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.

Bilateral increase in MEG planar gradients prior to saccade onset.

Every time we move our eyes, the retinal locations of objects change. To distinguish the changes caused by eye movements from actual external motion of the objects, the visual system is thought to anticipate the consequences of eye movements (saccades). Single neuron recordings have indeed demonstrated changes in receptive fields before saccade onset. Although some EEG studies with human participants have also demonstrated a pre-saccadic increased potential over the hemisphere that will process a stimulus after a saccade, results have been mixed. Here, we used magnetoencephalography to investigate the timing and lateralization of visually evoked planar gradients before saccade onset. We modelled the gradients from trials with both a saccade and a stimulus as the linear combination of the gradients from two conditions with either only a saccade or only a stimulus. We reasoned that any residual gradients in the condition with both a saccade and a stimulus must be uniquely linked to visually-evoked neural activity before a saccade. We observed a widespread increase in residual planar gradients. Interestingly, this increase was bilateral, showing activity both contralateral and ipsilateral to the stimulus, i.e. over the hemisphere that would process the stimulus after saccade offset. This pattern of results is consistent with predictive pre-saccadic changes involving both the current and the future receptive fields involved in processing an attended object, well before the start of the eye movement. The active, sensorimotor coupling of vision and the oculomotor system may underlie the seamless subjective experience of stable and continuous perception.

Topographic organization of eye-position dependent gain fields in human visual cortex.

The ability to move has introduced animals with the problem of sensory ambiguity: the position of an external stimulus could change over time because the stimulus moved, or because the animal moved its receptors. This ambiguity can be resolved with a change in neural response gain as a function of receptor orientation. Here, we developed an encoding model to capture gain modulation of visual responses in high field (7 T) fMRI data. We characterized population eye-position dependent gain fields (pEGF). The information contained in the pEGFs allowed us to reconstruct eye positions over time across the visual hierarchy. We discovered a systematic distribution of pEGF centers: pEGF centers shift from contra- to ipsilateral following pRF eccentricity. Such a topographical organization suggests that signals beyond pure retinotopy are accessible early in the visual hierarchy, providing the potential to solve sensory ambiguity and optimize sensory processing information for functionally relevant behavior.

The Neurobiological Correlates of Gaze Perception in Healthy Individuals and Neurologic Patients.

The ability to adaptively follow conspecific eye movements is crucial for establishing shared attention and survival. Indeed, in humans, interacting with the gaze direction of others causes the reflexive orienting of attention and the faster object detection of the signaled spatial location. The behavioral evidence of this phenomenon is called gaze-cueing. Although this effect can be conceived as automatic and reflexive, gaze-cueing is often susceptible to context. In fact, gaze-cueing was shown to interact with other factors that characterize facial stimulus, such as the kind of cue that induces attention orienting (i.e., gaze or non-symbolic cues) or the emotional expression conveyed by the gaze cues. Here, we address neuroimaging evidence, investigating the neural bases of gaze-cueing and the perception of gaze direction and how contextual factors interact with the gaze shift of attention. Evidence from neuroimaging, as well as the fields of non-invasive brain stimulation and neurologic patients, highlights the involvement of the amygdala and the superior temporal lobe (especially the superior temporal sulcus (STS)) in gaze perception. However, in this review, we also emphasized the discrepancies of the attempts to characterize the distinct functional roles of the regions in the processing of gaze. Finally, we conclude by presenting the notion of invariant representation and underline its value as a conceptual framework for the future characterization of the perceptual processing of gaze within the STS.

Vision while the eyes move: Getting the full picture.

Visual information is continuously sampled from our environment, even as the eyes move, which helps the visual system create a stable view of the world.

Inhibition of return in the oculomotor decision process: Dissociating visual target discrimination from saccade readiness delays.

Saccades toward previously cued or fixated locations typically have longer latencies than those toward novel locations, a phenomenon known as inhibition of return (IOR). Despite extensive debate on its potential function, it remains unclear what the role of IOR in the oculomotor decision process is. Here, we ask whether the effect on eye movement planning is best characterized as a delay in visual target discrimination or as a reduction in readiness to execute the movement (saccade readiness). To evaluate this question, we use target-distractor tasks with clear speed-accuracy trade-offs. Simultaneously cueing both the target and distractor (or neither) we find longer latencies at the cued locations. Despite this delay in latencies, accuracy improves in line with the speed-accuracy trade-off curve (Experiment 1). This suggests that while visual target discrimination can progress unimpeded, saccade readiness is reduced. Based on this reduction in readiness we predict that the more saccades rely on visual target discrimination, the less their destination will be affected by inducing IOR. Indeed, after cueing either the target or an onset distractor (Experiment 2), short-latency, stimulus-driven, saccades are strongly biased away from the cued location, while the destinations of longer latency goal-driven saccades are affected only minimally. The fact that primarily stimulus-driven saccades are affected by inducing IOR is interesting as it can explain why the spatial bias associated with IOR is not consistently found. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Low-Level Visual Information Is Maintained across Saccades, Allowing for a Postsaccadic Handoff between Visual Areas.

Experience seems continuous and detailed despite saccadic eye movements changing retinal input several times per second. There is debate whether neural signals related to updating across saccades contain information about stimulus features, or only location pointers without visual details. We investigated the time course of low-level visual information processing across saccades by decoding the spatial frequency of a stationary stimulus that changed from one visual hemifield to the other because of a horizontal saccadic eye movement. We recorded magnetoencephalography while human subjects (both sexes) monitored the orientation of a grating stimulus, making spatial frequency task irrelevant. Separate trials, in which subjects maintained fixation, were used to train a classifier, whose performance was then tested on saccade trials. Decoding performance showed that spatial frequency information of the presaccadic stimulus remained present for ∼200 ms after the saccade, transcending retinotopic specificity. Postsaccadic information ramped up rapidly after saccade offset. There was an overlap of over 100 ms during which decoding was significant from both presaccadic and postsaccadic processing areas. This suggests that the apparent richness of perception across saccades may be supported by the continuous availability of low-level information with a "soft handoff" of information during the initial processing sweep of the new fixation.SIGNIFICANCE STATEMENT Saccades create frequent discontinuities in visual input, yet perception appears stable and continuous. How is this discontinuous input processed resulting in visual stability? Previous studies have focused on presaccadic remapping. Here we examined the time course of processing of low-level visual information (spatial frequency) across saccades with magnetoencephalography. The results suggest that spatial frequency information is not predictively remapped but also is not discarded. Instead, they suggest a soft handoff over time between different visual areas, making this information continuously available across the saccade. Information about the presaccadic stimulus remains available, while the information about the postsaccadic stimulus has also become available. The simultaneous availability of both the presaccadic and postsaccadic information could enable rich and continuous perception across saccades.

Saccades reset the priority of visual information to access awareness.

Subjectively, we experience a stable representation of the outside world across saccades. Although previous studies have reported that presaccadically acquired visual information influences postsaccadic perception, whether such information's priority to access visual awareness is either reset by each saccade or continuous across saccades remains unclear. To investigate this issue, we combined a breaking continuous flash suppression (b-CFS) with a saccade task. Before each saccade, a grating was presented in the peripheral visual field under suppression. After the saccade, the same grating was again presented under suppression at either the retinotopically matched, the spatiotopically matched, or a control location. By measuring the duration of the grating to break through CFS into awareness after a saccade, we could compare the breakthrough times across stimuli presented at the different locations. No difference in the reaction times between the spatiotopic and control location was observed, indicating that a saccade resets the buildup of an object's priority to access visual awareness. However, a longer breakthrough time was observed for the retinotopic as compared to the control location, suggesting that a form of retinotopic adaptation to the grating suppressed the priority to access visual awareness after a saccade.

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.

Trans-saccadic memory after right parietal brain damage.

INTRODUCTION: Spatial remapping, the process of updating information across eye movements, is an important mechanism for trans-saccadic perception. The right posterior parietal cortex (PPC) is a region that has been associated most strongly with spatial remapping. The aim of the project was to investigate the effect of damage to the right PPC on direction specific trans-saccadic memory. We compared trans-saccadic memory performance for central items that had to be remembered while making a left- versus rightward eye movement, or for items that were remapped within the left versus right visual field. METHODS: We included 9 stroke patients with unilateral right PPC lesions and 31 healthy control subjects. Participants memorized the location of a briefly presented item, had to make one saccade (either towards the left or right, or upward or downward), and subsequently had to decide in what direction the probe had shifted. We used a staircase to adjust task difficulty (i.e., the distance between the memory item and probe). Bayesian repeated measures ANOVAs were used to compare left versus right eye movements and items in the left versus right visual field. RESULTS: In both conditions, patients with right PPC damage showed worse trans-saccadic memory performance compared to healthy control subjects (for the condition with left- and rightward gaze shifts, BF10 = 3.79; and when items were presented left or right, BF10 = 6.77), regardless of the direction of the gaze or the initial location of the memory item. At the individual level, none of the patients showed a direction specific deficit after leftward versus rightward saccades, whereas two patients showed worse performance for items in the left versus right visual field. CONCLUSION: Damage in the right PPC did not lead to gaze direction specific impairments in trans-saccadic memory, but instead caused more general spatial memory impairments.

Time course of spatiotopic updating across saccades.

Humans move their eyes several times per second, yet we perceive the outside world as continuous despite the sudden disruptions created by each eye movement. To date, the mechanism that the brain employs to achieve visual continuity across eye movements remains unclear. While it has been proposed that the oculomotor system quickly updates and informs the visual system about the upcoming eye movement, behavioral studies investigating the time course of this updating suggest the involvement of a slow mechanism, estimated to take more than 500 ms to operate effectively. This is a surprisingly slow estimate, because both the visual system and the oculomotor system process information faster. If spatiotopic updating is indeed this slow, it cannot contribute to perceptual continuity, because it is outside the temporal regime of typical oculomotor behavior. Here, we argue that the behavioral paradigms that have been used previously are suboptimal to measure the speed of spatiotopic updating. In this study, we used a fast gaze-contingent paradigm, using high phi as a continuous stimulus across eye movements. We observed fast spatiotopic updating within 150 ms after stimulus onset. The results suggest the involvement of a fast updating mechanism that predictively influences visual perception after an eye movement. The temporal characteristics of this mechanism are compatible with the rate at which saccadic eye movements are typically observed in natural viewing.

Feature integration is unaffected by saccade landing point, even when saccades land outside of the range of regular oculomotor variance.

The experience of our visual surroundings appears continuous, contradicting the erratic nature of visual processing due to saccades. A possible way the visual system can construct a continuous experience is by integrating presaccadic and postsaccadic visual input. However, saccades rarely land exactly at the intended location. Feature integration would therefore need to be robust against variations in saccade execution to facilitate visual continuity. In the current study, observers reported a feature (color) of the saccade target, which occasionally changed slightly during the saccade. In transsaccadic change-trials, observers reported a mixture of the pre- and postsaccadic color, indicating transsaccadic feature integration. Saccade landing distance was not a significant predictor of the reported color. Next, to investigate the influence of more extreme deviations of saccade landing point on color reports, we used a global effect paradigm in a second experiment. In global effect trials, a distractor appeared together with the saccade target, causing most saccades to land in between the saccade target and the distractor. Strikingly, even when saccades land further away (up to 4°) from the saccade target than one would expect under single target conditions, there was no effect of saccade landing point on the reported color. We reason that saccade landing point does not affect feature integration, due to dissociation between the intended saccade target and the actual saccade landing point. Transsaccadic feature integration seems to be a mechanism that is dependent on visual spatial attention, and, as a result, is robust against variance in saccade landing point.

Object files across eye movements: Previous fixations affect the latencies of corrective saccades.

One of the factors contributing to a seamless visual experience is object correspondence-that is, the integration of pre- and postsaccadic visual object information into one representation. Previous research had suggested that before the execution of a saccade, a target object is loaded into visual working memory and subsequently is used to locate the target object after the saccade. Until now, studies on object correspondence have not taken previous fixations into account. In the present study, we investigated the influence of previously fixated information on object correspondence. To this end, we adapted a gaze correction paradigm in which a saccade was executed toward either a previously fixated or a novel target. During the saccade, the stimuli were displaced such that the participant's gaze landed between the target stimulus and a distractor. Participants then executed a corrective saccade to the target. The results indicated that these corrective saccades had lower latencies toward previously fixated than toward nonfixated targets, indicating object-specific facilitation. In two follow-up experiments, we showed that presaccadic spatial and object (surface feature) information can contribute separately to the execution of a corrective saccade, as well as in conjunction. Whereas the execution of a corrective saccade to a previously fixated target object at a previously fixated location is slowed down (i.e., inhibition of return), corrective saccades toward either a previously fixated target object or a previously fixated location are facilitated. We concluded that corrective saccades are executed on the basis of object files rather than of unintegrated feature information.

Spatiotopic updating facilitates perception immediately after saccades.

As the neural representation of visual information is initially coded in retinotopic coordinates, eye movements (saccades) pose a major problem for visual stability. If no visual information were maintained across saccades, retinotopic representations would have to be rebuilt after each saccade. It is currently strongly debated what kind of information (if any at all) is accumulated across saccades, and when this information becomes available after a saccade. Here, we use a motion illusion to examine the accumulation of visual information across saccades. In this illusion, an annulus with a random texture slowly rotates, and is then replaced with a second texture (motion transient). With increasing rotation durations, observers consistently perceive the transient as large rotational jumps in the direction opposite to rotation direction (backward jumps). We first show that accumulated motion information is updated spatiotopically across saccades. Then, we show that this accumulated information is readily available after a saccade, immediately biasing postsaccadic perception. The current findings suggest that presaccadic information is used to facilitate postsaccadic perception and are in support of a forward model of transsaccadic perception, aiming at anticipating the consequences of eye movements and operating within the narrow perisaccadic time window.

Spatial inhibition of return as a function of fixation history, task, and spatial references.

In oculomotor selection, each saccade is thought to be automatically biased toward uninspected locations, inhibiting the inefficient behavior of repeatedly refixating the same objects. This automatic bias is related to inhibition of return (IOR). Although IOR seems an appealing property that increases efficiency in visual search, such a mechanism would not be efficient in other tasks. Indeed, evidence for additional, more flexible control over refixations has been provided. Here, we investigated whether task demands implicitly affect the rate of refixations. We measured the probability of refixations after series of six binary saccadic decisions under two conditions: visual search and free viewing. The rate of refixations seems influenced by two effects. One effect is related to the rate of intervening fixations, specifically, more refixations were observed with more intervening fixations. In addition, we observed an effect of task set, with fewer refixations in visual search than in free viewing. Importantly, the history-related effect was more pronounced when sufficient spatial references were provided, suggesting that this effect is dependent on spatiotopic encoding of previously fixated locations. This known history-related bias in gaze direction is not the primary influence on the refixation rate. Instead, multiple factors, such as task set and spatial references, assert strong influences as well.