Retinal Motion Information Research Articles

Binocular integration of retinal motion information underlies optic flow processing by the cortex

SummaryLocomotion creates various patterns of optic flow on the retina, which provide the observer with information about their movement relative to the environment. However, it is unclear how these optic flow patterns are encoded by the cortex. Here, we use two-photon calcium imaging in awake mice to systematically map monocular and binocular responses to horizontal motion in four areas of the visual cortex. We find that neurons selective to translational or rotational optic flow are abundant in higher visual areas, whereas neurons suppressed by binocular motion are more common in the primary visual cortex. Disruption of retinal direction selectivity in Frmd7 mutant mice reduces the number of translation-selective neurons in the primary visual cortex and translation- and rotation-selective neurons as well as binocular direction-selective neurons in the rostrolateral and anterior visual cortex, blurring the functional distinction between primary and higher visual areas. Thus, optic flow representations in specific areas of the visual cortex rely on binocular integration of motion information from the retina.

The combined effect of eye movements improve head centred local motion information during walking.

Eye movements play multiple roles in human behaviour-small stabilizing movements are important for keeping the image of the scene steady during locomotion, whilst large scanning movements search for relevant information. It has been proposed that eye movement induced retinal motion interferes with the estimation of self-motion based on optic flow. We investigated the effect of eye movements on retinal motion information during walking. Observers walked towards a target, wearing eye tracking glasses that simultaneously recorded the scene ahead and tracked the movements of both eyes. By realigning the frames of the recording from the scene ahead, relative to the centre of gaze, we could mimic the input received by the retina (retinocentric coordinates) and compare this to the input received by the scene camera (head centred coordinates). We asked which of these coordinate frames resulted in the least noisy motion information. Motion noise was calculated by finding the error in between the optic flow signal and a noise-free motion expansion pattern. We found that eye movements improved the optic flow information available, even when large diversions away from target were made.

Illusory motion reveals velocity matching, not foveation, drives smooth pursuit of large objects.

When small objects move in a scene, we keep them foveated with smooth pursuit eye movements. Although large objects such as people and animals are common, it is nonetheless unknown how we pursue them since they cannot be foveated. It might be that the brain calculates an object's centroid, and then centers the eyes on it during pursuit as a foveation mechanism might. Alternatively, the brain merely matches the velocity by motion integration. We test these alternatives with an illusory motion stimulus that translates at a speed different from its retinal motion. The stimulus was a Gabor array that translated at a fixed velocity, with component Gabors that drifted with motion consistent or inconsistent with the translation. Velocity matching predicts different pursuit behaviors across drift conditions, while centroid matching predicts no difference. We also tested whether pursuit can segregate and ignore irrelevant local drifts when motion and centroid information are consistent by surrounding the Gabors with solid frames. Finally, observers judged the global translational speed of the Gabors to determine whether smooth pursuit and motion perception share mechanisms. We found that consistent Gabor motion enhanced pursuit gain while inconsistent, opposite motion diminished it, drawing the eyes away from the center of the stimulus and supporting a motion-based pursuit drive. Catch-up saccades tended to counter the position offset, directing the eyes opposite to the deviation caused by the pursuit gain change. Surrounding the Gabors with visible frames canceled both the gain increase and the compensatory saccades. Perceived speed was modulated analogous to pursuit gain. The results suggest that smooth pursuit of large stimuli depends on the magnitude of integrated retinal motion information, not its retinal location, and that the position system might be unnecessary for generating smooth velocity to large pursuit targets.

Conjugate Adaptation of Smooth Pursuit during Monocular Viewing in Strabismic Monkeys with Exotropia

Humans and monkeys are able to adapt their smooth pursuit output when challenged with consistent errors in foveal/parafoveal image motion during tracking. Visual motion information from the retina is known to be necessary for guiding smooth pursuit adaptation. The purpose of this study is to determine whether retinal motion signals delivered to one eye during smooth pursuit produce adaptation in the fellow eye. We tested smooth pursuit adaptation during monocular viewing in strabismic monkeys with exotropia. To induce smooth pursuit adaptation experimentally, we used a step-ramp tracking with two different velocities (adaptation paradigm), where the target begins moving at one speed (25°/s) for first 100 ms and then changes to a lower speed (5°/s) for the remainder of the trial. Typically, 100 to 200 trials were used to adapt the smooth pursuit response. Control trials employing single speed step-ramp target motion (ramp speed = 25°/s) were used before and after adaptation paradigm to estimate adaptation. The magnitude of adaptation as calculated by percentage change was not significantly different (P = 0.53) for the viewing (mean, 40.3% ± 5.9%) and the nonviewing (mean, 39.7% ± 6.2%) eyes during monocular viewing conditions, even in cases with large angle (18°-20°) strabismus. Our results indicate that animals with strabismus retain the ability to produce conjugate adaptation of smooth pursuit. Therefore, we suggest that a single central representation of retinal motion information in the viewing eye drives adaptation for both eyes equally.

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.

The pursuit theory of motion parallax

Although motion parallax is closely associated with observer head movement, the underlying neural mechanism appears to rely on a pursuit-like eye movement signal to disambiguate perceived depth sign from the ambiguous retinal motion information [Naji, J. J., & Freeman, T. C. A. (2004). Perceiving depth order during pursuit eye movement. Vision Research, 44, 3025–3034; Nawrot, M. (2003). Eye movements provide the extra-retinal signal required for the perception of depth from motion parallax. Vision Research, 43, 1553–1562]. Here, we outline the evidence for a pursuit signal in motion parallax and propose a simple neural network model for how the pursuit theory of motion parallax might function within the visual system. The first experiment demonstrates the crucial role that an extra-retinal pursuit signal plays in the unambiguous perception of depth from motion parallax. The second experiment demonstrates that identical head movements can generate opposite depth percepts, and even ambiguous percepts, when the pursuit signal is altered. The pursuit theory of motion parallax provides a parsimonious explanation for all of these observations.

Specific motion processing pathway deficit during eye tracking in schizophrenia: A performance-matched functional magnetic resonance imaging study

The neural mechanisms underlying smooth pursuit eye movement (SPEM) abnormalities in schizophrenia are not well understood. Previous evidence suggests that a deficit in the processing of internal representations of object motion (extraretinal motion) contributes to SPEM deficits in patients. Functional magnetic resonance imaging (fMRI) activation was compared between patients and control subjects to determine whether schizophrenia patients exhibit abnormal cerebral activation in regions associated with extraretinal motion processing during SPEM. Patients and control subjects were selected based on matched performance in the closed-loop gain. Despite similar performance on closed-loop pursuit gain, patients showed consistent deficits in extraretinal motion based on predictive pursuit. In the magnet, subjects were tested using a traditional smooth-pursuit task that elicits closed-loop response. Patients had reduced pursuit-related activation in several known extraretinal motion processing areas including frontal and supplemental eye fields, medial superior temporal cortex, and anterior cingulate. Patients also showed increased activation in medial occipitotemporal cortex. These results provide functional anatomic evidence supporting reduced function in the extraretinal motion processing pathway in schizophrenia. Increased activation in medial occipitotemporal cortex suggests an increased dependence on immediate retinal motion information, which may be used to compensate for reduced extraretinal signaling during sustained visual tracking.

Visual motion due to eye movements helps guide the hand

Movement of the body, head, or eyes with respect to the world creates one of the most common yet complex situations in which the visuomotor system must localize objects. In this situation, vestibular, proprioceptive, and extra-retinal information contribute to accurate visuomotor control. The utility of retinal motion information, on the other hand, is questionable, since a single pattern of retinal motion can be produced by any number of head or eye movements. Here we investigated whether retinal motion during a smooth pursuit eye movement contributes to visuomotor control. When subjects pursued a moving object with their eyes and reached to the remembered location of a separate stationary target, the presence of a moving background significantly altered the endpoints of their reaching movements. A background that moved with the pursuit, creating a retinally stationary image (no retinal slip), caused the endpoints of the reaching movements to deviate in the direction of pursuit, overshooting the target. A physically stationary background pattern, however, producing retinal image motion opposite to the direction of pursuit, caused reaching movements to become more accurate. The results indicate that background retinal motion is used by the visuomotor system in the control of visually guided action.

Isotropic integration of binocular disparity and relative motion in the perception of three-dimensional shape.

Richards (1985) showed that veridical three-dimensional shape may be recovered from the integration of binocular disparity and retinal motion information, but proposed that this integration may only occur for horizontal retinal motion. Psychophysical evidence supporting the combination of stereo and motion information is limited to the case of horizontal motion (Johnston et al., 1994), and has been criticised on the grounds of potential object boundary cues to shape present in the stimuli. We investigated whether veridical shape can be recovered under more general conditions. Observers viewed cylinders that were defined by binocular disparity, two-frame motion or a combination of disparity and motion, presented at simulated distances of 30 cm, 90 cm or 150 cm. Horizontally and vertically oriented cylinders were rotated about vertical and horizontal axes. When rotation was about the cylinder's own axis, no boundary cues to shape were introduced. Settings were biased for the disparity and two-frame motion stimuli, while more veridical shape judgements were made under all conditions for combined cue stimuli. These results demonstrate that the improved perception of three-dimensional shape in these stimuli is not a consequence of the presence of object boundary cues, and that the combination of disparity and motion is not restricted to horizontal image motion.

Neural correlates of reafference: evoked brain activity during motion perception and saccadic eye movements.

The ability to perceive a stable visual environment despite eye movements and the resulting displacement of the retinal image is a striking feature of visual perception. In order to study the brain mechanism related to this phenomenon, an EEG was recorded from 30 electrodes spaced over the occipital, temporal and parietal brain areas while stationary or moving visual stimuli with velocities between 178 degrees/s and 533 degrees/s were presented. The visual stimuli were presented both during saccadic eye movements and with stationary eyes. Stimulus-related potentials were measured, and the effects of absolute and relative stimulus velocity were analyzed. Healthy adults participated in the experiments. In all 36 subjects and experimental conditions, four potential components were found with mean latencies of about 70, 140, 220 and 380 ms. The latency of the two largest components between 100 and 240 ms decreased while field strength increased with higher absolute stimulus velocity for both stationary and moving eyes, whereas relative stimulus velocity had no effect on amplitude, latency and topography of the visual evoked potential (VEP) components. If the visual system uses retinal motion information only, we would expect a dependence upon relative velocity. Since field strength and latency of the components were independent of eye movements but dependent upon absolute stimulus velocity, the visual cortex must use extraretinal information to extract stimulus velocity. This was confirmed by the fact that significant topographic changes were observed when brain activity evoked during saccades and with stationary eyes was compared. In agreement with the reafference principle, the findings indicate that the same absolute visual stimulus activates different neuronal elements during saccades than during fixation.

What gives rise to impaired smooth pursuit in the relatives of patients with schizophrenia?

<b>ARCHIVES OF GENERAL PSYCHIATRY</b> <b>Smooth Pursuit Eye Movements to Extraretinal Motion Signals: Deficits in Relatives of Patients With Schizophrenia</b> <i>Gunvant K. Thaker, MD; David E. Ross, MD; Shawn L. Cassady, MD; Helene M. Adami, MSW; David LaPorte, PhD; Deborah R. Medoff, PhD; Adrienne Lahti, MD</i> <h3></h3> <b>Background:</b>Although mounting evidence supports the idea that smooth pursuit abnormality marks the genetic liability to schizophrenia, the precise ocular motor mechanism underlying the abnormality remains unknown. Based on recent findings in schizophrenia, we hypothesize that subtle deficits in the ability to hold online and/or use extraretinal motion information underlie the pursuit abnormality in vulnerable individuals. <b>Methods:</b>The hypothesis was tested in 69 first-degree, biological relatives of probands with schizophrenia; 26 relatives had schizophrenia spectrum personalities (SSP). Subjects recruited from the community (n=71; 29 with SSP), without a known family history of psychosis, constituted the comparison groups. The traditional smooth pursuit gain measure, which is a ratio of smooth pursuit eye velocity in response to both retinal and extraretinal motion signals and the target velocity, was obtained. In addition, newly developed measures of predictive smooth pursuit (ie, in the presence of only extraretinal motion signals) were obtained. The latter measures were evaluated after the current retinal motion signals were made unavailable by briefly making the target invisible. <b>Results:</b>Relatives, particularly those with SSP, showed significantly poorer predictive pursuit, it response to extraretinal motion signals (F_2,130=6.51,<i>P</i>&lt;.005), compared with the community subjects. However, the traditional smooth pursuit gain in response to both retinal and extraretinal motion signals was not different between groups. <b>Conclusions:</b>These results suggest that relatives of patients with schizophrenia, particularly those with SSP, have specific deficits in predictive pursuit based on only extraretinal motion signals. Normal smooth pursuit gain in response to both retinal and extraretinal motion signals is likely due to compensation based on retinal motion information. The latter suggests normal retinal motion processing and smooth pursuit motor output. <i>1998;55:830-836.</i>

Smooth pursuit eye movements to extraretinal motion signals: deficits in relatives of patients with schizophrenia.

Although mounting evidence supports the idea that smooth pursuit abnormality marks the genetic liability to schizophrenia, the precise ocular motor mechanism underlying the abnormality remains unknown. Based on recent findings in schizophrenia, we hypothesize that subtle deficits in the ability to hold online and/or use extraretinal motion information underlie the pursuit abnormality in vulnerable individuals. The hypothesis was tested in 69 first-degree, biological relatives of probands with schizophrenia; 26 relatives had schizophrenia spectrum personalities (SSP). Subjects recruited from the community (n=71; 29 with SSP), without a known family history of psychosis, constituted the comparison groups. The traditional smooth pursuit gain measure, which is a ratio of smooth pursuit eye velocity in response to both retinal and extraretinal motion signals and the target velocity, was obtained. In addition, newly developed measures of predictive smooth pursuit (ie, in the presence of only extraretinal motion signals) were obtained. The latter measures were evaluated after the current retinal motion signals were made unavailable by briefly making the target invisible. Relatives, particularly those with SSP, showed significantly poorer predictive pursuit response to extraretinal motion signals (F(2,136)=6.51, P<.005), compared with the community subjects. However, the traditional smooth pursuit gain in response to both retinal and extraretinal motion signals was not different between groups. These results suggest that relatives of patients with schizophrenia, particularly those with SSP, have specific deficits in predictive pursuit based on only extraretinal motion signals. Normal smooth pursuit gain in response to both retinal and extraretinal motion signals is likely due to compensation based on retinal motion information. The latter suggests normal retinal motion processing and smooth pursuit motor output.

Does pursuit abnormality in schizophrenia represent a deficit in the predictive mechanism?

Although an abnormality of smooth pursuit eye movement has been consistently noted in schizophrenia, the underlying ocular motor pathophysiology is unknown. It is unclear whether the abnormality represents deficits in processing of information provided by the moving target, generation of pursuit eye movements, or other ocular motor and related cognitive processes. To evaluate the ability to process information provided by a moving target, saccadic accuracies were studied in step-ramp and single step tasks. Schizophrenic (with and without tardive dyskinesia [TD]) and normal subjects made equally accurate initial corrective saccades to the moving target. Thus, when the target jumped and then smoothly moved (creating a position and a velocity error on the retina), the patients were able to process retinal motion information and generate a normally accurate saccadic response. After the initial corrective saccade, both groups followed the target with a combination of pursuit eye movements and occasional catch-up saccades. During this period, the retinal velocity error is minimal because the eye approximates the target motion, and the major source of target motion information both for the smooth pursuit and saccadic responses is extra-retinal (i.e., predictive mechanism). The accuracies of catch-up saccades were significantly lower in the schizophrenic patients than in the normal subjects. During this period, overall pursuit performance, measured by pursuit gain, was also significantly worse in the patients. Accuracies of subsequent catch-up saccades, but not initial corrective saccades, significantly predicted the pursuit gain. Low pursuit gain was associated with high numbers of saccades per time spent in pursuit, which were similar in both schizophrenic subgroups (i.e., with and without TD), but were only significantly higher in the patients with TD than in the normal subjects. These preliminary data suggest that schizophrenic patients are able to process retinal motion information but have difficulties in using extra-retinal motion information to generate an appropriate saccadic response.

The effects of lesions of anteromedial cortex on a ballistic visuomotor task in the Mongolian gerbil ( Meriones unguiculatus)

Mongolian gerbils were trained to jump across a gap of randomly varying distance and then received one of three surgical treatments: Ten gerbils received aspiration lesions of anteromedial cortex (AMC), four gerbils received control lesions of a part of frontal cortex and nine gerbils received a sham procedure. Following a short recovery period, gerbils were tested in the jumping task. Gerbils with AMC lesions carried out fewer head movements than both sham and frontal gerbils. In addition, gerbils with AMC lesions were significantly less accurate in the distance estimation component of the jumping task, particularly at longer distances. These results suggest that anteromedial cortex participates in the generation of vertical head movements that are used to produce retinal motion information and confirms that these head movements are used to heighten the precision of distance estimation at longer testing distances.