Retinal Motion Research Articles

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.

Motion perception during sinusoidal smooth pursuit eye movements: Signal latencies and non-linearities

Smooth pursuit eye movements add motion to the retinal image. To compensate, the visual system can combine estimates of pursuit velocity and retinal motion to recover motion with respect to the head. Little attention has been paid to the temporal characteristics of this compensation process. Here, we describe how the latency difference between the eye movement signal and the retinal signal can be measured for motion perception during sinusoidal pursuit. In two experiments, observers compared the peak velocity of a motion stimulus presented in pursuit and fixation intervals. Both the pursuit target and the motion stimulus moved with a sinusoidal profile. The phase and amplitude of the motion stimulus were varied systematically in different conditions, along with the amplitude of pursuit. The latency difference between the eye movement signal and the retinal signal was measured by fitting the standard linear model and a non-linear variant to the observed velocity matches. We found that the eye movement signal lagged the retinal signal by a small amount. The non-linear model fitted the velocity matches better than the linear one and this difference increased with pursuit amplitude. The results support previous claims that the visual system estimates eye movement velocity and retinal velocity in a non-linear fashion and that the latency difference between the two signals is small.

Local motion inside an object affects pointing less than smooth pursuit

During smooth pursuit eye movements, briefly presented objects are mislocalized in the direction of motion. It has been proposed that the localization error is the sum of the pursuit signal and the retinal motion signal in a ~200 ms interval after flash onset. To evaluate contributions of retinal motion signals produced by the entire object (global motion) and elements within the object (local motion), we asked observers to reach to flashed Gabor patches (Gaussian-windowed sine-wave gratings). Global motion was manipulated by varying the duration of a stationary flash, and local motion was manipulated by varying the motion of the sine-wave. Our results confirm that global retinal motion reduces the localization error. The effect of local retinal motion on object localization was far smaller, even though local and global motion had equal effects on eye velocity. Thus, local retinal motion has differential access to manual and oculomotor control circuits. Further, we observed moderate correlations between smooth pursuit gain and localization error.

The mechanisms responsible for the flash-lag effect cannot provide the motor prediction that we need in daily life

AbstractThe visual prediction that Nijhawan proposes cannot explain why the flash-lag effect depends on what happens after the flash. Moreover, using a visual prediction based on retinal image motion to compensate for neuronal time delays will seldom be of any use for motor control, because one normally pursues objects with which one intends to interact with ones eyes.

A neural representation of depth from motion parallax in macaque visual cortex

Perception of depth is a fundamental challenge for the visual system, particularly for observers moving through their environment. The brain makes use of multiple visual cues to reconstruct the three-dimensional structure of a scene. One potent cue, motion parallax, frequently arises during translation of the observer because the images of objects at different distances move across the retina with different velocities. Human psychophysical studies have demonstrated that motion parallax can be a powerful depth cue, and motion parallax seems to be heavily exploited by animal species that lack highly developed binocular vision. However, little is known about the neural mechanisms that underlie this capacity. Here we show, by using a virtual-reality system to translate macaque monkeys (Macaca mulatta) while they viewed motion parallax displays that simulated objects at different depths, that many neurons in the middle temporal area (area MT) signal the sign of depth (near versus far) from motion parallax in the absence of other depth cues. To achieve this, neurons must combine visual motion with extra-retinal (non-visual) signals related to the animal's movement. Our findings suggest a new neural substrate for depth perception and demonstrate a robust interaction of visual and non-visual cues in area MT. Combined with previous studies that implicate area MT in depth perception based on binocular disparities, our results suggest that area MT contains a more general representation of three-dimensional space that makes use of multiple cues.

Effects of attention shifts to stationary objects during steady-state smooth pursuit eye movements

A number of studies have shown that stationary backgrounds compromise smooth pursuit eye movements. It has been suggested that poor attentional selection of the pursuit target was responsible for reductions of pursuit gain. To quantify the detrimental effects of attention, we instructed observers to either pay attention to background objects or to ignore them. The to-be-attended object was indicated by peripheral or central cues. Strong reductions of pursuit gain occurred when the following conditions were met: (a) the subject payed attention to the object (b) a salient event was present, for instance the onset of the target or cue and (c) the attended target produced retinal motion. Removing any of the three conditions resulted in no or far smaller decreases of pursuit gain. Further, decreases in pursuit gain were present with perceptual discrimination and simple manual detection.

Evidence for flow-parsing in radial flow displays

Retinal motion of objects is not in itself enough to signal whether or how objects are moving in the world; the same pattern of retinal motion can result from movement of the object, the observer or both. Estimation of scene-relative movement of an object is vital for successful completion of many simple everyday tasks. Recent research has provided evidence for a neural flow-parsing mechanism which uses the brain’s sensitivity to optic flow to separate retinal motion signals into those components due to observer movement and those due to the movement of objects in the scene. In this study we provide further evidence that flow-parsing is implicated in the assessment of object trajectory during observer movement. Furthermore, it is shown that flow-parsing involves a global analysis of retinal motion, as might be expected if optic flow processing underpinned this mechanism.

Neuronal correlates of perceptual stability during eye movements

We are usually unaware of retinal image motion resulting from our own movement. For instance, during slow-tracking eye movements the world around us remains perceptually stable despite the retinal image slip induced by the eye movement. It is commonly held that this example of perceptual invariance is achieved by subtracting an internal reference signal, reflecting the eye movement, from the retinal motion signal. If the two cancel each other, visual objects, which do not move, will also be perceived as non-moving. If, however, the reference signal is too small or too large, a false eye movement-induced motion of the external world, the Filehne illusion, will be perceived. We have exploited our ability to manipulate the size of the reference signal in an attempt to identify neurons in the visual cortex of monkeys, influenced by the percept of self-induced visual motion or the reference signal rather than the retinal motion signal. We report here that such 'percept-related' neurons can already be found in the primary visual cortex area, although few in numbers. They become more frequent in areas middle temporal and medial superior temporal in the superior temporal sulcus, and comprise almost 50% of all neurons in area visual posterior sylvian (VPS) in the posterior part of the lateral sulcus. In summary, our findings suggest that our ability to perceive a visual world, which is stable despite self-motion, is based on a neuronal network, which culminates in the VPS located in the lateral sulcus below the classical dorsal stream of visual processing.

Capture of attention by scene-relative object movement during self-movement

If the observer is not moving object movement is uniquely signalled by retinal image motion. Under such circumstances a moving object captures attention. During self-movement the global image motion that results from movement of the eyes may mask the image motion that signals object movement. We investigated whether a moving object captures attention in this case. Through stereo glasses, observers viewed 24 objects arranged in a 3-D volume. Four of the objects were potential target objects that could change shape. During viewing the camera viewpoint was translated and rotated to simulate self-movement. Observers were required to identify a shape change as rapidly as possible. On every 35th trial an object within the scene would unexpectedly move at approximately the same time as the shape change. When the object that changed shape was also the object that moved, response time was shorter that when a different object moved; this is the hallmark of attentional capture. Therefore we conclude that during self-movement, unexpected object movement captures attention.

Perceptual Stability—Going with the Flow

Historically, inflow and outflow hypotheses have been formulated as the primary explanations for perceptual stability. Central to these hypotheses is the postulation that, following an intended eye movement, knowledge of eye position cancels the consequences of the retinal image motion. Here, we reconsider the evidence for the extra-retinal signal and discuss whether this cancellation approach is compatible with the available empirical evidence. In particular, we propose that visual-oculomotor processing is a distributed process and that population-coding models of sensorimotor transformations are critical elements that need to be incorporated in any comprehensive explanation of spatial constancy.

Binocular phasic coactivation does not prevent ocular dominance segregation

The segregation of geniculo-cortical afferents into ocular dominance columns is an activity-dependent process. It was hypothesized that this process is susceptible to the temporal patterning of the retinal input. Accordingly, asynchronous activation of the two eyes should enhance ocular dominance segregation but synchronous activation should decrease or prevent it. In order to test the second part of the hypothesis, kitten were raised in strobe light which phasically coactivated the retinal inputs during 10 microsecond flashes at 8 Hz. Strobe rearing prevents retinal motion signals but allows vision of stationary contours. At the age of 10-14 weeks, ocular dominance columns were labeled either transneuronally by (3H)-proline or by (14C)-2-deoxyglucose autoradiography. Contrary to the hypothesis, ocular dominance columns were very well segregated and the pattern closely resembled the pattern observed in squinting cats. We conclude that the light flashes were sufficient to enable binocular competition and that ocular dominance segregation was supported by the mismatch of the stationary contours. Our result thus emphasizes a feature-selective mechanism over mere global temporal patterning of retinal signals.

Efficient encoding of natural optic flow

Statistically efficient processing schemes focus the resources of a signal processing system on the range of statistically probable signals. Relying on the statistical properties of retinal motion signals during ego-motion we propose a nonlinear processing scheme for retinal flow. It maximizes the mutual information between the visual input and its neural representation, and distributes the processing load uniformly over the neural resources. We derive predictions for the receptive fields of motion sensitive neurons in the velocity space. The properties of the receptive fields are tightly connected to their position in the visual field, and to their preferred retinal velocity. The velocity tuning properties show characteristics of properties of neurons in the motion processing pathway of the primate brain.

Shared Computational Mechanism for Tilt Compensation Accounts for Biased Verticality Percepts in Motion and Pattern Vision

To determine the direction of object motion in external space, the brain must combine retinal motion signals and information about the orientation of the eyes in space. We assessed the accuracy of this process in eight laterally tilted subjects who aligned the motion direction of a random-dot pattern (30% coherence, moving at 6 degrees /s) with their perceived direction of gravity (motion vertical) in otherwise complete darkness. For comparison, we also tested the ability to align an adjustable visual line (12 degrees diameter) to the direction of gravity (line vertical). For small head tilts (<40 degrees ), systematic errors in either task were almost negligible. In contrast, tilts >60 degrees revealed a pattern of large systematic errors (often >30 degrees ) that was virtually identical in both tasks. Regression analysis confirmed that mean errors in the two tasks were closely related, with slopes close to 1.0 and correlations >0.89. Control experiments ruled out that motion settings were based on processing of individual single-dot paths. We conclude that the conversion of both motion direction and line orientation on the retina into a spatial frame of reference involves a shared computational strategy. Simulations with two spatial-orientation models suggest that the pattern of systematic errors may be the downside of an optimal strategy for dealing with imperfections in the tilt signal that is implemented before the reference-frame transformation.

Vestibular Nuclei and Cerebellum Put Visual Gravitational Motion in Context

Animal survival in the forest, and human success on the sports field, often depend on the ability to seize a target on the fly. All bodies fall at the same rate in the gravitational field, but the corresponding retinal motion varies with apparent viewing distance. How then does the brain predict time-to-collision under gravity? A perspective context from natural or pictorial settings might afford accurate predictions of gravity's effects via the recovery of an environmental reference from the scene structure. We report that embedding motion in a pictorial scene facilitates interception of gravitational acceleration over unnatural acceleration, whereas a blank scene eliminates such bias. Functional magnetic resonance imaging (fMRI) revealed blood-oxygen-level-dependent correlates of these visual context effects on gravitational motion processing in the vestibular nuclei and posterior cerebellar vermis. Our results suggest an early stage of integration of high-level visual analysis with gravity-related motion information, which may represent the substrate for perceptual constancy of ubiquitous gravitational motion.

Simultaneous adaptation of retinal and extra-retinal motion signals

A number of models of motion perception include estimates of eye velocity to help compensate for the incidental retinal motion produced by smooth pursuit. The ‘classical’ model uses extra-retinal motor command signals to obtain the estimate. More recent ‘reference-signal’ models use retinal motion information to enhance the extra-retinal signal. The consequence of simultaneously adapting to pursuit and retinal motion is thought to favour the reference-signal model, largely because the perception of motion during pursuit (‘perceived stability’) changes despite the absence of a standard motion aftereffect. The current experiments investigated whether the classical model could also account for these findings. Experiment 1 replicated the changes to perceived stability and then showed how simultaneous motion adaptation changes perceived retinal speed (a velocity aftereffect). Contrary to claims made by proponents of the reference-signal model, adapting simultaneously to pursuit and retinal motion therefore alters the retinal motion inputs to the stability computation. Experiment 2 tested the idea that simultaneous motion adaptation sets up a competitive interaction between two types of velocity aftereffect, one retinal and one extra-retinal. The results showed that pursuit adaptation by itself drove perceived stability in one direction and that adding adapting retinal motion drove perceived stability in the other. Moreover, perceived stability changed in conditions that contained no mismatch between adapting pursuit and adapting retinal motion, contrary to the reference-signal account. Experiment 3 investigated whether the effects of simultaneous motion adaptation were directionally tuned. Surprisingly no tuning was found, but this was true for both perceived stability and retinal velocity aftereffect. The three experiments suggest that simultaneous motion adaptation alters perceived stability based on separable changes to retinal and extra-retinal inputs. Possible mechanisms underlying the extra-retinal velocity aftereffect are discussed.

A unified probabilistic model of the perception of three-dimensional structure from optic flow

Human observers can perceive the three- dimensional (3-D) structure of their environment using various cues, an important one of which is optic flow. The motion of any point's projection on the retina depends both on the point's movement in space and on its distance from the eye. Therefore, retinal motion can be used to extract the 3-D structure of the environment and the shape of objects, in a process known as structure-from-motion (SFM). However, because many combinations of 3-D structure and motion can lead to the same optic flow, SFM is an ill-posed inverse problem. The rigidity hypothesis is a constraint supposed to formally solve the SFM problem and to account for human performance. Recently, however, a number of psychophysical results, with both moving and stationary human observers, have shown that the rigidity hypothesis alone cannot account for human performance in SFM tasks, but no model is known to account for the new results. Here, we construct a Bayesian model of SFM based mainly on one new hypothesis, that of stationarity, coupled with the rigidity hypothesis. The predictions of the model, calculated using a new and powerful methodology called Bayesian programming, account for a wide variety of experimental findings.

Synchronized Firing among Retinal Ganglion Cells Signals Motion Reversal

We show that when a moving object suddenly reverses direction, there is a brief, synchronous burst of firing within a population of retinal ganglion cells. This burst can be driven by either the leading or trailing edge of the object. The latency is constant for movement at different speeds, objects of different size, and bright versus dark contrasts. The same ganglion cells that signal a motion reversal also respond to smooth motion. We show that the brain can build a pure reversal detector using only a linear filter that reads out synchrony from a group of ganglion cells. These results indicate that not only can the retina anticipate the location of a smoothly moving object, but that it can also signal violations in its own prediction. We show that the reversal response cannot be explained by models of the classical receptive field and suggest that nonlinear receptive field subunits may be responsible.

Perception of object trajectory: Parsing retinal motion into self and object movement components

A moving observer needs to be able to estimate the trajectory of other objects moving in the scene. Without the ability to do so, it would be difficult to avoid obstacles or catch a ball. We hypothesized that neural mechanisms sensitive to the patterns of motion generated on the retina during self-movement (optic flow) play a key role in this process, "parsing" motion due to self-movement from that due to object movement. We investigated this "flow parsing" hypothesis by measuring the perceived trajectory of a moving probe placed within a flow field that was consistent with movement of the observer. In the first experiment, the flow field was consistent with an eye rotation; in the second experiment, it was consistent with a lateral translation of the eyes. We manipulated the distance of the probe in both experiments and assessed the consequences. As predicted by the flow parsing hypothesis, manipulating the distance of the probe had differing effects on the perceived trajectory of the probe in the two experiments. The results were consistent with the scene geometry and the type of simulated self-movement. In a third experiment, we explored the contribution of local and global motion processing to the results of the first two experiments. The data suggest that the parsing process involves global motion processing, not just local motion contrast. The findings of this study support a role for optic flow processing in the perception of object movement during self-movement.

Postural control in dyslexic and non-dyslexic children

Postural control relies to visual-motion processing (afferent or efferent) and this is thought to be deficient in dyslexics. There is a controversy between clinic and fundamental studies as to the presence of posture abnormalities in dyslexics. To explore further this issue, this study examines posture stability in quite stance in 13 dyslexics (mean age: 13.5 years) and in 13 non-dyslexics (mean age: 13 years). Experiment 1 shows that, similarly to adults and elderly, all children (dyslexics and non-dyslexics), present better stability at near distance (i.e. smaller surface area of the COP, smaller lateral and antero-posterior oscillations). This could be due to reduced angular size of retinal motion signals at far, but also to convergence relaxation. Importantly, the surface area of the COP, lateral and antero-posterior oscillations are significantly higher in dyslexics. Experiment 2 examines posture stability while subjects make active vergence movements between a far and a near target. For many dyslexics, moving the eyes back and forth in depth rather improved postural stability. The only significant difference was that the lateral oscillations were still higher in dyslexics. Experiment 3 uses eye movement recordings (video-oculography) and demonstrates that dyslexics have problems with maintaining stable the angle of vergence for a prolonged period. We conclude that mild postural instability may exist in dyslexics but it could be improved by oculomotor and attention processes.

Backscroll illusion in far peripheral vision

The backscroll illusion refers to the apparent motion perceived in the background of a movie image that presents a locomotive object such as a person, an animal, or a vehicle. Here, we report that the backscroll illusion can occur in far peripheral visual fields at retinal eccentricity of more than 30 degrees. In psychological experiments, we presented a walking person in profile against an ambiguously moving background of vertical counterphase grating. This stimulus, which subtended 30 degrees of visual angle in width and height, was projected onto a hemispheric screen and positioned at horizontal eccentricity between 0 degrees and 50 degrees at intervals of 10 degrees. The eccentricity was changed randomly trial by trial, and stimulus duration was as short as 350 ms so that observers could not effectively move their eyes to the stimulus. Six observers viewed the stimulus either monocularly or binocularly and reported their perceptual impression for the grating in a three-alternative forced-choice procedure: drifting left, drifting right, or flickering. Results showed that the grating appeared to move in the opposite direction of walking at high probabilities even in the far periphery. Additional experiments confirmed that walking action could be recognized from the far peripheral stimulation. Our findings suggest that the visual system uses high-level object-centered motion signals to disambiguate retinal motion signals in the whole visual field.