Pre-saccadic Shift Of Attention Research Articles

Dissociable roles of human frontal eye fields and early visual cortex in presaccadic attention

Shortly before saccadic eye movements, visual sensitivity at the saccade target is enhanced, at the expense of sensitivity elsewhere. Some behavioral and neural correlates of this presaccadic shift of attention resemble those of covert attention, deployed during fixation. Microstimulation in non-human primates has shown that presaccadic attention modulates perception via feedback from oculomotor to visual areas. This mechanism also seems plausible in humans, as both oculomotor and visual areas are active during saccade planning. We investigated this hypothesis by applying TMS to frontal or visual areas during saccade preparation. By simultaneously measuring perceptual performance, we show their causal and differential roles in contralateral presaccadic attention effects: Whereas rFEF+ stimulation enhanced sensitivity opposite the saccade target throughout saccade preparation, V1/V2 stimulation reduced sensitivity at the saccade target only shortly before saccade onset. These findings are consistent with presaccadic attention modulating perception through cortico-cortical feedback and further dissociate presaccadic and covert attention.

Presaccadic attention sharpens visual acuity

Visual perception is limited by spatial resolution, the ability to discriminate fine details. Spatial resolution not only declines with eccentricity but also differs for polar angle locations around the visual field, also known as ‘performance fields'. To compensate for poor peripheral resolution, we make rapid eye movements—saccades—to bring peripheral objects into high-acuity foveal vision. Already before saccade onset, visual attention shifts to the saccade target location and prioritizes visual processing. This presaccadic shift of attention improves performance in many visual tasks, but whether it changes resolution is unknown. Here, we investigated whether presaccadic attention sharpens peripheral spatial resolution; and if so, whether such effect interacts with performance fields asymmetries. We measured acuity thresholds in an orientation discrimination task during fixation and saccade preparation around the visual field. The results revealed that presaccadic attention sharpens acuity, which can facilitate a smooth transition from peripheral to foveal representation. This acuity enhancement is similar across the four cardinal locations; thus, the typically robust effect of presaccadic attention does not change polar angle differences in resolution.

Presaccadic attention enhances contrast sensitivity, but not at the upper vertical meridian

SummaryVisual performance has striking polar performance asymmetries: At a fixed eccentricity, it is better along the horizontal than vertical meridian and the lower than upper vertical meridian. These asymmetries are not alleviated by covert exogenous or endogenous attention, but have been studied exclusively during eye fixation. However, a major driver of everyday attentional orienting is saccade preparation, during which attention automatically shifts to the future eye fixation. This presaccadic attention shift is considered strong and compulsory, and relies on different neural computations and substrates than covert attention. Thus, we asked: Can presaccadic attention compensate for the ubiquitous performance asymmetries observed during eye fixation? Our data replicate polar performance asymmetries during fixation and document the same asymmetries during saccade preparation. Crucially, however, presaccadic attention enhanced contrast sensitivity at the horizontal and lower vertical meridian, but not at the upper vertical meridian. Thus, instead of attenuating performance asymmetries, presaccadic attention exacerbates them.

Pupil dynamics: A potential proxy of neural preparation for goal-directed eye movement.

The pupils reflexively constrict or dilate to regulate the influx of light on the retinae. Pupillary light reflex (PLR) is susceptible to many non-visual cognitive processes including covert orientation of attention and planning rapid saccadic eye movement. The frontal eye field (FEF) and superior colliculus (SC), which also send projections to the PLR pathway, are two important areas in primate's brain for planning saccade and orientation of attention. The saccadic reaction time (SRT) and the rate of increase in activity of movement neurons in these areas are inversely correlated. This study addressed how pupil dynamics, activity in the FEF and SC and SRT are related in a saccadic decision-making task. The rate of visually evoked pupil constriction was found inversely related to SRT. This was further verified by simulating a homeomorphic biomechanical model of pupillary muscle plants, wherein we projected signals similar to build-up activity in the FEF and SC to the parasympathetic (constriction) and sympathetic (dilation) division of the PLR pathway, respectively. A striking similarity between simulated and observed dynamics of pupil constriction suggests that PLR is a potential proxy of saccade planning by movement neurons in the FEF and SC. Indistinguishable pupil dynamics when planned saccades were elicited versus when they were cancelled eliminated the possibility that the obligatory pre-saccadic shift of attention alone influenced the rate of pupil constriction. Our study envisages a mechanism of how the oculomotor system influences the autonomic activity in an attempt to timely minimize saccadic visual transients by regulating the influx of light.

Impaired pre-saccadic shifts of attention in neglect patients

Every saccade is generally preceded by a mandatory shift of attention to the saccade endpoint, allowing us to process visual information more effectively. Whether this ‘pre-saccadic shift of attention’ is still intact in hemispatial neglect is unknown. Whereas neglect patients exhibit lateralized impairments of attention and often show impaired saccadic behaviour, it is not yet clear how the pre-saccadic shift of attention is affected during accurately executed eye movements. In this study, we used a gaze contingent visual discrimination task, in which neglect patients had to discriminate a probe presented before saccade onset. Results revealed an imbalance in discrimination performance between the two hemifields with poor performance to probes in the contralesional compared to the ipsilesional hemifield when accounting for saccadic impairments. These results suggest that attention and eye movements are both unique impairments of neglect patients. We hypothesize that the impaired pre-saccadic shift of attention could be one of the key problems of neglect and might underlie other spatial and non-spatial deficits often reported in neglect patients.

Understanding the collinear masking effect in visual search through eye tracking.

Recent research has reported that, while both orientation contrast and collinearity increase target salience in visual search, a combination of the two counterintuitively masks a local target. Through eye-tracking and eye-movement analysis with hidden Markov models (EMHMM), here we showed that this collinear masking effect was associated with reduced eye-fixation consistency (as measured in entropy) at the central fixation cross prior to the search display presentation. As a decreased precision of saccade landing position is shown to be related to attention shift away from the saccadic target, our result suggested that the collinear masking effect may be related to attention shift to a non-saccadic-goal location in expectation of the search display before saccading to the central fixation cross. This attention shift may consequently interfere with attention capture by the collinear distractor containing the target, resulting in the masking effect. In contrast, although older adults had longer response times, more dispersed eye-movement pattern, and lower eye-movement consistency than young adults during visual search, the two age groups did not differ in the masking effect, suggesting limited contribution from ageing-related cognitive decline. Thus, participants' pre-saccadic attention shift prior to search may be an important factor influencing their search behavior.

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.

Psychophysical dual-task setups do not measure pre-saccadic attention but saccade-related strengthening of sensory representations.

Visual attention and saccadic eye movements are linked in a tight, yet flexible fashion. In humans, this link is typically studied with dual‐task setups. Participants are instructed to execute a saccade to some target location, while a discrimination target is flashed on a screen before the saccade can be made. Participants are also instructed to report a specific feature of this discrimination target at the trial end. Discrimination performance is usually better if the discrimination target occurred at the same location as the saccade target compared to when it occurred at a different location, which is explained by the mandatory shift of attention to the saccade target location before saccade onset. This pre‐saccadic shift of attention presumably enhances the perception of the discrimination target if it occurred at the same, but not if it occurred at a different location. It is, however, known that a dual‐task setup can alter the primary process under investigation. Here, we directly compared pre‐saccadic attention in single‐task versus dual‐task setups using concurrent electroencephalography (EEG) and eye‐tracking. Our results corroborate the idea of a pre‐saccadic shift of attention. They, however, question that this shift leads to the same‐position discrimination advantage. The relation of saccade and discrimination target position affected the EEG signal only after saccade onset. Our results, thus, favor an alternative explanation based on the role of saccades for the consolidation of sensory and short‐term memory. We conclude that studies with dual‐task setups arrived at a valid conclusion despite not measuring exactly what they intended to measure.

Transsaccadic perception is affected by saccade landing point deviations after saccadic adaptation.

Whenever we move our eyes, some visual information obtained before a saccade is combined with the visual information obtained after a saccade. Interestingly, saccades rarely land exactly on the saccade target, which may pose a problem for transsaccadic perception as it could affect the quality of postsaccadic input. Recently, however, we showed that transsaccadic feature integration is actually unaffected by deviations of saccade landing points. Possibly, transsaccadic integration remains unaffected because the presaccadic shift of attention follows the intended saccade target and not the actual saccade landing point during regular saccades. Here, we investigated whether saccade landing point errors can in fact alter transsaccadic perception when the presaccadic shift of attention follows the saccade landing point deviation. Given that saccadic adaptation not only changes the saccade vector, but also the presaccadic shift of attention, we combined a feature report paradigm with saccadic adaptation. Observers reported the color of the saccade target, which occasionally changed slightly during a saccade to the target. This task was performed before and after saccadic adaptation. The results showed that, after adaptation, presaccadic color information became less precise and transsaccadic perception had a stronger reliance on the postsaccadic color estimate. Therefore, although previous studies have shown that transsaccadic perception is generally unaffected by saccade landing point deviations, our results reveal that this cannot be considered a general property of the visual system. When presaccadic shifts of attention follow altered saccade landing points, transsaccadic perception is affected, suggesting that transsaccadic feature perception might be dependent on visual spatial attention.

Placeholder objects shape spatial attention effects before eye movements.

In the time leading up to a saccade, the saccade target is perceptually enhanced compared to other objects in the visual field. This enhancement is attributed to a shift of spatial attention toward the target. We examined whether the presence of visual objects is critical for the perceptual enhancement at the saccade target to occur. We hypothesized that attention may need an object to focus on in order to be effective. We conducted four experiments using a dual-task design, where participants performed eye movements either to a location demarked by a placeholder or to an empty screen location where no object was displayed. At the same time, they discriminated a probe flashed at the location targeted by the eye movement or at one of two control locations. A strong perceptual advantage at the saccade target location was observed only when placeholders were displayed at the time of probe presentation. The complete absence of placeholders (Experiment 1), the presence of placeholders before but not during probe presentation (Experiment 3), and the presence of objects only around the saccade target (Experiments 3 and 4) led to a strong reduction in the saccade-target benefit. We conclude that placeholders may indeed be necessary to observe presaccadic enhancement at the saccade target. However, this is not because placeholders provide an object to focus attention on, but rather because they produce a masking (or crowding) effect. This detrimental effect is overcome by the presaccadic shift of attention, resulting in heightened perception only at the saccade target object.

Effects of central and peripheral cueing on perceptual and saccade performance

Previous research on the spatiotemporal dynamics of exogenous and endogenous attentional allocation during saccade preparation yielded conflicting results. We hypothesize that this can be explained by the cueing type used to orient attention in a perceptual task. We investigated the time-course of attentional allocation as a function of cueing type (central vs peripheral), spatial congruency of the cued perceptual and saccade task locations, and cue validity in a dual-task paradigm. Participants performed a visual discrimination task during saccade preparation. We found that central and peripheral cues differentially affected the time-course of attentional allocation depending on spatial congruency and cue validity. Peripheral cues quickly and transiently oriented attention to the cued location. In the congruent condition, attention was maintained by the pre-saccadic attention shift, but declined in the spatially incongruent condition. Central cues slowly oriented attention to the cued location. In the congruent condition, attention was boosted by the pre-saccadic attention shift compared to a slower increase in the spatially incongruent condition. The pre-saccadic attention shift – the automatic and obligatory shift of attention to the saccade target – observed in the invalid spatially incongruent condition was not differentially affected by the cueing type orienting attention away from it. Our results suggest that exogenous and endogenous attention is dynamically and flexibly allocated to cued locations during saccade preparation while pre-saccadic attentional resources are progressively shifted to the saccade target irrespective of the cueing type. We argue that attentional selection for perception represents a partially independent process in contrast to the pre-saccadic attention shift.

Selective enhancement of orientation tuning before saccades.

Saccadic eye movements cause a rapid sweep of the visual image across the retina and bring the saccade's target into high-acuity foveal vision. Even before saccade onset, visual processing is selectively prioritized at the saccade target. To determine how this presaccadic attention shift exerts its influence on visual selection, we compare the dynamics of perceptual tuning curves before movement onset at the saccade target and in the opposite hemifield. Participants monitored a 30-Hz sequence of randomly oriented gratings for a target orientation. Combining a reverse correlation technique previously used to study orientation tuning in neurons and general additive mixed modeling, we found that perceptual reports were tuned to the target orientation. The gain of orientation tuning increased markedly within the last 100 ms before saccade onset. In addition, we observed finer orientation tuning right before saccade onset. This increase in gain and tuning occurred at the saccade target location and was not observed at the incongruent location in the opposite hemifield. The present findings suggest, therefore, that presaccadic attention exerts its influence on vision in a spatially and feature-selective manner, enhancing performance and sharpening feature tuning at the future gaze location before the eyes start moving.

Investigating the parameters of transsaccadic memory: inhibition of return impedes information acquisition near a saccade target

ABSTRACTA limited amount of visual information is retained between saccades, which is subsequently stored into a memory system, such as transsaccadic memory. Since the capacity of transsaccadic memory is limited, selection of information is crucial. Selection of relevant information is modulated by attentional processes such as the presaccadic shift of attention. This involuntary shift of attention occurs prior to execution of the saccade and leads to information acquisition at an intended saccade target. The aim of the present study was to investigate the influence that another attentional effect, inhibition of return (IOR), has on the information that gets stored into transsaccadic memory. IOR is the phenomenon where participants are slower to respond to a cue at a previously attended location. To this end, we used a transsaccadic memory paradigm in which stimuli, oriented on a horizontal axis relative to saccade direction, are only visible to the participant before executing a saccade. Previous research showed that items in close proximity to a saccade target are likely to be reported more accurately. In our current study, participants were cued to fixate one of the stimulus locations and subsequently refixated the centre fixation point before executing the transsaccadic memory task. Results indicate that information at a location near a saccade landing point is less likely to be acquired into transsaccadic memory when this location was previously associated with IOR. Furthermore, we found evidence which implicates a reduction of the overall amount of elements retained in transsaccadic memory when a location near a saccade target is associated with IOR. These results suggest that the presaccadic shift of attention may be modulated by IOR and thereby reduces information acquisition by transsaccadic memory.

There is no attentional global effect: Attentional shifts are independent of the saccade endpoint.

Many studies have found a strong coupling between selective attention and eye movements. The premotor theory of attention suggests that saccade preparation is directly responsible for such attentional shifts. While it has already been shown that the attentional shift is not directly coupled to the final stages of motor execution, it is currently unknown to what aspect of the earlier stages of saccade preparation the attentional shift is coupled. An important step in this preparation process is resolving the landing point when multiple elements compete for the saccade. Here we ask how such a competition influences the presaccadic attentional locus and whether the presaccadic shift of attention is coupled to the saccade landing position or the possible saccade goals. To this end, we adopt a global effect paradigm where a target is accompanied by a salient distractor resulting in the majority of eye movements landing in between target and distractor. To determine the allocation of attention, participants are presented with a discrimination task shortly before the execution of the saccade. Despite a strong global effect obtained for saccade endpoints, we find little evidence for attentional facilitation at the location between target and distractor, but strong attentional facilitation at the location of the target and distractor. We argue that attention is coupled to active oculomotor programs, but not part of the resolution of these programs towards the execution of the saccade.

The pupillary light response reflects eye-movement preparation.

When the eyes are exposed to an increased influx of light, the pupils constrict. The pupillary light response (PLR) is traditionally believed to be purely reflexive and not susceptible to cognitive influences. In contrast to this traditional view, we report that preparation of a PLR occurs in parallel with preparation of a saccadic eye movement toward a bright (or dark) stimulus, even before the eyes set in motion. Participants fixated a central gray area and made a saccade toward a peripheral target. Using gaze-contingent display changes, we manipulated whether or not the brightness of the target background was the same during and after saccade preparation. More specifically, on some trials we changed the brightness of the target background during the saccade, thus dissociating the preparatory PLR (i.e., to the brightness of the target background before the saccade) from the regular PLR (i.e., to the brightness after the saccade). We show that preparation triggers a pupillary response to the brightness of a to-be-fixated target background already before the eyes have landed on it. We link our findings to the presaccadic shift of attention: The pupil prepares to adjust its size to the brightness of a to-be-fixated stimulus as soon as attention covertly shifts toward that stimulus. Our findings illustrate that the PLR is a dynamic movement that is tightly linked to visual attention and eye-movement preparation.

Predictability of spatial and non-spatial target properties improves perception in the pre-saccadic interval

In a dual-task paradigm with a perceptual discrimination task and a concurrent saccade task, we examined participants' ability to make use of prior knowledge of a critical property of the perceptual target to improve discrimination. Previous research suggests that during a short time window before a saccade, covert attention is imperatively directed towards the saccade target location. Consequently, discrimination of perceptual targets at the saccade target location is better than at other locations. We asked whether the obligatory pre-saccadic attention shift prevents perceptual benefits arising for perceptual target stimuli with predictable as opposed to non-predictable properties. We compared conditions in which the color or location of the perceptual target was constant to conditions in which those properties varied randomly across trials. In addition to the expected improvements of perception at the saccade target location, we found perception to be better with constant than with random properties of the perceptual target. Thus, color or location information about an upcoming perceptual target facilitates perception even while spatial attention is shifted to the saccade target. The improvement occurred irrespective of the saccade target location, which suggests that the underlying mechanism is independent of the pre-saccadic attention shift, but alternative interpretations are discussed as well.

Adaptive deployment of spatial and feature-based attention before saccades.

What you see depends not only on where you are looking but also on where you will look next. The pre-saccadic attention shift is an automatic enhancement of visual sensitivity at the target of the next saccade. We investigated whether and how perceptual factors independent of the oculomotor plan modulate pre-saccadic attention within and across trials. Observers made saccades to one (the target) of six patches of moving dots and discriminated a brief luminance pulse (the probe) that appeared at an unpredictable location. Sensitivity to the probe was always higher at the target's location (spatial attention), and this attention effect was stronger if the previous probe appeared at the previous target's location. Furthermore, sensitivity was higher for probes moving in directions similar to the target's direction (feature-based attention), but only when the previous probe moved in the same direction as the previous target. Therefore, implicit cognitive processes permeate pre-saccadic attention, so that-contingent on recent experience-it flexibly distributes resources to potentially relevant locations and features.

Crowding is immune to the pre-saccadic shift of attention

Crowding is immune to the pre-saccadic shift of attention

Visual attention and stability.

In the present review, we address the relationship between attention and visual stability. Even though with each eye, head and body movement the retinal image changes dramatically, we perceive the world as stable and are able to perform visually guided actions. However, visual stability is not as complete as introspection would lead us to believe. We attend to only a few items at a time and stability is maintained only for those items. There appear to be two distinct mechanisms underlying visual stability. The first is a passive mechanism: the visual system assumes the world to be stable, unless there is a clear discrepancy between the pre- and post-saccadic image of the region surrounding the saccade target. This is related to the pre-saccadic shift of attention, which allows for an accurate preview of the saccade target. The second is an active mechanism: information about attended objects is remapped within retinotopic maps to compensate for eye movements. The locus of attention itself, which is also characterized by localized retinotopic activity, is remapped as well. We conclude that visual attention is crucial in our perception of a stable world.

Eye movement signals influence perception: Evidence from the adaptation of reactive and volitional saccades

Information about upcoming saccadic eye movements is used to orient visuo-spatial attention across the visual field. Different eye movement signals (intended or actual) could be used according to the intentionality of the saccade in preparation (Reactive or Volitional), and can be dissociated by saccadic adaptation. Gap 0 and overlap paradigms were contrasted to elicit the two saccade populations with different latencies and an asymmetric transfer of saccadic adaptation. Preparation of both saccade types caused a concomitant shift in the attentional focus (indexed by relative perceptual performance) to the actual, not intended, eye position. The attentional shift emerged progressively, earlier for V-saccades but reaching a maximal level around saccade onset for both saccade types. These results suggest that information about actual eye movements mediates the pre-saccadic shift of attention.