as well as on parameters of the pursuit system.     

Induced motion and oculomotor capture

Three experiments investigating the basis of induced motion are reported. The proposition that induced motion is based on the visual capture of eye-position information and is therefore a subject-relative, rather than object-relative, motion was explored in the first experiment. Observers made saccades to an invisible auditory stimulus following fixation on a stationary stimulus in which motion was induced. In the remaining two experiments, the question of whether perceived induced motion produces a straight ahead shift was explored. The critical eye movement was directed to apparent straight ahead. Because these saccades partially compensated for the apparent displacement of the induction stimulus, and saccades to the auditory stimulus did not, we conclude that induced motion is not based on oculomotor visual capture. Rather, it is accompanied by a shift in the judged direction of straight ahead, an instance of the straight ahead shift. The results support an object-relative theory of induced motion.     

Adaptation in distance perception based on oculomotor cues

Accommodation and convergence primarily serve to adjust the eyes to the distance of the object viewed, but, once made, these oculomotor adjustments serve as cues for the object’s distance. Experiments are reported that show that the relation between oculomotor adjustments and the distances they signify can be changed by adaptation to glasses that cause alteration in the oculomotor adjustments with which objects are viewed. This changed relation manifested itself in marked alterations of size perception. Wearing, for 30 min, glasses that caused a change in accommodation and convergence corresponding to a smaller object distance and equivalent to 1.5 lens diopters caused subsequent mean size increases that ranged from 50% to 65%. Adaptation to glasses that changed oculomotor adjustments in the same amount but in the opposite direction resulted in decreases in perceived sizes that varied from 18% to 40%, dependent on the distance of the test object. These were the results of size estimates obtained before and after the adaptation period under conditions where only accommodation and convergence served as cues for distance. A newly developed test of size perception was also used, in which S adjusted the size of the projected image of an array of familiar objects on a screen until the size of the objects appeared normal. Again, such adjustments were made before and after the adaptation period, and size differences were obtained that were in the direction to be expected of adaptation and varied in amount between 12% and 33%, dependent on the distance of the screen. The reason for the different amounts of size change measured by the two kinds of tests was investigated.     

Properties of adaptive oculomotor control systems and perception

The adaptive capabilities, perceptual and motor, of several oculomotor systems were examined in the context of their respective control systems. By comparing the systems for the means by which adaptation is thought to occur, certain uniformities emerge to provide the basis for inductive generalizations about the relations between perception, control-system characteristics, visual-motor plasticity, and dysfunction. Major principles to emerge are: (1) adaptation arises out of a symbiotic relation between negative feedback and feedforward control system elements; (2) error signals circulating in negative feedback loops represent the basis for both adaptation and dysfunction in the form of motion sickness and aesthenopia; (3) conscious correlates of oculomotor systems are associated with steady states of the system, but not with system transients; and (4) illusions arise from the issuing of compensatory innervation in order to balance against competing demands on the oculomotor system.     

Visual and proprioceptive adaptation to altered oculomotor adjustments

Adaptation to spectacles that alter in equivalent amounts the accommodation and the convergence with which objects are viewed was produced under two conditions. In one, S alternately pushed away or pulled toward him a screen that exhibited only a single vertical contour while wearing glaaaes that caused decreases in accommodation and convergence equivalent to 1.5 lens diopters. Here kinesthesis for these arm movements provided the only veridical distance cues, A small, but highly significant, adaptation effect was obtained with a teat in which S, before and after the adaptation period, pointed to the location of a test line in the distance dimension. Corresponding tests consisting in size and in depth estimates did not show an adaptation effect. In the other condition of adaptation, S moved objects by hand toward and away from himself while wearing spectacles that increased accommodation and convergence by the equivalent of 1.5 lens diopters. In addition to the altered oculomotor cues, some veridical visual cues for distance such as are caused by perspective were present. This condition yielded changes in size and depth estimates indicative of an adaptation in visual distance perception and a larger effect of adaptation measured by the pointing test. We concluded that the excess of the adaptation effect measured by pointing over that measured by size estimation represents an adaptation in proprioception, as did the pointing effect produced by our first adaptation condition.     

Neurophysiology and neuroanatomy of smooth pursuit in humans

Smooth pursuit eye movements enable us to focus our eyes on moving objects by utilizing well-established mechanisms of visual motion processing, sensorimotor transformation and cognition. Novel smooth pursuit tasks and quantitative measurement techniques can help unravel the different smooth pursuit components and complex neural systems involved in its control. The maintenance of smooth pursuit is driven by a combination of the prediction of target velocity and visual feedback about performance quality, thus a combination of retinal and extraretinal information that has to be integrated in various networks. Different models of smooth pursuit with specific in- and output parameters have been developed for a better understanding of the underlying neurophysiological mechanisms and to make quantitative predictions that can be tested in experiments. Functional brain imaging and neurophysiological studies have defined motion sensitive visual area V5, frontal (FEF) and supplementary (SEF) eye fields as core cortical smooth pursuit regions. In addition, a dense neural network is involved in the adjustment of an optimal smooth pursuit response by integrating also extraretinal information. These networks facilitate interaction of the smooth pursuit system with multiple other visual and non-visual sensorimotor systems on the cortical and subcortical level. Future studies with fMRI advanced techniques (e.g., event-related fMRI) promise to provide an insight into how smooth pursuit eye movements are linked to specific brain activation. Applying this approach to neurological and also mental illness can reveal distinct disturbances within neural networks being present in these disorders and also the impact of medication on this circuitry.     

Cognitive processes involved in smooth pursuit eye movements

Ocular pursuit movements allow moving objects to be tracked with a combination of smooth movements and saccades. The principal objective is to maintain smooth eye velocity close to object velocity, thus minimising retinal image motion and maintaining acuity. Saccadic movements serve to realign the image if it falls outside the fovea, the area of highest acuity. Pursuit movements are often portrayed as voluntary but their basis lies in processes that sense retinal motion and can induce eye movements without active participation. The factor distinguishing pursuit from such reflexive movements is the ability to select and track a single object when presented with multiple stimuli. The selective process requires attention, which appears to raise the gain for the selected object and/or suppress that associated with other stimuli, the resulting competition often reducing pursuit velocity. Although pursuit is essentially a feedback process, delays in motion processing create problems of stability and speed of response. This is countered by predictive processes, probably operating through internal efference copy (extra-retinal) mechanisms using short-term memory to store velocity and timing information from prior stimulation. In response to constant velocity motion, the initial response is visually driven, but extra-retinal mechanisms rapidly take over and sustain pursuit. The same extra-retinal mechanisms may also be responsible for generating anticipatory smooth pursuit movements when past experience creates expectancy of impending object motion. Similar, but more complex, processes appear to operate during periodic pursuit, where partial trajectory information is stored and released in anticipation of expected future motion, thus minimising phase errors associated with motion processing delays.     

Neurophysiology and neuroanatomy of smooth pursuit in humans

Smooth pursuit eye movements enable us to focus our eyes on moving objects by utilizing well-established mechanisms of visual motion processing, sensorimotor transformation and cognition. Novel smooth pursuit tasks and quantitative measurement techniques can help unravel the different smooth pursuit components and complex neural systems involved in its control. The maintenance of smooth pursuit is driven by a combination of the prediction of target velocity and visual feedback about performance quality, thus a combination of retinal and extraretinal information that has to be integrated in various networks. Different models of smooth pursuit with specific in- and output parameters have been developed for a better understanding of the underlying neurophysiological mechanisms and to make quantitative predictions that can be tested in experiments. Functional brain imaging and neurophysiological studies have defined motion sensitive visual area V5, frontal (FEF) and supplementary (SEF) eye fields as core cortical smooth pursuit regions. In addition, a dense neural network is involved in the adjustment of an optimal smooth pursuit response by integrating also extraretinal information. These networks facilitate interaction of the smooth pursuit system with multiple other visual and non-visual sensorimotor systems on the cortical and subcortical level. Future studies with fMRI advanced techniques (e.g., event-related fMRI) promise to provide an insight into how smooth pursuit eye movements are linked to specific brain activation. Applying this approach to neurological and also mental illness can reveal distinct disturbances within neural networks being present in these disorders and also the impact of medication on this circuitry.     

Cognitive processes involved in smooth pursuit eye movements

Ocular pursuit movements allow moving objects to be tracked with a combination of smooth movements and saccades. The principal objective is to maintain smooth eye velocity close to object velocity, thus minimising retinal image motion and maintaining acuity. Saccadic movements serve to realign the image if it falls outside the fovea, the area of highest acuity. Pursuit movements are often portrayed as voluntary but their basis lies in processes that sense retinal motion and can induce eye movements without active participation. The factor distinguishing pursuit from such reflexive movements is the ability to select and track a single object when presented with multiple stimuli. The selective process requires attention, which appears to raise the gain for the selected object and/or suppress that associated with other stimuli, the resulting competition often reducing pursuit velocity. Although pursuit is essentially a feedback process, delays in motion processing create problems of stability and speed of response. This is countered by predictive processes, probably operating through internal efference copy (extra-retinal) mechanisms using short-term memory to store velocity and timing information from prior stimulation. In response to constant velocity motion, the initial response is visually driven, but extra-retinal mechanisms rapidly take over and sustain pursuit. The same extra-retinal mechanisms may also be responsible for generating anticipatory smooth pursuit movements when past experience creates expectancy of impending object motion. Similar, but more complex, processes appear to operate during periodic pursuit, where partial trajectory information is stored and released in anticipation of expected future motion, thus minimising phase errors associated with motion processing delays.     

Distance adaptation depends upon plasticity in the oculomotor control system

Maintaining binocular fixation on a target at 20 cm in the absence of secondary cues to distance produced changes in apparent distance and lateral phoria. Positive lenses of 0, .5, 2.0, 3.5, and 5.0 spherical diopters (SD) were used to manipulate the level of accommodative convergence in force during the period of maintained fixation. An inverse relationship was found between the stimulus to accommodation and the magnitude of the induced esophoria, the phoria being linearly related to an increase in apparent distance. The distance aftereffect obtained in the condition with the lowest net accommodative stimulus li.e., 0 D) equaled that typically produced by base-out prism adaptation with full secondary cues to distance available. In a second experiment, subjects walked through a well-lit hallway while viewing through a pair of 5h base-out prisms. It was shown that increasing the stimulus to accommodation by adding negative lenses of 0, 1.5, 3.5, and 5.5 SD reduced the adaptive change in apparent distance, as well as the change in phoria produced by the conventional base-out prism adaptation paradigm. It was concluded that a change in the resting tonus of the disparity vergence system underlies such adaptation, rather than recalibration of the oculomotor cues to distance. Monocular exposure data indicated that a small change in the tonus control for the accommodative system may be present as well.     

Distractor interference during smooth pursuit eye movements

When 2 targets for pursuit eye movements move in different directions, the eye velocity follows the vector average (S. G. Lisberger & V. P. Ferrera, 1997). The present study investigates the mechanisms of target selection when observers are instructed to follow a predefined horizontal target and to ignore a moving distractor stimulus. Results show that at 140 ms after distractor onset, horizontal eye velocity is decreased by about 25%. Vertical eye velocity increases or decreases by 1 degrees /s in the direction opposite from the distractor. This deviation varies in size with distractor direction, velocity, and contrast. The effect was present during the initiation and steady-state tracking phase of pursuit but only when the observer had prior information about target motion. Neither vector averaging nor winner-take-all models could predict the response to a moving to-be-ignored distractor during steady-state tracking of a predefined target. The contributions of perceptual mislocalization and spatial attention to the vertical deviation in pursuit are discussed.     

Intentionally-evoked modulations of smooth pursuit eye movements

When observers pursue a moving target with their eyes, they use predictions of future target positions in order to keep the target within the fovea. It was suggested that these predictions of smooth pursuit (SP) eye movements are computed only from the visual feedback of the target characteristics. As a consequence, if the target vanishes unexpectedly, the eye movements do not stop immediately, but they overshoot the vanishing point. We compared the spatial and temporal features of such predictive eye movements in a task with or without intentional control over the target vanishing point. If the observers stopped the target with a button press, the overshoot of the eyes was reduced compared to a condition where the offset was computer generated. Accordingly, the eyes started to decelerate well before the target offset and lagged further behind the target when it disappeared. The involvement of intentionally-generated expectancies in eye movement control was also obvious in the spatial trajectories of the eyes, which showed a clear flexion in anticipation of the circular motion path we used. These findings are discussed together with neurophysiological mechanisms underlying the SP eye movements.