Extraretinal Signals Research Articles

Predictive posture stabilization before contact with moving objects: equivalence of smooth pursuit tracking and peripheral vision.

Postural stabilization is essential to effectively interact with our environment. Humans preemptively adjust their posture to counteract impending disturbances, such as those encountered during interactions with moving objects, a phenomenon known as anticipatory postural adjustments (APAs). APAs are thought to be influenced by predictive models that incorporate object motion via retinal motion and extraretinal signals. Building on our previous work that examined APAs in relation to the perceived momentum of moving objects, here we explored the impact of object motion within different visual field sectors on the human capacity to anticipate motion and prepare APAs for contact between virtual moving objects and the limb. Participants interacted with objects moving toward them under different gaze conditions. In one condition, participants fixated on either a central point (central fixation) or left-right of the moving object (peripheral fixation), whereas in another, they followed the moving object with smooth pursuit eye movements (SPEMs). We found that APAs had the smallest magnitude in the central fixation condition and that no notable differences in APAs were apparent between the SPEM and peripheral fixation conditions. This suggests that the visual system can accurately perceive motion of objects in peripheral vision for posture stabilization. Using Bayesian model averaging, we also evaluated the contribution of different gaze variables, such as eye velocity and gain (ratio of eye and object velocity) and showed that both eye velocity and gain signals were significant predictors of APAs. Taken together, our study underscores the roles of oculomotor signals in the modulation of APAs.NEW & NOTEWORTHY We show that the human visuomotor system can detect motion in peripheral vision and make anticipatory adjustments to posture before contact with moving objects, just as effectively as when the eye movement system tracks those objects with smooth pursuit eye movements. These findings pave the way for research into how age-induced changes in spatial vision, eye movements, and motion perception could affect the control of limb movements and postural stability during motion-mediated interactions with objects.

Pathways from the superior colliculus and the nucleus of the optic tract to the posterior parietal cortex in macaque monkeys: Functional frameworks for representation updating and online movement guidance.

The posterior parietal cortex (PPC) integrates multisensory and motor-related information for generating and updating body representations and movement plans. We used retrograde transneuronal transfer of rabies virus combined with a conventional tracer in macaque monkeys to identify direct and disynaptic pathways to the arm-related rostral medial intraparietal area (MIP), the ventral lateral intraparietal area (LIPv), belonging to the parietal eye field, and the pursuit-related lateral subdivision of the medial superior temporal area (MSTl). We found that these areas receive major disynaptic pathways via the thalamus from the nucleus of the optic tract (NOT) and the superior colliculus (SC), mainly ipsilaterally. NOT pathways, targeting MSTl most prominently, serve to process the sensory consequences of slow eye movements for which the NOT is the key sensorimotor interface. They potentially contribute to the directional asymmetry of the pursuit and optokinetic systems. MSTl and LIPv receive feedforward inputs from SC visual layers, which are potential correlates for fast detection of motion, perceptual saccadic suppression and visual spatial attention. MSTl is the target of efference copy pathways from saccade- and head-related compartments of SC motor layers and head-related reticulospinal neurons. They are potential sources of extraretinal signals related to eye and head movement in MSTl visual-tracking neurons. LIPv and rostral MIP receive efference copy pathways from all SC motor layers, providing online estimates of eye, head and arm movements. Our findings have important implications for understanding the role of the PPC in representation updating, internal models for online movement guidance, eye-hand coordination and optic ataxia.

Autokinesis Reveals a Threshold for Perception of Visual Motion

In natural viewing conditions, the brain can optimally integrate retinal and extraretinal signals to maintain a stable visual perception. These mechanisms, however, may fail in circumstances where extraction of a motion signal is less viable such as impoverished visual scenes. This can result in a phenomenon known as autokinesis in which one may experience apparent motion of a small visual stimulus in an otherwise completely dark environment. In this study, we examined the effect of autokinesis on visual perception of motion in human observers. We used a novel method with optical tracking in which the visual motion was reported manually by the observer. Experiment results show at lower speeds of motion, the perceived direction of motion was more aligned with the effect of autokinesis, whereas in the light or at higher speeds in the dark, it was more aligned with the actual direction of motion. These findings have important implications for understanding how the stability of visual representation in the brain can affect accurate perception of motion signals.

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.

Smooth pursuit eye movements contribute to anticipatory force control during mechanical stopping of moving objects.

When stopping a closing door or catching an object, humans process the motion of inertial objects and apply reactive limb force over short period to interact with them. One way in which the visual system processes motion is through extraretinal signals associated with smooth pursuit eye movements (SPEMs). We conducted three experiments to investigate how SPEMs contribute to anticipatory and reactive hand force modulation when interacting with a virtual object moving in the horizontal plane. We hypothesized that SPEM signals are critical for timing motor responses, anticipatory control of hand force, and task performance. Participants held a robotic manipulandum and attempted to stop an approaching simulated object by applying a force impulse (area under force-time curve) that matched the object's virtual momentum upon contact. We manipulated the object's momentum by varying either its virtual mass or its speed under free gaze or constrained gaze conditions. We examined gaze variables, the timing of hand motor responses, anticipatory force control, and overall task performance. Our results show that when participants were fixated at a designated location instead of following objects with SPEM, anticipatory modulation of hand force before contact decreased. However, constraining gaze by asking participants to fixate did not seem to affect the timing of the motor response or the task performance. Together, these results suggest that SPEMs may be important for anticipatory control of hand force before contact and may also play a critical role in anticipatory stabilization of limb posture when humans interact with moving objects.NEW & NOTEWORTHY We show for the first time that smooth pursuit eye movements (SPEMs) play a role in the modulation of anticipatory control of hand force to stabilize posture against contact forces. SPEMs are critical for tracking moving objects, facilitate processing motion of moving objects, and are impacted during aging and in many neurological disorders, such as Alzheimer's disease and multiple sclerosis. These results provide a novel basis to probe how changes in SPEMs could contribute to deficient limb motor control in older adults and patients with neurological disorders.

Neurons in Primate Area MSTd Signal Eye Movement Direction Inferred from Dynamic Perspective Cues in Optic Flow.

Smooth eye movements are common during natural viewing; we frequently rotate our eyes to track moving objects or to maintain fixation on an object during self-movement. Reliable information about smooth eye movements is crucial to various neural computations, such as estimating heading from optic flow or judging depth from motion parallax. While it is well established that extraretinal signals (e.g., efference copies of motor commands) carry critical information about eye velocity, the rotational optic flow field produced by eye rotations also carries valuable information. Although previous work has shown that dynamic perspective cues in optic flow can be used in computations that require estimates of eye velocity, it has remained unclear where and how the brain processes these visual cues and how they are integrated with extraretinal signals regarding eye rotation. We examined how neurons in the dorsal region of the medial superior temporal area (MSTd) of two male rhesus monkeys represent the direction of smooth pursuit eye movements based on both visual cues (dynamic perspective) and extraretinal signals. We find that most MSTd neurons have matched preferences for the direction of eye rotation based on visual and extraretinal signals. Moreover, neural responses to combinations of these signals are well predicted by a weighted linear summation model. These findings demonstrate a neural substrate for representing the velocity of smooth eye movements based on rotational optic flow and establish area MSTd as a key node for integrating visual and extraretinal signals into a more generalized representation of smooth eye movements.SIGNIFICANCE STATEMENT We frequently rotate our eyes to smoothly track objects of interest during self-motion. Information about eye velocity is crucial for a variety of computations performed by the brain, including depth perception and heading perception. Traditionally, information about eye rotation has been thought to arise mainly from extraretinal signals, such as efference copies of motor commands. Previous work shows that eye velocity can also be inferred from rotational optic flow that accompanies smooth eye movements, but the neural origins of these visual signals about eye rotation have remained unknown. We demonstrate that macaque neurons signal the direction of smooth eye rotation based on visual signals, and that they integrate both visual and extraretinal signals regarding eye rotation in a congruent fashion.

The human middle temporal cortex responds to both active leg movements and egomotion-compatible visual motion.

The human middle-temporal region MT+ is highly specialized in processing visual motion. However, recent studies have shown that this region is modulated by extraretinal signals, suggesting a possible involvement in processing motion information also from non-visual modalities. Here, we used functional MRI data to investigate the influence of retinal and extraretinal signals on MT+ in a large sample of subjects. Moreover, we used resting-state functional MRI to assess how the subdivisions of MT+ (i.e., MST, FST, MT, and V4t) are functionally connected. We first compared responses in MST, FST, MT, and V4t to coherent vs. random visual motion. We found that only MST and FST were positively activated by coherent motion. Furthermore, regional analyses revealed that MST and FST were positively activated by leg, but not arm, movements, while MT and V4t were deactivated by arm, but not leg, movements. Taken together, regional analyses revealed a visuomotor role for the anterior areas MST and FST and a pure visual role for the anterior areas MT and V4t. These findings were mirrored by the pattern of functional connections between these areas and the rest of the brain. Visual and visuomotor regions showed distinct patterns of functional connectivity, with the latter preferentially connected with the somatosensory and motor areas representing leg and foot. Overall, these findings reveal a functional sensitivity for coherent visual motion and lower-limb movements in MST and FST, suggesting their possible involvement in integrating sensory and motor information to perform locomotion.

Exposure to Blue Light Reduces Melanopsin Expression in Intrinsically Photoreceptive Retinal Ganglion Cells and Damages the Inner Retina in Rats.

PurposeThe purpose of this study was to investigative the effects of blue light on intrinsically photoreceptive retinal ganglion cells (ipRGCs).MethodsBrown Norway rats were used. Nine rats were continuously exposed to blue light (light emitting diodes [LEDs]: 463 nm; 1000 lx) for 2 days (acute exposure [AE]); 9 rats were exposed to 12 hours of blue light and 12 hours of darkness for 10 days (long-term exposure [LTE]); 6 control rats were exposed to 12 hours of white fluorescent light (1000 lx) and 12 hours of darkness for 10 days. Whole-mount retinas were immunolabelled with melanopsin antibodies; melanopsin-positive (MP) ipRGC somas and processes were counted and measured with Neuron J. To detect apoptosis, retinal cryo-sections were stained with terminal deoxynucleotidyl transferase dUTP nick-end labeling. Ultra-thin sections were visualized with transmission electron microscopy.ResultsThe number of MP ipRGC somas was significantly lower in retinas from AE and LTE rats than in those from control rats (P < 0.001 and = 0.002, respectively). The mean length of MP areas of processes was significantly lower in AE rats (P < 0.001). AE rats had severe retinal damage and massive apoptosis in the outer nuclear layer; their mitochondria were damaged in the axons and dendrites of the nerve fiber layer and the inner plexiform layer. Retinal ganglion cells (RGCs) in AE rats appeared to have reduced amounts of free ribosomes and rough endoplasmic reticulum.ConclusionsAE to blue light reduces melanopsin expression and damages RGCs, likely including ipRGCs. Changes in the axons and dendrites of RGCs suggest possible disruption of intraretinal and extraretinal signal transmission.

Neural correlates of intra-saccadic motion perception.

Retinal motion of the visual scene is not consciously perceived during ocular saccades in normal everyday conditions. It has been suggested that extra-retinal signals actively suppress intra-saccadic motion perception to preserve stable perception of the visual world. However, using stimuli optimized to preferentially activate the M-pathway, Castet and Masson (2000) demonstrated that motion can be perceived during a saccade. Based on this psychophysical paradigm, we used electroencephalography and eye-tracking recordings to investigate the neural correlates related to the conscious perception of intra-saccadic motion. We demonstrated the effective involvement during saccades of the cortical areas V1-V2 and MT-V5, which convey motion information along the M-pathway. We also showed that individual motion perception was related to retinal temporal frequency.

Retinal error signals and fluctuations in eye velocity influence oculomotor behavior in subsequent trials.

The oculomotor system makes use of an integration of previous stimulus velocities (the prior) and current sensory inputs to adjust initial eye speeds. The present study extended this research by investigating the roles of different retinal or extra-retinal signals for this process. To test for this, participants viewed movement sequences that all ended with the same test trial. Earlier in the sequence, the prior was manipulated by presenting targets that either had different velocities, different starting positions, or target movements designed to elicit differential oculomotor behavior (tracked with or without additional corrective saccades). Additionally, these prior targets could vary in terms of contrast to manipulate reliability. When the velocity of prior trials differed from test trials, the reliability-weighted integration of prior information was replicated. When the prior trials differed in starting position, significant effects on subsequent oculomotor behavior were only observed for the reliable target. Although there were also differences in eye velocity across the different manipulations, they could not explain the observed reliability-weighted integration. When comparing the same physical prior trials but tracked with additional corrective saccades, the eye velocity in the test trial also differed systematically (slower for forward saccades, and faster for backward saccades). The direction of the observed effect contradicts the expectations based on perceived speed and eye velocity, but can be predicted by a combination of retinal velocity and position error signals. Together, these results suggest that general fluctuations in eye velocity as well as retinal error signals are related to oculomotor behavior in subsequent trials.

The Effects of Depth Cues and Vestibular Translation Signals on the Rotation Tolerance of Heading Tuning in Macaque Area MSTd.

When the eyes rotate during translational self-motion, the focus of expansion (FOE) in optic flow no longer indicates heading, yet heading judgements are largely unbiased. Much emphasis has been placed on the role of extraretinal signals in compensating for the visual consequences of eye rotation. However, recent studies also support a purely visual mechanism of rotation compensation in heading-selective neurons. Computational theories support a visual compensatory strategy but require different visual depth cues. We examined the rotation tolerance of heading tuning in macaque area MSTd using two different virtual environments, a frontoparallel (2D) wall and a 3D cloud of random dots. Both environments contained rotational optic flow cues (i.e., dynamic perspective), but only the 3D cloud stimulus contained local motion parallax cues, which are required by some models. The 3D cloud environment did not enhance the rotation tolerance of heading tuning for individual MSTd neurons, nor the accuracy of heading estimates decoded from population activity, suggesting a key role for dynamic perspective cues. We also added vestibular translation signals to optic flow, to test whether rotation tolerance is enhanced by non-visual cues to heading. We found no benefit of vestibular signals overall, but a modest effect for some neurons with significant vestibular heading tuning. We also find that neurons with more rotation tolerant heading tuning typically are less selective to pure visual rotation cues. Together, our findings help to clarify the types of information that are used to construct heading representations that are tolerant to eye rotations.

Contribution of retinal and extra-retinal signals for oculomotor priors

Contribution of retinal and extra-retinal signals for oculomotor priors

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.

The role of the posterior parietal cortex in saccadic error processing.

Ocular saccades rapidly displace the fovea from one point of interest to another, thus minimizing the loss of visual information and ensuring the seamless continuity of visual perception. However, because of intrinsic variability in sensory-motor processing, saccades often miss their intended target, necessitating a secondary corrective saccade. Behavioral evidence suggests that the oculomotor system estimates saccadic error by relying on two sources of information: the retinal feedback obtained post-saccadically and an internal extra-retinal signal obtained from efference copy or proprioception. However, the neurophysiological mechanisms underlying this process remain elusive. We trained two rhesus monkeys to perform visually guided saccades towards a target that was imperceptibly displaced at saccade onset on some trials. We recorded activity from neurons in the lateral intraparietal area (LIP), an area implicated in visual, attentional and saccadic processing. We found that a subpopulation of neurons detect saccadic motor error by firing more strongly after an inaccurate saccade. This signal did not depend on retinal feedback or on the execution of a secondary corrective saccade. Moreover, inactivating LIP led to a large and selective increase in the latency of small (i.e., natural) corrective saccade initiation. Our results indicate a key role for LIP in saccadic error processing.

Adaptive heading performance during self-motion perception.

Previous studies have documented that the perception of self-motion direction can be extracted from the patterns of image motion on the retina (also termed optic flow). Self-motion perception remains stable even when the optic-flow information is distorted by concurrent gaze shifts from body/eye rotations. This has been interpreted that extraretinal signals-efference copies of eye/body movements-are involved in compensating for retinal distortions. Here, we tested an alternative hypothesis to the extraretinal interpretation. We hypothesized that accurate self-motion perception can be achieved from a purely optic-flow-based visual strategy acquired through experience, independent of extraretinal mechanism. To test this, we asked human subjects to perform a self-motion direction discrimination task under normal optic flow (fixation condition) or distorted optic flow resulted from either realistic (pursuit condition) or simulated (simulated condition) eye movements. The task was performed either without (pre- and posttraining) or with (during training) the feedback about the correct answer. We first replicated the previous observation that before training, direction perception was greatly impaired in the simulated condition where the optic flow was distorted and extraretinal eye movement signals were absent. We further showed that after a few training sessions, the initial impairment in direction perception was gradually improved. These results reveal that behavioral training can enforce the exploitation of retinal cues to compensate for the distortion, without the contribution from the extraretinal signals. Our results suggest that self-motion perception is a flexible and adaptive process which might depend on neural plasticity in relevant cortical areas.

The eye that binds: Feature integration is not disrupted by saccadic eye movements

Feature integration theory proposes that visual features, such as shape and color, can only be combined into a unified object when spatial attention is directed to their location in retinotopic maps. Eye movements cause dramatic changes on our retinae, and are associated with obligatory shifts in spatial attention. In two experiments, we measured the prevalence of conjunction errors (that is, reporting an object as having an attribute that belonged to another object), for brief stimulus presentation before, during, and after a saccade. Planning and executing a saccade did not itself disrupt feature integration. Motion did disrupt feature integration, leading to an increase in conjunction errors. However, retinal motion of an equal extent but caused by saccadic eye movements is spared this disruption, and showed similar rates of conjunction errors as a condition with static stimuli presented to a static eye. The results suggest that extra-retinal signals are able to compensate for the motion caused by saccadic eye movements, thereby preserving the integrity of objects across saccades and preventing their features from mixing or mis-binding.

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.

Retinal Stabilization Reveals Limited Influence of Extraretinal Signals on Heading Tuning in the Medial Superior Temporal Area.

Heading perception in primates depends heavily on visual optic-flow cues. Yet during self-motion, heading percepts remain stable, even though smooth-pursuit eye movements often distort optic flow. According to theoretical work, self-motion can be represented accurately by compensating for these distortions in two ways: via retinal mechanisms or via extraretinal efference-copy signals, which predict the sensory consequences of movement. Psychophysical evidence strongly supports the efference-copy hypothesis, but physiological evidence remains inconclusive. Neurons that signal the true heading direction during pursuit are found in visual areas of monkey cortex, including the dorsal medial superior temporal area (MSTd). Here we measured heading tuning in MSTd using a novel stimulus paradigm, in which we stabilize the optic-flow stimulus on the retina during pursuit. This approach isolates the effects on neuronal heading preferences of extraretinal signals, which remain active while the retinal stimulus is prevented from changing. Our results from 3 female monkeys demonstrate a significant but small influence of extraretinal signals on the preferred heading directions of MSTd neurons. Under our stimulus conditions, which are rich in retinal cues, we find that retinal mechanisms dominate physiological corrections for pursuit eye movements, suggesting that extraretinal cues, such as predictive efference-copy mechanisms, have a limited role under naturalistic conditions.SIGNIFICANCE STATEMENT Sensory systems discount stimulation caused by an animal's own behavior. For example, eye movements cause irrelevant retinal signals that could interfere with motion perception. The visual system compensates for such self-generated motion, but how this happens is unclear. Two theoretical possibilities are a purely visual calculation or one using an internal signal of eye movements to compensate for their effects. The latter can be isolated by experimentally stabilizing the image on a moving retina, but this approach has never been adopted to study motion physiology. Using this method, we find that extraretinal signals have little influence on activity in visual cortex, whereas visually based corrections for ongoing eye movements have stronger effects and are likely most important under real-world conditions.

Learning to use vestibular sense for spatial updating is context dependent

As we move, perceptual stability is crucial to successfully interact with our environment. Notably, the brain must update the locations of objects in space using extra-retinal signals. The vestibular system is a strong candidate as a source of information for spatial updating as it senses head motion. The ability to use this cue is not innate but must be learned. To date, the mechanisms of vestibular spatial updating generalization are unknown or at least controversial. In this paper we examine generalization patterns within and between different conditions of vestibular spatial updating. Participants were asked to update the position of a remembered target following (offline) or during (online) passive body rotation. After being trained on a single spatial target position within a given task, we tested generalization of performance for different spatial targets and an unpracticed spatial updating task. The results demonstrated different patterns of generalization across the workspace depending on the task. Further, no transfer was observed from the practiced to the unpracticed task. We found that the type of mechanism involved during learning governs generalization. These findings provide new knowledge about how the brain uses vestibular information to preserve its spatial updating ability.

The influence of retinal image motion on the perceptual grouping of temporally asynchronous stimuli.

Briefly presented stimuli can reveal the lower limit of retinal-based perceptual stabilization mechanisms. This is demonstrated in perceptual grouping of temporally asynchronous stimuli, in which alternate row or column elements of a regular grid are presented over two successive display frames with an imperceptible temporal offset. The grouping phenomenon results from a subtle shift between alternate grid elements due to incomplete compensation of small, fixational eye movements occurring between the two presentation frames. This suggests that larger retinal shifts should amplify the introduced shifts between alternate grid elements and improve grouping performance. However, large shifts are necessarily absent in small eye movements. Furthermore, shifts follow a random walk, making the relationship between shift magnitude and performance difficult to explore systematically. Here, we established a systematic relationship between retinal image motion and perceptual grouping by presenting alternate grid elements (untracked) during smooth pursuit of known velocities. Our results show grouping performance to improve in direct proportion to pursuit velocity. Any potential compensation by extraretinal signals (e.g., efference copy) does not seem to occur.