Extraretinal Information Research Articles

Brain representations of motion and position in the double-drift illusion.

In the 'double-drift' illusion, local motion within a window moving in the periphery of the visual field alters the window's perceived path. The illusion is strong even when the eyes track a target whose motion matches the window so that the stimulus remains stable on the retina. This implies that the illusion involves the integration of retinal signals with non-retinal eye-movement signals. To identify where in the brain this integration occurs, we measured BOLD fMRI responses in visual cortex while subjects experienced the double-drift illusion. We then used a combination of univariate and multivariate decoding analyses to identify (1) which brain areas were sensitive to the illusion and (2) whether these brain areas contained information about the illusory stimulus trajectory. We identified a number of cortical areas that responded more strongly during the illusion than a control condition that was matched for low-level stimulus properties. Only in area hMT+ was it possible to decode the illusory trajectory. We additionally performed a number of important controls that rule out possible low-level confounds. Concurrent eye tracking confirmed that subjects accurately tracked the moving target; we were unable to decode the illusion trajectory using eye position measurements recorded during fMRI scanning, ruling out explanations based on differences in oculomotor behavior. Our results provide evidence for a perceptual representation in human visual cortex that incorporates extraretinal information.

More (corrective) consecutive saccades after a lesion to the posterior parietal cortex.

To reach a target, primary saccades (S1s) are often followed by (corrective) consecutive saccades (S2, and potentially S3, S4, S5), which are based on retinal and extraretinal feedback. Processing these extraretinal signals was found to be significantly impaired by lesions to the posterior parietal cortex (PPC). Recent studies, however, added a more nuanced view to the role of the PPC, where patients with PPC lesions still used extraretinal signals for S2s and perceptual judgements (Fabius et al., 2020; Rath-Wilson & Guitton, 2015). Hence, it seems that a PPC lesion is not disrupting extraretinal processing per se. Yet, a lesion might still result in less reliable processing of extraretinal signals. Here, we investigated whether this lower reliability manifests as decreased or delayed S2 initiation. Patients with PPC lesions (n = 7) and controls (n = 26) performed a prosaccade task where the target either remained visible or was removed after S1 onset. When S1 is removed, accurate S2s (corrections of S1 error) rely solely on extraretinal signals. We analysed S2 quantity and timing using linear mixed-effects modelling and additive hazards analyses. Patients demonstrated slower S1 execution and lower S1 amplitudes than controls, but their S2s still compensated the S1 undershoot, also when they only relied on extraretinal information. Surprisingly, patients showed an increased amount of S2s. This deviation from control behaviour can be seen as suboptimal, but given the decreased accuracy of the primary saccade, it could be optimal for patients to employ more (corrective) consecutive saccades to overcome this inaccuracy.

Distributions of Visual Receptive Fields from Retinotopic to Craniotopic Coordinates in the Lateral Intraparietal Area and Frontal Eye Fields of the Macaque

Even though retinal images of objects change their locations following each eye movement, we perceive a stable and continuous world. One possible mechanism by which the brain achieves such visual stability is to construct a craniotopic coordinate by integrating retinal and extraretinal information. There have been several proposals on how this may be done, including eye-position modulation (gain fields) of retinotopic receptive fields (RFs) and craniotopic RFs. In the present study, we investigated coordinate systems used by RFs in the lateral intraparietal (LIP) cortex and frontal eye fields (FEF) and compared the two areas. We mapped the two-dimensional RFs of neurons in detail under two eye fixations and analyzed how the RF of a given neuron changes with eye position to determine its coordinate representation. The same recording and analysis procedures were applied to the two brain areas. We found that, in both areas, RFs were distributed from retinotopic to craniotopic representations. There was no significant difference between the distributions in the LIP and FEF. Only a small fraction of neurons was fully craniotopic, whereas most neurons were between the retinotopic and craniotopic representations. The distributions were strongly biased toward the retinotopic side but with significant craniotopic shifts. These results suggest that there is only weak evidence for craniotopic RFs in the LIP and FEF, and that transformation from retinotopic to craniotopic coordinates in these areas must rely on other factors such as gain fields.

Brightness Perception in World-Centered Coordinates Assessed by Pupillometry.

Subjective brightness perception reportedly differs among the peripheral visual fields owing to lower- and higher-order cognition. However, there is still a lack of information associated with subjective brightness perception in the world-centered coordinates, not in the visual fields. In this study, we aimed to investigate the anisotropy of subjective brightness perception in the world-centered coordinates based on pupillary responses to the stimuli in five locations by manipulating the world-centered coordinates through active (requiring head movement) and passive scenes (without head movement) in a virtual reality environment. Specifically, this study aimed to elucidate if there is an ecological advantage in the five different locations in the world-centered coordinates. The pupillary responses to glare and halo stimuli indicated that the brightness perception differed among the five locations in the world-centered coordinates. Furthermore, we found that the pupillary response to stimuli at the top location might be influenced by ecological factors (such as from the bright sky and the sun's existence). Thus, we have contributed to the understanding of the extraretinal information influence on subjective brightness perception in the world-centered coordinates, demonstrating that the pupillary response is independent of head movement.

Transsaccadic visual perception of foveal compared to peripheral environmental changes.

The maintenance of stable visual perception across eye movements is hypothesized to be aided by extraretinal information (e.g., corollary discharge [CD]). Previous studies have focused on the benefits of this information for perception at the fovea. However, there is little information on the extent that CD benefits peripheral visual perception. Here we systematically examined the extent that CD supports the ability to perceive transsaccadic changes at the fovea compared to peripheral changes. Human subjects made saccades to targets positioned at different amplitudes (4° or 8°) and directions (rightward or upward). On each trial there was a reference point located either at (fovea) or 4° away (periphery) from the target. During the saccade the target and reference disappeared and, after a blank period, the reference reappeared at a shifted location. Subjects reported the perceived shift direction, and we determined the perceptual threshold for detection and estimate of the reference location. We also simulated the detection and location if subjects solely relied on the visual error of the shifted reference experienced after the saccade. The comparison of the reference location under these two conditions showed that overall the perceptual estimate was approximately 53% more accurate and 30% less variable than estimates based solely on visual information at the fovea. These values for peripheral shifts were consistently lower than that at the fovea: 34% more accurate and 9% less variable. Overall, the results suggest that CD information does support stable visual perception in the periphery, but is consistently less beneficial compared to the fovea.

Eye-movements support chronometric imagery performance even when the task is occluded

ABSTRACT Mental chronometry has often been used to provide a temporal comparison between executed and imagined movements, with smaller discrepancies indicating more accurate image production and better imagery performance. In this study, we examined the importance of retinal and extra-retinal information in the performance of simple, sequential movements. After physical practice of four activities of daily living (Southampton Hand Assessment Procedure), nineteen participants imagined completing the same tasks with: 1) free eye-movements and visible objects, 2) free eye-movements and no visibility of the objects, and 3) constrained eye-movements and visible objects. Results suggested imagery performance was slower/less accurate compared to physical execution when the eyes were constrained. Conversely, chronometric imagery performance was unaffected with free eye movements, even when task-specific visual information was occluded. This study highlights the crucial role that eye-movements play in the regulation of the temporal aspects of imagery even when retinal information is absent, suggesting that temporal sequencing of imagined actions is largely dependent on extra-retinal information sources.

Intra-saccadic displacement sensitivity after a lesion to the posterior parietal cortex

Visual perception is introspectively stable and continuous across eye movements. It has been hypothesized that displacements in retinal input caused by eye movements can be dissociated from displacements in the external world using extra-retinal information, such as a corollary discharge from the oculomotor system. The extra-retinal information can inform the visual system about an upcoming eye movement and accompanying displacements in retinal input. The parietal cortex has been hypothesized to be critically involved in integrating retinal and extra-retinal information. Two tasks have been widely used to assess the quality of this integration: double-step saccades and intra-saccadic displacements. Double-step saccades performed by patients with parietal cortex lesions seemed to show hypometric second saccades. However, recently idea has been refuted by demonstrating that patients with very similar lesions were able to perform the double step saccades, albeit taking multiple saccades to reach the saccade target. So, it seems that extra-retinal information is still available for saccade execution after a lesion to the parietal lobe. Here, we investigated whether extra-retinal signals are also available for perceptual judgements in nine patients with strokes affecting the posterior parietal cortex. We assessed perceptual continuity with the intra-saccadic displacement task. We exploited the increased sensitivity when a small temporal blank is introduced after saccade offset (blank effect). The blank effect is thought to reflect the availability of extra-retinal signals for perceptual judgements. Although patients exhibited a relative difference to control subjects, they still demonstrated the blank effect. The data suggest that a lesion to the posterior parietal cortex (PPC) alters the processing of extra-retinal signals but does not abolish their influence altogether.

Misperception of motion in depth originates from an incomplete transformation of retinal signals.

Depth perception requires the use of an internal model of the eye-head geometry to infer distance from binocular retinal images and extraretinal 3D eye-head information, particularly ocular vergence. Similarly, for motion in depth perception, gaze angle is required to correctly interpret the spatial direction of motion from retinal images; however, it is unknown whether the brain can make adequate use of extraretinal version and vergence information to correctly transform binocular retinal motion into 3D spatial coordinates. Here we tested this hypothesis by asking participants to reconstruct the spatial trajectory of an isolated disparity stimulus moving in depth either peri-foveally or peripherally while participants' gaze was oriented at different vergence and version angles. We found large systematic errors in the perceived motion trajectory that reflected an intermediate reference frame between a purely retinal interpretation of binocular retinal motion (not accounting for veridical vergence and version) and the spatially correct motion. We quantify these errors with a 3D reference frame model accounting for target, eye, and head position upon motion percept encoding. This model could capture the behavior well, revealing that participants tended to underestimate their version by up to 17%, overestimate their vergence by up to 22%, and underestimate the overall change in retinal disparity by up to 64%, and that the use of extraretinal information depended on retinal eccentricity. Since such large perceptual errors are not observed in everyday viewing, we suggest that both monocular retinal cues and binocular extraretinal signals are required for accurate real-world motion in depth perception.

Visuomotor feedback gains are modulated by gaze position.

During goal-directed reaching, people typically direct their gaze to the target before the start of the hand movement and maintain fixation until the hand arrives. This gaze strategy improves reach accuracy in two ways. It enables the use of central vision at the end of movement, and it allows the use of extraretinal information in guiding the hand to the target. Here we tested whether fixating the reach target further facilitates reach accuracy by optimizing the use of peripheral vision in detecting, and rapidly responding to, reach errors during the ongoing movement. We examined automatic visuomotor corrections in response to displacements of the cursor representing the hand position as a function of gaze fixation location during unimanual goal-directed reaching. Eight fixation targets were positioned either in line with, or at different angles relative to, the straight-ahead movement direction (manipulation of fixation angle), and at different distances from the location of the visual perturbation (manipulation of fixation distance). We found that corrections were fastest and strongest when gaze was directed at the reach target compared with when gaze was directed to a different location in the workspace. We found that the gain of the visuomotor response was strongly affected by fixation angle, and to a smaller extent by fixation distance, with lower gains as the angle or distance increased. We submit that fixating the reach target improves reach accuracy by facilitating rapid visuomotor responses to reach errors viewed in peripheral vision. NEW & NOTEWORTHY It is well known that directing gaze to the reach target allows the use of foveal visual feedback and extraretinal information to improve the accuracy of reaching movements. Here we demonstrate that target fixation also optimizes rapid visuomotor corrections to reach errors viewed in peripheral vision, with the angle of gaze relative to the hand movement being a critical determinant in the gain of the visuomotor response.

Optimal integration of retinal and extra-retinal information is contingent upon trans-saccadic discontinuity

Optimal integration of retinal and extra-retinal information is contingent upon trans-saccadic discontinuity

Different gaze strategies during eye versus hand tracking of a moving target

The ability to visually track, using smooth pursuit eye movements, moving objects is critical in both perceptual and action tasks. Here, by asking participants to view a moving target or track it with their hand, we tested whether different task demands give rise to different gaze strategies. We hypothesized that during hand tracking, in comparison to eye tracking, the frequency of catch-up saccades would be lower, and the smooth pursuit gain would be greater, because it limits the loss of stable retinal and extra-retinal information due to saccades. In our study participants viewed a visual target that followed a smooth but unpredictable trajectory in a horizontal plane and were instructed to either track the target with their gaze or with a cursor controlled by a manipulandum. Although the mean distance between gaze and target was comparable in both tasks, we found, consistent with our hypothesis, an increase in smooth pursuit gain and a decrease in the frequency of catch-up saccades during hand tracking. We suggest that this difference in gaze behavior arises from different tasks demands. Whereas keeping gaze close to the target is important in both tasks, obtaining stable retinal and extra-retinal information is critical for guiding hand movement.

Quantifying the spatial extent of the corollary discharge benefit to transsaccadic visual perception.

Extraretinal information, such as corollary discharge (CD), is hypothesized to help compensate for saccade-induced visual input disruptions. However, support for this hypothesis is largely for one-dimensional transsaccadic visual changes, with little comprehensive information on the spatial characteristics. Here we systematically mapped the two-dimensional extent of this compensation by quantifying the insensitivity to different displacement metrics. Human subjects made saccades to targets positioned at different amplitudes (4° or 8°) and directions (rightward, oblique, or upward). After the saccade the initial target disappeared and, after a blank period, reappeared at a shifted location-a collinear, diagonal, or orthogonal displacement. Subjects reported the perceived shift direction, and we determined the displacement detection based on the perceptual judgments. The two-dimensional insensitivity fields resulting from the perceptual thresholds had spatial features similar to the saccadic eye movement variability: 1) scaled with movement amplitude, 2) oriented (less sensitive to the change) along the saccade vector, and 3) approximately constant in shape when normalized by movement amplitude. In addition, comparing the postsaccadic perceptual estimate of the presaccadic target location to that based solely on the postsaccade visual error showed that overall the perceptual estimate was approximately 50% more accurate and 35% less variable than estimates based solely on this visual information. However, this relationship was not uniform: The benefit of extraretinal information was observed largely for displacements with a component parallel to the saccade vector. These results suggest a graded use of extraretinal information when forming the postsaccadic perceptual evaluation of transsaccadic environmental changes.

The Role of Temporal Information in Perisaccadic Mislocalization.

In dynamic environments, it is crucial to accurately consider the timing of information. For instance, during saccades the eyes rotate so fast that even small temporal errors in relating retinal stimulation by flashed stimuli to extra-retinal information about the eyes’ orientations will give rise to substantial errors in where the stimuli are judged to be. If spatial localization involves judging the eyes’ orientations at the estimated time of the flash, we should be able to manipulate the pattern of mislocalization by altering the estimated time of the flash. We reasoned that if we presented a relevant flash within a short rapid sequence of irrelevant flashes, participants’ estimates of when the relevant flash was presented might be shifted towards the centre of the sequence. In a first experiment, we presented five bars at different positions around the time of a saccade. Four of the bars were black. Either the second or the fourth bar in the sequence was red. The task was to localize the red bar. We found that when the red bar was presented second in the sequence, it was judged to be further in the direction of the saccade than when it was presented fourth in the sequence. Could this be because the red bar was processed faster when more black bars preceded it? In a second experiment, a red bar was either presented alone or followed by two black bars. When two black bars followed it, it was judged to be further in the direction of the saccade. We conclude that the spatial localization of flashed stimuli involves judging the eye orientation at the estimated time of the flash.

Perceiving stimulus displacements across saccades

The visual world appears stable despite frequent retinal image movements caused by saccades. Many theories of visual stability assume that extraretinal eye position information is used to spatially adjust perceived locations across saccades, whereas others have proposed that visual stability depends upon coding of the relative positions of objects. McConkie and Currie (1996) proposed a refined combination of these views (called the Saccade Target Object Theory) in which the perception of stability across saccades relies on a local evaluation process centred on the saccade target object rather than on a remapping of the entire scene, with some contribution from memory for the relative positions of objects as well. Three experiments investigated the saccade target object theory, along with an alternative hypothesis that proposes that multiple objects are updated across saccades, but with variable resolution, with the saccade target object (by virtue of being the focus of attention before the saccade and residing near the fovea after the saccade) having priority in the perception of displacement. Although support was found for the saccade target object theory in Experiment 1, the results of Experiments 2 and 3 found that multiple objects are updated across saccades and that their positions are evaluated to determine perceived stability. There is an advantage for detecting displacements of the saccade target, most likely because of visual acuity or attentional focus being better near the fovea, but it is not the saccade target alone that determines the perception of stability and of displacements across saccades. Rather, multiple sources of information appear to contribute.

Optimal Multimodal Integration in Spatial Localization

Saccadic eye movements facilitate rapid and efficient exploration of visual scenes, but also pose serious challenges to establishing reliable spatial representations. This process presumably depends on extraretinal information about eye position, but it is still unclear whether afferent or efferent signals are implicated and how these signals are combined with the visual input. Using a novel gaze-contingent search paradigm with highly controlled retinal stimulation, we examined the performance of human observers in locating a previously fixated target after a variable number of saccades, a task that generates contrasting predictions for different updating mechanisms. We show that while localization accuracy is unaffected by saccades, localization precision deteriorates nonlinearly, revealing a statistically optimal combination of retinal and extraretinal signals. These results provide direct evidence for optimal multimodal integration in the updating of spatial representations and elucidate the contributions of corollary discharge signals and eye proprioception.

Error Correcting Mechanisms during Antisaccades: Contribution of Online Control during Primary Saccades and Offline Control via Secondary Saccades

Errors in eye movements can be corrected during the ongoing saccade through in-flight modifications (i.e., online control), or by programming a secondary eye movement (i.e., offline control). In a reflexive saccade task, the oculomotor system can use extraretinal information (i.e., efference copy) online to correct errors in the primary saccade, and offline retinal information to generate a secondary corrective saccade. The purpose of this study was to examine the error correction mechanisms in the antisaccade task. The roles of extraretinal and retinal feedback in maintaining eye movement accuracy were investigated by presenting visual feedback at the spatial goal of the antisaccade. We found that online control for antisaccade is not affected by the presence of visual feedback; that is whether visual feedback is present or not, the duration of the deceleration interval was extended and significantly correlated with reduced antisaccade endpoint error. We postulate that the extended duration of deceleration is a feature of online control during volitional saccades to improve their endpoint accuracy. We found that secondary saccades were generated more frequently in the antisaccade task compared to the reflexive saccade task. Furthermore, we found evidence for a greater contribution from extraretinal sources of feedback in programming the secondary “corrective” saccades in the antisaccade task. Nonetheless, secondary saccades were more corrective for the remaining antisaccade amplitude error in the presence of visual feedback of the target. Taken together, our results reveal a distinctive online error control strategy through an extension of the deceleration interval in the antisaccade task. Target feedback does not improve online control, rather it improves the accuracy of secondary saccades in the antisaccade task.

The role of temporal information in perisaccadic mislocalization

In dynamic environments, it is crucial to accurately consider the timing of information. For instance, during saccades the eyes rotate so fast that even small temporal errors in relating retinal stimulation by flashed stimuli to extra-retinal information about the eyes’ orientations will give rise to substantial errors in where the stimuli are judged to be. If spatial localization involves judging the eyes’ orientations at the estimated time of the flash, we should be able to manipulate the pattern of mislocalization by altering the estimated time of the flash. We reasoned that if we presented a relevant flash within a short rapid sequence of irrelevant flashes, participants’ estimates of when the relevant flash was presented might be shifted towards the centre of the sequence. In a first experiment, we presented five bars at different positions around the time of a saccade. Four of the bars were black. Either the second or the fourth bar in the sequence was red. The task was to localize the red bar. We found that when the red bar was presented second in the sequence, it was judged to be further in the direction of the saccade than when it was presented fourth in the sequence. Could this be because the red bar was processed faster when more black bars preceded it? In a second experiment, a red bar was either presented alone or followed by two black bars. When two black bars followed it, it was judged to be further in the direction of the saccade. We conclude that the spatial localization of flashed stimuli involves judging the eye orientation at the estimated time of the flash.

Evidence for a retinal velocity memory underlying the direction of anticipatory smooth pursuit eye movements

To compute spatially correct smooth pursuit eye movements, the brain uses both retinal motion and extraretinal signals about the eyes and head in space (Blohm and Lefèvre 2010). However, when smooth eye movements rely solely on memorized target velocity, such as during anticipatory pursuit, it is unknown if this velocity memory also accounts for extraretinal information, such as head roll and ocular torsion. To answer this question, we used a novel behavioral updating paradigm in which participants pursued a repetitive, spatially constant fixation-gap-ramp stimulus in series of five trials. During the first four trials, participants' heads were rolled toward one shoulder, inducing ocular counterroll (OCR). With each repetition, participants increased their anticipatory pursuit gain, indicating a robust encoding of velocity memory. On the fifth trial, they rolled their heads to the opposite shoulder before pursuit, also inducing changes in ocular torsion. Consequently, for spatially accurate anticipatory pursuit, the velocity memory had to be updated across changes in head roll and ocular torsion. We tested how the velocity memory accounted for head roll and OCR by observing the effects of changes to these signals on anticipatory trajectories of the memory decoding (fifth) trials. We found that anticipatory pursuit was updated for changes in head roll; however, we observed no evidence of compensation for OCR, representing the absence of ocular torsion signals within the velocity memory. This indicated that the directional component of the memory must be coded retinally and updated to account for changes in head roll, but not OCR.

Visual and non-visual contributions to perception of object movement during observer movement

Accurate estimation of object movement is difficult for moving observers, since it is unclear whether to attribute retinal motion to movement of the object or observer. Recently, we have proposed a purely visual neural mechanism (?flow parsing?) which aids in this process by attempting to globally filter retinal motion due to observer movement. Here we investigate the contributions of visual and non-visual information to object movement perception during pursuit eye movements. Participants tracked a pursuit target amongst a background of stereoscopically presented wireframe objects and made judgements about the trajectory of a probe dot moving vertically upwards on the retina (assuming perfect tracking of the target). Eye movements were recorded and trials on which tracking was poor were excluded. Extra-retinal (E) movement information was manipulated by changing the target speed. Retinal (R) movement information was manipulated by changing the relative speed between the target and background. Using a 2IFC procedure, on each trial participants saw the reference stimulus, for which R and E were in conflict (E = 3 deg/s; R = 5 deg/s ? achieved by moving the background in the opposite direction to the target at 2 deg/s) and a comparison stimulus, for which R and E were equal (E = R = 1, 2,..., 7 deg/s). Participants judged the interval in which probe movement was more vertical. If probe trajectory perception was based on extra-retinal information alone then the PSE of the recovered psychometric function would be 3 deg/s. PSEs above 3 deg/s indicate some contribution of the retinal information. For all (N=3) observers, PSEs were considerably greater than 3 deg/s and, assuming a linear combination rule, the associated estimated weights for R were between 25% and 49%.We conclude that visual self movement information is involved in the estimation of object movement, even when extra-retinal information is present.

The Oculomotor Systems Ability to Adapt to Structural Changes Caused by the Process of Senescence: A Review

Age-related binocular vision anomalies are frequently encountered during clinical examination of mature patients. Observations of both concomitant and incomitant restrictions in eye motility indicate that all oculomotor system levels are implicated, from cortical neurons down to extraocular muscles. The system can make adaptations in response to changes induced by growth and ageing, which it does by monitoring and adjusting its own performance. This adaptive mechanism, which is important for maintaining motility, spatial orientation, and perceptual stability, seems to rely on extra-retinal information about eye position in relation to the head and trunk. Receptors in the extraocular muscles and the vestibular system, assumed to contribute to this type of information, also undergo age-related changes. This may compromise their ability to assist in the adaptive process and in potential calibrations of other neural systems. Furthermore, recent observations of a dual, common, final pathway and double insertions of distal extraocular muscles suggest that muscle and tendon receptors may facilitate other, still unresolved, functions in the visual system. Consequently, age-related changes in certain mechanoreceptors may have more severe implications for ocular motility and visual functions than previously assumed. This review aims to detail some of the most frequent neurogenic and myogenic age-related changes that take place in the human oculomotor system and relevant pre-motor structures. It will also address clinical implications of these changes and the potential adaptive mechanism they initiate.