Pre-saccadic shifts of attention in individuals diagnosed with schizophrenia.

INTRODUCTION: Pathophysiological theories of schizophrenia (SZ) symptoms posit an abnormality in using predictions to guide behavior. One such prediction is based on imminent movements, via corollary discharge signals (CD) that relay information about planned movement kinematics to sensory brain regions. Empirical evidence suggests a reduced influence of sensorimotor predictions in individuals with SZ within multiple sensory systems, including in the visual system. One function of CD in the visual system is to selectively enhance visual sensitivity at the location of planned eye movements (pre-saccadic attention), thus enabling a prediction of the to-be-foveated stimulus. We expected pre-saccadic attention shifts to be less pronounced in individuals with SZ than in healthy controls (HC), resulting in unexpected sensory consequences of eye movements, which may relate to symptoms than can be explained in the context of altered allocation of attention. METHODS: We examined this question by testing 30 SZ and 30 HC on a pre-saccadic attention task. On each trial participants made a saccade to a cued location in an array of four stimuli. A discrimination target that was either congruent or incongruent with the cued location was briefly presented after the cue, during saccade preparation. Pre-saccadic attention was quantified by comparing accuracy on congruent trials to incongruent trials within the interval preceding the saccade. RESULTS: Although SZs were less accurate overall, the magnitude of the pre-saccadic attention effect generally did not differ across groups nor show a convincing relationship with symptom severity. We did, however, observe that SZ had reduced pre-saccadic attention effects when the discrimination target (probe) was presented at early stages of saccade planning, when pre-saccadic attention effects first emerged in HC. CONCLUSION: These findings suggest generally intact pre-saccadic shifts of attention in SZ, albeit slightly delayed. Results contribute to our understanding of altered sensory predictions in people with schizophrenia.

Abnormal Oculomotor Corollary Discharge Signaling as a Trans-diagnostic Mechanism of Psychosis.

BACKGROUND AND HYPOTHESIS: Corollary discharge (CD) signals are "copies" of motor signals sent to sensory areas to predict the corresponding input. They are a posited mechanism enabling one to distinguish actions generated by oneself vs external forces. Consequently, altered CD is a hypothesized mechanism for agency disturbances in psychosis. Previous studies have shown a decreased influence of CD signals on visual perception in individuals with schizophrenia-particularly in those with more severe positive symptoms. We therefore hypothesized that altered CD may be a trans-diagnostic mechanism of psychosis. STUDY DESIGN: We examined oculomotor CD (using the blanking task) in 49 participants with schizophrenia or schizoaffective disorder (SZ), 36 bipolar participants with psychosis (BPP), and 40 healthy controls (HC). Participants made a saccade to a visual target. Upon saccade initiation, the target disappeared and reappeared at a horizontally displaced position. Participants indicated the direction of displacement. With intact CD, participants can make accurate perceptual judgements. Otherwise, participants may use saccade landing site as a proxy of pre-saccadic target to inform perception. Thus, multi-level modeling was used to examine the influence of target displacement and saccade landing site on displacement judgements. STUDY RESULTS: SZ and BPP were equally less sensitive to target displacement than HC. Moreover, regardless of diagnosis, SZ and BPP with more severe positive symptoms were more likely to rely on saccade landing site. CONCLUSIONS: These results suggest that altered CD may be a trans-diagnostic mechanism of psychosis.

Saccadic selection in visual working memory is robust across the visual field and linked to saccade metrics: Evidence from nine experiments and more than 100,000 trials.

Visual working memory and actions are closely intertwined. Memory can guide our actions, but actions also impact what we remember. Even during memory maintenance, actions such as saccadic eye movements select content in visual working memory, resulting in better memory at locations that are congruent with the action goal as compared to incongruent locations. Here, we further substantiate the claim that saccadic eye movements are fundamentally linked to visual working memory by analyzing a large data set (> 100k trials) of nine experiments (eight of them previously published). Using Bayesian hierarchical models, we demonstrate robust saccadic selection across the full range of probed saccade directions, manifesting as better memory performance at the saccade goal irrespective of its location in the visual field. By inspecting individual differences in saccadic selection, we show that saccadic selection was highly prevalent in the population. Moreover, both saccade metrics and visual working memory performance varied considerably across the visual field. Crucially, however, both idiosyncratic and systematic visual field anisotropies were not correlated between visual working memory and the oculomotor system, suggesting that they resulted from different sources (e.g., rely on separate spatial maps). In stark contrast, trial-by-trial variations in saccade metrics were strongly associated with memory performance: At any given location, shorter saccade latencies and more accurate saccades were associated with better memory performance, undergirding a robust link between action selection and visual memory. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Orienting attention across binocular disparity.

The spatial distribution of covert visual attention following an exogenous cue is often described as a spotlight, which disregards depth. Here, we study the orienting of attention across binocular disparity, a key depth cue in primates. A small Gabor patch target was displayed at ±12-arcmin horizontal offset in each eye independently, resulting in four possible 3D locations. With some latency relative to target onset (0-300 ms), an attentional cue was displayed at one of five binocular locations, resulting in various combinations of relative azimuth (horizontal position) and disparity (depth). Observers' task was to discriminate the orientation of the target. Observers' performance decreased as the relative azimuth between the cue and the target increased. Performance also decreased with the difference in disparity, even when the azimuth remained constant. Performance varied with the delay between the cue and the target and was maximal between 100 and 150 ms. The orienting of attention in azimuth and depth followed the same time course. We mapped the 3D shape of attentional focus over time and found that the spatial envelope was approximately a Gaussian modulated in time. These results could not be explained by monocular confounds nor by eye movements. We conclude that exogenous cues direct attention not only to their visual direction but also to their depth and that binocular disparity is sufficient to define that depth. The identical time course and interaction between azimuth and depth suggest a shared mechanism, and therefore that visual attention to spatial location is an intrinsically 3D process.

Perceptual learning across saccades: Feature but not location specific.

Perceptual learning is the ability to enhance perception through practice. The hallmark of perceptual learning is its specificity for the trained location and stimulus features, such as orientation. For example, training in discriminating a grating's orientation improves performance only at the trained location but not in other untrained locations. Perceptual learning has mostly been studied using stimuli presented briefly while observers maintained gaze at one location. However, in everyday life, stimuli are actively explored through eye movements, which results in successive projections of the same stimulus at different retinal locations. Here, we studied perceptual learning of orientation discrimination across saccades. Observers were trained to saccade to a peripheral grating and to discriminate its orientation change that occurred during the saccade. The results showed that training led to transsaccadic perceptual learning (TPL) and performance improvements which did not generalize to an untrained orientation. Remarkably, however, for the trained orientation, we found a complete transfer of TPL to the untrained location in the opposite hemifield suggesting high flexibility of reference frame encoding in TPL. Three control experiments in which participants were trained without saccades did not show such transfer, confirming that the location transfer was contingent upon eye movements. Moreover, performance at the trained location, but not at the untrained location, was also improved in an untrained fixation task. Our results suggest that TPL has both, a location-specific component that occurs before the eye movement and a saccade-related component that involves location generalization.

Objects guide human gaze behavior in dynamic real-world scenes.

The complexity of natural scenes makes it challenging to experimentally study the mechanisms behind human gaze behavior when viewing dynamic environments. Historically, eye movements were believed to be driven primarily by space-based attention towards locations with salient features. Increasing evidence suggests, however, that visual attention does not select locations with high saliency but operates on attentional units given by the objects in the scene. We present a new computational framework to investigate the importance of objects for attentional guidance. This framework is designed to simulate realistic scanpaths for dynamic real-world scenes, including saccade timing and smooth pursuit behavior. Individual model components are based on psychophysically uncovered mechanisms of visual attention and saccadic decision-making. All mechanisms are implemented in a modular fashion with a small number of well-interpretable parameters. To systematically analyze the importance of objects in guiding gaze behavior, we implemented five different models within this framework: two purely spatial models, where one is based on low-level saliency and one on high-level saliency, two object-based models, with one incorporating low-level saliency for each object and the other one not using any saliency information, and a mixed model with object-based attention and selection but space-based inhibition of return. We optimized each model's parameters to reproduce the saccade amplitude and fixation duration distributions of human scanpaths using evolutionary algorithms. We compared model performance with respect to spatial and temporal fixation behavior, including the proportion of fixations exploring the background, as well as detecting, inspecting, and returning to objects. A model with object-based attention and inhibition, which uses saliency information to prioritize between objects for saccadic selection, leads to scanpath statistics with the highest similarity to the human data. This demonstrates that scanpath models benefit from object-based attention and selection, suggesting that object-level attentional units play an important role in guiding attentional processing.

An interactive motion perception tool for kindergarteners (and vision scientists).

We implement Adelson and Bergen's spatiotemporal energy model with extension to three-dimensional (x-y-t) in an interactive tool. It helps gain an easy understanding of early (first-order) visual motion perception. We demonstrate its usefulness in explaining an assortment of phenomena, including some that are typically not associated with the spatiotemporal energy model.

Temporal and spatial reference frames in visual working memory are defined by ordinal and relational properties.

Natural environments provide a rich spatiotemporal context that allows for visual objects to be differentiated based on different types of information: their absolute or relative spatial or temporal coordinates, or their ordinal positions in a spatial or temporal sequence. Here, we investigated which spatial and temporal properties are incidentally encoded along with to-be-remembered features to provide reference frames in visual working memory (VWM). We tested the different possibilities in a spatiotemporal color change-detection task by transforming spatial and/or temporal structures of item presentation at retrieval relative to encoding. More precisely, spatial and/or temporal coordinates were (a) switched, changing the order of items in a spatial or temporal sequence (ordinal transformation); (b) multiplied by different factors, changing interitem distances (relational transformation); or (c) multiplied by a constant factor, expanding or shrinking the entire configuration (global transformation). Such transformations of the external reference frame at retrieval should only interfere with VWM if the internal reference frame relies on the spatial or temporal properties affected by the respective transformation. We found that ordinal and relational transformations of either the spatial or temporal structure impaired performance, whereas global transformations did not. Thus, reference frames appear to be primarily defined by interitem relations-including relative distances between items as well as their order-rather than absolute positions in space or time. These results corroborate and extend previous findings for the spatial domain, and highlight functional similarities of the spatial and temporal dimensions in VWM by revealing the same metrical properties for temporal reference frames. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Foveal vision anticipates defining features of eye movement targets.

High-acuity foveal processing is vital for human vision. Nonetheless, little is known about how the preparation of large-scale rapid eye movements (saccades) affects visual sensitivity in the center of gaze. Based on findings from passive fixation tasks, we hypothesized that during saccade preparation, foveal processing anticipates soon-to-be fixated visual features. Using a dynamic large-field noise paradigm, we indeed demonstrate that defining features of an eye movement target are enhanced in the pre-saccadic center of gaze. Enhancement manifested as higher Hit Rates for foveal probes with target-congruent orientation and a sensitization to incidental, target-like orientation information in foveally presented noise. Enhancement was spatially confined to the center of gaze and its immediate vicinity, even after parafoveal task performance had been raised to a foveal level. Moreover, foveal enhancement during saccade preparation was more pronounced and developed faster than enhancement during passive fixation. Based on these findings, we suggest a crucial contribution of foveal processing to trans-saccadic visual continuity: Foveal processing of saccade targets commences before the movement is executed and thereby enables a seamless transition once the center of gaze reaches the target.

Oculomotor freezing indicates conscious detection free of decision bias.

The appearance of a salient stimulus rapidly and automatically inhibits saccadic eye movements. Curiously, this "oculomotor freezing" response is triggered only by stimuli that the observer reports seeing. It remains unknown, however, whether oculomotor freezing is linked to the observer's sensory experience or their decision that a stimulus was present. To dissociate between these possibilities, we manipulated decision criterion via monetary payoffs and stimulus probability in a detection task. These manipulations greatly shifted observers' decision criteria but did not affect the degree to which microsaccades were inhibited by stimulus presence. Moreover, the link between oculomotor freezing and explicit reports of stimulus presence was stronger when the criterion was conservative rather than liberal. We conclude that the sensory threshold for oculomotor freezing is independent of decision bias. Provided that conscious experience is also unaffected by such bias, oculomotor freezing is an implicit indicator of sensory awareness.NEW & NOTEWORTHY Sometimes a visual stimulus reaches awareness, and sometimes it does not. To understand why, we need objective, bias-free measures of awareness. We discovered that a reflexive freezing of small eye movements indicates when an observer detects a stimulus. Furthermore, when we biased observers' decisions to report seeing the stimulus, the oculomotor response was unaltered. This suggests that the threshold for conscious perception is independent of the decision criterion and is revealed by oculomotor freezing.

A direct comparison of attentional orienting to spatial and temporal positions in visual working memory.

Different visual attributes effectively guide attention to specific items in visual working memory (VWM), ensuring that particularly important memory contents are readily available. Predictable temporal structures contribute to this efficient use of VWM: items are prospectively prioritized when they are expected to be needed. Occasionally, however, visual events only gain relevance through their timing after they have passed. We investigated retrospective attentional orienting based on temporal position by directly comparing it with orienting to spatial locations, which is typically considered the most powerful selection mechanism. In a colour-change-detection task, in which items appeared sequentially at different locations, symbolic number cues validly indicated the temporal or spatial location of the upcoming probe item either before encoding (precues; Experiment 1) or during maintenance (retrocues; Experiments 1-3). Temporal and spatial cues were physically identical and only differed in their mapping onto either temporal or spatial positions. Predictive cues yielded cueing benefits (i.e., higher accuracy and shorter reaction times) as compared with neutral cues, with larger benefits for precues than for retrocues. Importantly, spatial and temporal cueing benefits did not differ. Equivalent retrocueing benefits were also observed across different cue-probe intervals and irrespective of whether spatial or temporal position was used as retrieval cue, indicating that items were directly bound to temporal position and not prioritized via a space-based mechanism. These findings show that spatial and temporal properties can be used equally well to flexibly prioritise representations held in VWM and they highlight the functional similarities of space and time in VWM.

Moving fast and seeing slow? The visual consequences of vigorous movement.

In active agents, sensory and motor processes form an inevitable bond. This wedding is particularly striking for saccadic eye movements - the prime target of Shadmehr and Ahmed's thesis - which impose frequent changes on the retinal image. Changes in movement vigor (latency and speed), therefore, will need to be accompanied by changes in visual and attentional processes. We argue that the mechanisms that control movement vigor may also enable vision to attune to changes in movement kinematics.

Oculomotor corollary discharge signaling is related to repetitive behavior in children with autism spectrum disorder.

Corollary discharge (CD) signals are "copies" of motor signals sent to sensory regions that allow animals to adjust sensory consequences of self-generated actions. Autism spectrum disorder (ASD) is characterized by sensory and motor deficits, which may be underpinned by altered CD signaling. We evaluated oculomotor CD using the blanking task, which measures the influence of saccades on visual perception, in 30 children with ASD and 35 typically developing (TD) children. Participants were instructed to make a saccade to a visual target. Upon saccade initiation, the presaccadic target disappeared and reappeared to the left or right of the original position. Participants indicated the direction of the jump. With intact CD, participants can make accurate perceptual judgements. Otherwise, participants may use saccade landing site as a proxy of the presaccadic target and use it to inform perception. We used multilevel modeling to examine the influence of saccade landing site on trans-saccadic perceptual judgements. We found that, compared with TD participants, children with ASD were more sensitive to target displacement and less reliant on saccade landing site when spatial uncertainty of the post-saccadic target was high. This pattern was driven by ASD participants with less severe restricted and repetitive behaviors. These results suggest a relationship between altered CD signaling and core ASD symptoms.

Intrasaccadic motion streaks jump-start gaze correction.

Rapid eye movements (saccades) incessantly shift objects across the retina. To establish object correspondence, the visual system is thought to match surface features of objects across saccades. Here, we show that an object's intrasaccadic retinal trace-a signal previously considered unavailable to visual processing-facilitates this match making. Human observers made saccades to a cued target in a circular stimulus array. Using high-speed visual projection, we swiftly rotated this array during the eyes' flight, displaying continuous intrasaccadic target motion. Observers' saccades landed between the target and a distractor, prompting secondary saccades. Independently of the availability of object features, which we controlled tightly, target motion increased the rate and reduced the latency of gaze-correcting saccades to the initial presaccadic target, in particular when the target's stimulus features incidentally gave rise to efficient motion streaks. These results suggest that intrasaccadic visual information informs the establishment of object correspondence and jump-starts gaze correction.

Pre-saccadic attention spreads to stimuli forming a perceptual group with the saccade target.

The pre-saccadic attention shift-a rapid increase in visual sensitivity at the target-is an inevitable precursor of saccadic eye movements. Saccade targets are often parts of the objects that are of interest to the active observer. Although the link between saccades and covert attention shifts is well established, it remains unclear if pre-saccadic attention selects the location of the eye movement target or rather the entire object that occupies this location. Indeed, several neurophysiological studies suggest that attentional modulations of neural activity in visual cortex spreads across parts of objects (e.g., elements grouped by Gestalt principles) that contain the target location of a saccade. To understand the nature of pre-saccadic attentional selection, we examined how visual sensitivity, measured in a challenging orientation discrimination task, changes during saccade preparation at locations that are perceptually grouped with the saccade target. In Experiment 1, using grouping by color in a delayed-saccade task, we found no consistent spread of attention to locations that formed a perceptual group with the saccade target. However, performance depended on the side of the stimulus arrangement relative to the saccade target location, an effect we discuss with respect to attentional momentum. In Experiment 2, employing stronger perceptual grouping cues (color and motion) and an immediate-saccade task, we obtained a reliable grouping effect: Attention spread to locations that were perceptually grouped with the saccade target while saccade preparation was underway. We also replicated the side effect observed in Experiment 1. These results provide evidence that the pre-saccadic attention spreads beyond the target location along the saccade direction, and selects scene elements that-based on Gestalt criteria-are likely to belong to the same object as the saccade target.

The peripheral sensitivity profile at the saccade target reshapes during saccade preparation.

Goal-directed eye movements (saccades) bring peripheral objects of interest into high-acuity foveal vision. In preparation for the incoming foveal image, the perception of the saccade target may sharpen gradually before the eye movement is executed. Indeed, previous studies suggest that pre-saccadic attention shifts enhance sensitivity to high spatial frequencies (SFs) more than sensitivity to lower SFs. This pattern, however, was observed within a narrow frequency range and may reflect local changes in the shape of a broader underlying sensitivity profile. Depending on the development of the profile's shape, SFs above the previously examined range may profit less from saccade preparation. To assess the impact of saccade preparation on the shape of a broader sensitivity profile, we prompted observers to discriminate the orientation of a sinusoidal grating (the probe) presented briefly at the target of an impending saccade, at 10 dva (degree of visual angle) eccentricity. The probe's SF ranged from 1 to 5.5 cycles per dva (cpd) and was unpredictable on a given trial. We fitted observers' response accuracies across SFs with a log-parabolic, that is, inverted U-shaped function. Long before saccade onset, the profile peaked at .6 cpd and dropped off towards lower and higher SFs with broad bandwidth. During saccade preparation, the peak of the profile increased and shifted towards higher SFs while the bandwidth of the profile decreased. As a consequence of this reshaping process, pre-saccadic enhancement increased with SF up to 2.5 cpd, corroborating previous findings. Sensitivities to higher SFs, however, profited less from saccade preparation. We conclude that the extent of pre-saccadic enhancement to a particular SF is governed by its position on a broader sensitivity profile which reshapes substantially during saccade preparation. The shift of the profile's peak towards higher SFs increases resolution at the saccade target even when the features of relevant visual information are unpredictable.

Incidental encoding of visual information in temporal reference frames in working memory.

Visual events are structured in space and time, yet models of visual working memory (VWM) have largely relied on tasks emphasizing spatial aspects. Here, we show that temporal properties of visual events are incidentally encoded along with spatial properties. In five experiments, participants performed change-detection tasks, in which items had unique spatial and temporal coordinates at encoding. Crucially, neither space nor time was task-relevant. The key manipulation concerned the retrieval context: The test array was identical to the memory array either in its entire spatiotemporal structure, or only its spatial or temporal structure. Removing spatial or temporal information at retrieval resulted in costs, indicating that memory relied on both spatial and temporal context in which items were initially perceived. Encoding of spatiotemporal structure occurred incidentally, not strategically, as it was robust even when the retrieval context was perfectly predictable. However, spatial and temporal inter-item spacings influenced the weighting of spatial and temporal information: It favoured the domain in which items were more widely spaced, facilitating their individuation and, likely, access to representations. Across individuals, the weighting of spatial and temporal information varied substantially, but it remained consistent across sessions, suggesting stable preferences for coding in the spatial or temporal domain. No comparable incidental encoding occurred for other task-irrelevant feature dimensions (size or colour). We propose that temporal structure serves as fundamental a function in VWM as spatial structure, scaffolding events that unfold over time.

Intra-saccadic motion streaks as cues to linking object locations across saccades.

When visual objects shift rapidly across the retina, they produce motion blur. Intra-saccadic visual signals, caused incessantly by our own saccades, are thought to be eliminated at early stages of visual processing. Here we investigate whether they are still available to the visual system and could-in principle-be used as cues for localizing objects as they change locations on the retina. Using a high-speed projection system, we developed a trans-saccadic identification task in which brief but continuous intra-saccadic object motion was key to successful performance. Observers made a saccade to a target stimulus that moved rapidly either up or down, strictly during the eye movement. Just as the target reached its final position, an identical distractor stimulus appeared on the opposite side, resulting in a display of two identical stimuli upon saccade landing. Observers had to identify the original target using the only available clue: the target's intra-saccadic movement. In an additional replay condition, we presented the observers' own intra-saccadic retinal stimulus trajectories during fixation. Compared to the replay condition, task performance was impaired during saccades but recovered fully when a post-saccadic blank was introduced. Reverse regression analyses and confirmatory experiments showed that performance increased markedly when targets had long movement durations, low spatial frequencies, and orientations parallel to their retinal trajectory-features that promote intra-saccadic motion streaks. Although the potential functional role of intra-saccadic visual signals is still unclear, our results suggest that they could provide cues to tracking objects that rapidly change locations across saccades.

A comparison of the temporal and spatial properties of trans-saccadic perceptual recalibration and saccadic adaptation.

Repeated exposure to a consistent trans-saccadic step in the position of the saccadic target reliably produces a change of saccadic gain, a well-established trans-saccadic motor learning phenomenon known as saccadic adaptation. Trans-saccadic changes can also produce perceptual effects. Specifically, a systematic increase or decrease in the size of the object that is being foveated changes the perceptually equivalent size between fovea and periphery. Previous studies have shown that this recalibration of perceived size can be established within a few dozen trials, persists overnight, and generalizes across hemifields. In the current study, we use a novel adjustment paradigm to characterize both temporally and spatially the learning process that subtends this form of recalibration, and directly compare its properties to those of saccadic adaptation. We observed that sinusoidal oscillations in the amplitude of the trans-saccadic change produce sinusoidal oscillations in the reported peripheral size, with a lag of under 10 trials. This is qualitatively similar to what has been observed in the case of saccadic adaptation. We also tested whether learning is generalized to the mirror location on the opposite hemifield for both size recalibration and saccade adaptation. Here the results were markedly different, showing almost complete generalization for recalibration and no generalization for saccadic adaptation. We conclude that perceptual and visuomotor consequences of trans-saccadic changes rely on learning mechanisms that are distinct but develop on similar time scales.