Saccade Target Location Research Articles

Presaccadic attention does not facilitate the detection of changes in the visual field.

Planning a rapid eye movement (saccade) changes how we perceive our visual world. Even before we move the eyes visual discrimination sensitivity improves at the impending target of eye movements, a phenomenon termed "presaccadic attention." Yet, it is unknown if such presaccadic selection merely affects perceptual sensitivity, or also affects downstream decisional processes, such as choice bias. We report a surprising lack of presaccadic perceptual benefits in a common, everyday setting-detection of changes in the visual field. Despite the lack of sensitivity benefits, choice bias for reporting changes increased reliably for the saccade target. With independent follow-up experiments, we show that presaccadic change detection is rendered more challenging because percepts at the saccade target location are biased toward, and more precise for, only the most recent of two successive stimuli. With a Bayesian model, we show how such perceptual and choice biases are crucial to explain the effects of saccade plans on change detection performance. In sum, visual change detection sensitivity does not improve presaccadically, a result that is readily explained by teasing apart distinct components of presaccadic selection. The findings may have critical implications for real-world scenarios, like driving, that require rapid gaze shifts in dynamically changing environments.

Sound reduces saccadic chronostasis illusion

The saccadic chronostasis illusion refers to the duration overestimation of the first visual stimulation after saccadic eye movement, which is also known as “stopped clock illusion.” The present study investigated whether saccadic chronostasis would be observed in the auditory modality and whether the saccade-induced time dilation in the visual modality would be reduced by a synchronously presented sound. In each trial, a unisensory visual stimulus, unisensory sound, or bimodal audio-visual stimulus with a duration of 200–800 ms (probe stimulus) was presented at the saccade target location and temporally around the offset of the saccade, followed by a unisensory visual or auditory standard stimulus for a fixed 500 ms. Participants were required to identify which of the two stimuli (probe or standard) presented in the target modality (visual or auditory) was perceived as longer. The results showed that no saccadic chronostasis was observed in the auditory modality, regardless of whether the sound was presented alone or synchronously accompanied by a visual stimulus. Interestingly, the magnitude of the saccadic chronostasis illusion was reduced by the synchronously presented sound. Moreover, the combined effect of the saccade and sound on visual time perception fits well with the standard scalar model, and the weight of the cross-modal effect was higher than that of saccadic visual time dilation. These results suggest that sound dominates vision in time processing during saccades and linearly modulates saccadic chronostasis, which follows the Scalar Expectancy Theory.

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.

Decoding Saccade Intention From Primate Prefrontal Cortical Local Field Potentials Using Spectral, Spatial, and Temporal Dimensionality Reduction.

Most invasive Brain Computer Interfaces (iBCIs) use spike and Local Field Potentials (LFPs) from the motor or parietal cortices to decode movement intentions. It has been debated whether harvesting signals from other brain areas that encode global cognitive variables, such as the allocation of attention and eye movement goals in a variety of spatial reference frames, may improve the outcome of iBCIs. Here, we explore the ability of LFP signals, sampled from the lateral prefrontal cortex (LPFC) of macaque monkeys, to encode eye-movement intention during the pre-movement fixation period of a delayed saccade task. We use spectral dimensionality reduction to examine the spatiotemporal properties of the extracted non-rhythmic broadband activity and explore its usefulness in decoding saccade goals. The dynamics of the broadband signal in low spatial dimensions across the pre-movement fixation period uncovered saccade target separation; its discriminative potential was confirmed using support vector machine classifications. These findings reveal that broadband LFP from the LPFC can be used to decode intended saccade target location during pre-movement periods. We further provide a general workflow that can be implemented in iBCIs and it is relatively robust to the loss of spikes in individual electrodes.

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.

Preparation of saccade sequences and eye programming affect endogenous covert attention.

Endogenous attention can be allocated in parallel to at least two saccade target locations of a planned sequence, but attentional resources are larger in the location of the first than the second saccade. The meridian effect that is observed in endogenous attention can be explained by eye programming, but it is not known how eye-movement preparation and eye programming can together affect endogenous attention during sequential saccades. We used a double-task paradigm to investigate this issue. In two experiments, we confirmed the relation between the preparation of sequential saccades and attentional selection and also showed that eye programming could eliminate deterioration of attentional resources in the second saccade location. The finding of the meridian effect in both the saccadic task and the target discrimination task additionally indicates the important role of eye programming in endogenous attention. The results were discussed in terms of the Premotor Theory of Attention.

Feature prediction across eye movements is location specific and based on retinotopic coordinates.

With each saccadic eye movement, internal object representations change their retinal position and spatial resolution. Recently, we suggested that the visual system deals with these saccade-induced changes by predicting visual features across saccades based on transsaccadic associations of peripheral and foveal input (Herwig & Schneider, 2014). Here we tested the specificity of feature prediction by asking (a) whether it is spatially restricted to the previous learning location or the saccade target location, and (b) whether it is based on retinotopic (eye-centered) or spatiotopic (world-centered) coordinates. In a preceding acquisition phase, objects systematically changed their spatial frequency during saccades. In the following test phases of two experiments, participants had to judge the frequency of briefly presented peripheral objects. These objects were presented either at the previous learning location or at new locations and were either the target of a saccadic eye movement or not (Experiment 1). Moreover, objects were presented either in the same or different retinotopic and spatiotopic coordinates (Experiment 2). Spatial frequency perception was biased toward previously associated foveal input indicating transsaccadic learning and feature prediction. Importantly, while this pattern was not bound to the saccade target location, it was seen only at the previous learning location in retinotopic coordinates, suggesting that feature prediction probably affects low- or mid-level perception.

How visual spatial attention alters perception.

Visual attention is essential for visual perception. Spatial attention allows us to grant priority in processing and selectively process information at a given location. In this paper, I explain how two kinds of spatial attention: covert (allocated to the target location, without accompanying eye movements) and presaccadic (allocated to the location of the upcoming saccade's target) affect performance and alter appearance.First, I highlight some behavioral and neuroimaging research on covert attention, which alters performance and appearance in many basic visual tasks. Second, I review studies showing that presaccadic attention improves performance and alters appearance at the saccade target location. Further, these modulations change the processing of feature information automatically, even when it is detrimental to the task at hand. We propose that saccade preparation may support transsaccadic integration. Systematically investigating the common and differential characteristics of covert attention and presaccadic attention will continue to further our understanding of the pervasive selective processing of information, which enables us to make sense of our complex visual world.

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.

How post-saccadic target blanking affects the detection of stimulus displacements across saccades

When a visual stimulus is displaced during a saccade the displacement is often not noticed unless it is large compared to the amplitude of the eye movement. Displacement detection is improved, however, if a blank intervenes between saccade target offset and the presentation of the displaced post-saccadic stimulus. This has been interpreted as evidence that precise information about eye position and accurate memory for the position of the pre-saccadic target are available immediately after saccade offset, but are overridden by the presence of the post-saccadic stimulus if it is present when the eyes land. In the current set of experiments we examined in more detail how blanking contributes to the increase in displacement sensitivity. In two experiments we showed that the presentation of a blank interval between saccade offset and the presentation of the displaced stimulus improved people’s ability to detect that the stimulus had been displaced and also their ability to judge the direction that it had been displaced, but only for displacements opposite to the direction of the saccade (backward displacements). A third experiment suggested that this improvement in the detection of backward displacements was due in part to subjects misremembering the saccade target location as being closer to the initial fixation point than it actually was immediately after the saccade but remembering its location more veridically 50 ms later. This has the effect of improving the detection of displacements as well as their direction of displacement, but preferentially for backwards vs. forward displacements.

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.

Spatiotopic updating of visual feature information.

Saccades shift the retina with high-speed motion. In order to compensate for the sudden displacement, the visuomotor system needs to combine saccade-related information and visual metrics. Many neurons in oculomotor but also in visual areas shift their receptive field shortly before the execution of a saccade (Duhamel, Colby, & Goldberg, 1992; Nakamura & Colby, 2002). These shifts supposedly enable the binding of information from before and after the saccade. It is a matter of current debate whether these shifts are merely location based (i.e., involve remapping of abstract spatial coordinates) or also comprise information about visual features. We have recently presented fMRI evidence for a feature-based remapping mechanism in visual areas V3, V4, and VO (Zimmermann, Weidner, Abdollahi, & Fink, 2016). In particular, we found fMRI adaptation in cortical regions representing a stimulus' retinotopic as well as its spatiotopic position. Here, we asked whether spatiotopic adaptation exists independently from retinotopic adaptation and which type of information is behaviorally more relevant after saccade execution. We first adapted at the saccade target location only and found a spatiotopic tilt aftereffect. Then, we simultaneously adapted both the fixation and the saccade target location but with opposite tilt orientations. As a result, adaptation from the fixation location was carried retinotopically to the saccade target position. The opposite tilt orientation at the retinotopic location altered the effects induced by spatiotopic adaptation. More precisely, it cancelled out spatiotopic adaptation at the saccade target location. We conclude that retinotopic and spatiotopic visual adaptation are independent effects.

Spatial attention during saccade decisions.

Behavioral measures of decision making are usually limited to observations of decision outcomes. In the present study, we made use of the fact that oculomotor and sensory selection are closely linked to track oculomotor decision making before oculomotor responses are made. We asked participants to make a saccadic eye movement to one of two memorized target locations and observed that visual sensitivity increased at both the chosen and the nonchosen saccade target locations, with a clear bias toward the chosen target. The time course of changes in visual sensitivity was related to saccadic latency, with the competition between the chosen and nonchosen targets resolved faster before short-latency saccades. On error trials, we observed an increased competition between the chosen and nonchosen targets. Moreover, oculomotor selection and visual sensitivity were influenced by top-down and bottom-up factors as well as by selection history and predicted the direction of saccades. Our findings demonstrate that saccade decisions have direct visual consequences and show that decision making can be traced in the human oculomotor system well before choices are made. Our results also indicate a strong association between decision making, saccade target selection, and visual sensitivity.NEW & NOTEWORTHY We show that saccadic decisions can be tracked by measuring spatial attention. Spatial attention is allocated in parallel to the two competing saccade targets, and the time course of spatial attention differs for fast-slow and for correct-erroneous decisions. Saccade decisions take the form of a competition between potential saccade goals, which is associated with spatial attention allocation to those locations.

The Concurrent Programming of Saccades.

Sequences of saccades have been shown to be prepared concurrently however it remains unclear exactly what aspects of those saccades are programmed in parallel. To examine this participants were asked to make one or two target-driven saccades: a reflexive saccade; a voluntary saccade; a reflexive then a voluntary saccade; or vice versa. During the first response the position of a second target was manipulated. The new location of the second saccade target was found to impact on second saccade latencies and second saccade accuracy showing that some aspects of the second saccade program are prepared in parallel with the first. However, differences were found in the specific pattern of effects for each sequence type. These differences fit well within a general framework for saccade control in which a common priority map for saccade control is computed and the influence of saccade programs on one another depends not so much on the types of saccade being produced but rather on the rate at which their programs develop.

Using temporally aligned event-related potentials for the investigation of attention shifts prior to and during saccades

According to the pre-motor theory of attention, attention is shifted to a saccade's landing position before the saccade is executed. Such pre-saccadic attention shifts are usually studied in psychophysical dual-task conditions, with a target-discrimination task before saccade onset. Here, we present a novel approach to investigate pre-saccadic attention shifts with the help of event-related potentials (ERPs). Participants executed one or two saccades to color-defined targets while ERPs and eye-movements were recorded. In single-target blocks participants executed a single saccade. In two-targets blocks participants made either a single saccade to one of the targets, or two successive saccades to both targets. Importantly, in two-targets blocks, targets could appear on the same or on opposite sides of the vertical midline. This allowed us to study contra-to-ipsilateral ERP differences (such as the N2pc or PCN) that reflect attention shifts to the targets, prior to saccade onset and during saccades. If pre-saccadic attention shifts to saccade target locations are necessary for saccade execution and if searched-for saccade targets capture attention, there should be enhanced attentional competition (1) between two targets compared to single targets; (2) between two opposite-sides targets compared to two same-side targets; and (3) in two saccades rather than one saccade conditions: More attentional competition was expected to delay saccade latency and to weaken pre-saccadic laterality effects in ERPs. Hypotheses were tested by means of temporally aligned ERPs that were simultaneously time-locked to stimulus onsets, saccade onsets, and saccade offsets. Predictions (1) and (2) were partly and fully confirmed, respectively, but no evidence was found for (3). We explain the implications of our results for the role of attention during saccade preparation, and we point out how temporally aligned ERPs compare to ICA-based electroencephalogram (EEG) artifact correction procedures and to psychophysical dual-task approaches.

Single-trial decoding of intended eye movement goals from lateral prefrontal cortex neural ensembles.

Neurons in the lateral prefrontal cortex (LPFC) encode sensory and cognitive signals, as well as commands for goal-directed actions. Therefore, the LPFC might be a good signal source for a goal-selection brain-computer interface (BCI) that decodes the intended goal of a motor action previous to its execution. As a first step in the development of a goal-selection BCI, we set out to determine if we could decode simple behavioral intentions to direct gaze to eight different locations in space from single-trial LPFC neural activity. We recorded neuronal spiking activity from microelectrode arrays implanted in area 8A of the LPFC of two adult macaques while they made visually guided saccades to one of eight targets in a center-out task. Neuronal activity encoded target location immediately after target presentation, during a delay epoch, during the execution of the saccade, and every combination thereof. Many (40%) of the neurons that encoded target location during multiple epochs preferred different locations during different epochs. Despite heterogeneous and dynamic responses, the neuronal feature set that best predicted target location was the averaged firing rates from the entire trial and it was best classified using linear discriminant analysis (63.6-96.9% in 12 sessions, mean 80.3%; information transfer rate: 21-59, mean 32.8 bits/min). Our results demonstrate that it is possible to decode intended saccade target location from single-trial LPFC activity and suggest that the LPFC is a suitable signal source for a goal-selection cognitive BCI.

Effect of saccade automaticity on perisaccadic space compression.

Briefly presented stimuli occurring just before or during a saccadic eye movement are mislocalized, leading to a compression of visual space toward the target of the saccade. In most cases this has been measured in subjects over-trained to perform a stereotyped and unnatural task where saccades are repeatedly driven to the same location, marked by a highly salient abrupt onset. Here, we asked to what extent the pattern of perisaccadic mislocalization depends on this specific context. We addressed this question by studying perisaccadic localization in a set of participants with no prior experience in eye-movement research, measuring localization performance as they practiced the saccade task. Localization was marginally affected by practice over the course of the experiment and it was indistinguishable from the performance of expert observers. The mislocalization also remained similar when the expert observers were tested in a condition leading to less stereotypical saccadic behavior—with no abrupt onset marking the saccade target location. These results indicate that perisaccadic compression is a robust behavior, insensitive to the specific paradigm used to drive saccades and to the level of practice with the saccade task.

Continuous Updating of Visuospatial Memory in Superior Colliculus during Slow Eye Movements

Primates can remember and spatially update the visual direction of previously viewed objects during various types of self-motion. It is known that the brain "remaps" visual memory traces relative to gaze just before and after, but not during, discrete gaze shifts called saccades. However, it is not known how visual memory is updated during slow, continuous motion of the eyes. Here, we recorded the midbrain superior colliculus (SC) of two rhesus monkeys that were trained to spatially update the location of a saccade target across an intervening smooth pursuit (SP) eye movement. Saccade target location was varied across trials so that it passed through the neuron's receptive field at different points of the SP trajectory. Nearly all (99% of) visual responsive neurons, but no motor neurons, showed a transient memory response that continuously updated the saccade goal during SP. These responses were gaze centered (i.e., shifting across the SC's retinotopic map in opposition to gaze). Furthermore, this response was strongly enhanced by attention and/or saccade target selection. This is the first demonstration of continuous updating of visual memory responses during eye motion. We expect that this would generalize to other visuomotor structures when gaze shifts in a continuous, unpredictable fashion.

Effects of spatial congruency on saccade and visual discrimination performance in a dual-task paradigm.

The present study investigated the coupling of selection-for-perception and selection-for-action during saccadic eye movement planning in three dual-task experiments. We focused on the effects of spatial congruency of saccade target (ST) location and discrimination target (DT) location and the time between ST-cue and Go-signal (SOA) on saccadic eye movement performance. In two experiments, participants performed a visual discrimination task at a cued location while programming a saccadic eye movement to a cued location. In the third experiment, the discrimination task was not cued and appeared at a random location. Spatial congruency of ST-location and DT-location resulted in enhanced perceptual performance irrespective of SOA. Perceptual performance in spatially incongruent trials was above chance, but only when the DT-location was cued. Saccade accuracy and precision were also affected by spatial congruency showing superior performance when the ST- and DT-location coincided. Saccade latency was only affected by spatial congruency when the DT-cue was predictive of the ST-location. Moreover, saccades consistently curved away from the incongruent DT-locations. Importantly, the effects of spatial congruency on saccade parameters only occurred when the DT-location was cued; therefore, results from experiments 1 and 2 are due to the endogenous allocation of attention to the DT-location and not caused by the salience of the probe. The SOA affected saccade latency showing decreasing latencies with increasing SOA. In conclusion, our results demonstrate that visuospatial attention can be voluntarily distributed upon spatially distinct perceptual and motor goals in dual-task situations, resulting in a decline of visual discrimination and saccade performance.