Saccade Trials Research Articles

Decoding Remapped Spatial Information in the Peri-Saccadic Period.

It has been suggested that, prior to a saccade, visual neurons predictively respond to stimuli that will fall in their receptive fields after completion of the saccade. This saccadic remapping process is thought to compensate for the shift of the visual world across the retina caused by eye movements. To map the timing of this predictive process in the brain, we recorded neural activity using electroencephalography during a saccade task. Human participants (male and female) made saccades between two fixation points while covertly attending to oriented gratings briefly presented at various locations on the screen. Data recorded during trials in which participants maintained fixation were used to train classifiers on stimuli in different positions. Subsequently, data collected during saccade trials were used to test for the presence of remapped stimulus information at the post-saccadic retinotopic location in the peri-saccadic period, providing unique insight into when remapped information becomes available. We found that the stimulus could be decoded at the remapped location ∼180 ms post-stimulus onset, but only when the stimulus was presented 100-200 ms before saccade onset. Within this range, we found that the timing of remapping was dictated by stimulus onset rather than saccade onset. We conclude that presenting the stimulus immediately before the saccade allows for optimal integration of the corollary discharge signal with the incoming peripheral visual information, resulting in a remapping of activation to the relevant post-saccadic retinotopic neurons.

Saccadic latency differences in preclinical Alzheimer’s disease

AbstractBackgroundPrevious studies indicate that individuals with mild cognitive impairment (MCI) or Alzheimer’s disease (AD) have higher latencies on anti‐saccade tasks than healthy controls. We investigated whether this difference in latency appears even earlier, in cognitively healthy (CH) individuals at high risk of cognitive decline to MCI or AD and whether subliminal priming or task switching further impacted this latency difference.MethodWe studied CH participants whose cerebrospinal fluid (CSF) amyloid / tau ratio was normal (≥2.7132, low risk) or pathological (<2.7132, high risk) (PMID: 24260210). The testing paradigm included three blocks: (1) all saccades, (2) all anti‐saccades, and (3) patterned task switching with two saccades followed by two anti‐saccades. Trials began with a green (saccade) or red (anti‐saccade) cue appearing at a central fixation point. Then, a masked subliminal cue appeared on the right or left, followed by a target congruent or incongruent with the subliminal prime location. Trials ended 1000 ms after the participant first looked directly at the target for saccade trials or away from the target for anti‐saccade trials.ResultPreliminary results (n = 19, 3 high risk) using a 3‐way mixed ANOVA (d.f. = 3484) indicate that high risk participants perform slower across all conditions (F = 26.36, p <<< 0.001). This effect is especially pronounced when task switching (F = 3.41, p < 0.05), with high risk participants performing 70.9 ms slower in the task switching block (Bonferroni‐corrected p = 6.62×10−6, 95% CI = [29.8, 112]). During the block with all anti‐saccades, however, the difference in performance is not significant (Bonferroni‐corrected p = 0.78), unlike the effects previously observed in individuals with MCI or AD. Additionally, subliminal cues do not show a significant overall effect on behavioral data (F = 2.32, p = 0.13).ConclusionPilot results indicate that latency differences when task switching between saccade and anti‐saccade tasks exist in CH people at high risk of cognitive decline. Because eye tracking tasks are much less invasive and expensive than spinal taps, they could provide a potential screening tool for those at risk of cognitive decline.

Reduced task-evoked pupillary response in preparation for an executive cognitive control response among individuals across the psychosis spectrum

Task-evoked pupillary response (TEPR) is a measure of physiological arousal modulated by cognitive demand. Healthy individuals demonstrate greater TEPR prior to correct versus error antisaccade trials and correct antisaccade versus visually guided saccade (VGS) trials. The relationship between TEPR and antisaccade performance in individuals with psychotic disorders and their relatives has not been investigated.Probands with schizophrenia, schizoaffective disorder, psychotic bipolar disorder, their first-degree relatives, and controls from the B-SNIP study completed antisaccade and VGS tasks. TEPR prior to execution of responses on these tasks was evaluated among controls compared to probands and relatives according to diagnostic groups and neurobiologically defined subgroups (biotypes).Controls demonstrated greater TEPR on antisaccade correct versus error versus VGS trials. TEPR was not differentiated between antisaccade correct versus error trials in bipolar or schizophrenia probands, though was greater on antisaccade compared to prosaccade trials. There was no modulation of TEPR in schizoaffective probands. Relatives of schizophrenia and schizoaffective probands and those with elevated psychosis spectrum traits failed to demonstrate differential TEPR on antisaccade correct versus error trials. No proband or relative biotypes demonstrated differential TEPR on antisaccade correct versus error trials, and only proband biotype 3 and relative biotypes 3 and 2 demonstrated greater TEPR on antisaccade versus VGS trials.Our findings suggest that aberrant modulation of preparatory activity prior to saccade execution contributes to impaired executive cognitive control across the psychosis spectrum, including nonpsychotic relatives with elevated clinical risk. Reduced pupillary modulation under cognitive challenge may thus be a biomarker for the psychosis phenotype.

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

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

Low-Level Visual Information is Maintained Across Saccades by a 'Soft Hand-Off' between Visual Processing Areas

Subjective visual experience of a rich, detailed visual scene seems continuous despite us making several saccadic eye movements every second which radically change retinal input. Here, we investigated the time course of low-level visual information processing in the brain by decoding spatial frequency of an attended, stationary stimulus that changed from one visual hemifield to another due to a horizontal saccadic eye movement. Magneto-encephalography (MEG) was recorded while human participants made a large horizontal saccade and monitored the orientation of a grating stimulus, making spatial frequency task-irrelevant. Separate trials, in which participants maintained fixation, were used to train a classifier that was tested during saccade trials. Decoding performance showed that information about spatial frequency was present in the original retinotopic areas before, during and up to around 200 ms after the saccade. Post-saccadic information rapidly ramped up within a few tens of milliseconds, allowing for rapid decoding from the new retinotopic areas. There was an overlap of over 100 ms during which decoding was significant from both pre- and post-saccadic processing areas. These results suggest that the apparent richness of perception across saccades may be supported by the continuous availability of the low-level spatial frequency information that supports gist, object and ensemble perception, with a “soft hand-off” of this information during the initial visual processing sweep of the new fixation. Such a mechanism does not require remapping of low-level visual information before the saccade.

Target localization after saccades and at fixation: Nontargets both facilitate and bias responses

ABSTRACTThe image on our retina changes every time we make an eye movement. To maintain visual stability after saccades, specifically to locate visual targets, we may use nontarget objects as “landmarks”. In the current study, we compared how the presence of nontargets affects target localization after saccades and during sustained fixation. Participants fixated a target object, which either maintained its location on the screen (sustained-fixation trials), or displaced to trigger a saccade (saccade trials). After the target disappeared, participants reported the most recent target location with a mouse click. We found that the presence of nontargets decreased response error magnitude and variability. However, this nontarget facilitation effect was not larger for saccade trials than sustained-fixation trials, indicating that nontarget facilitation might be a general effect for target localization, rather than of particular importance to post-saccadic stability. Additionally, participants’ responses were biased towards the nontarget locations, particularly when the nontarget-target relationships were preserved in relative coordinates across the saccade. This nontarget bias interacted with biases from other spatial references, e.g., eye movement paths, possibly in a way that emphasized non-redundant information. In summary, the presence of nontargets is one of several sources of reference that combine to influence (both facilitate and bias) target localization.

Pre-saccadic perception: Separate time courses for enhancement and spatial pooling at the saccade target.

We interact with complex scenes using eye movements to select targets of interest. Studies have shown that the future target of a saccadic eye movement is processed differently by the visual system. A number of effects have been reported, including a benefit for perceptual performance at the target (“enhancement”), reduced influences of backward masking (“un-masking”), reduced crowding (“un-crowding”) and spatial compression towards the saccade target. We investigated the time course of these effects by measuring orientation discrimination for targets that were spatially crowded or temporally masked. In four experiments, we varied the target-flanker distance, the presence of forward/backward masks, the orientation of the flankers and whether participants made a saccade. Masking and randomizing flanker orientation reduced performance in both fixation and saccade trials. We found a small improvement in performance on saccade trials, compared to fixation trials, with a time course that was consistent with a general enhancement at the saccade target. In addition, a decrement in performance (reporting the average flanker orientation, rather than the target) was found in the time bins nearest saccade onset when random oriented flankers were used, consistent with spatial pooling around the saccade target. We did not find strong evidence for un-crowding. Overall, our pattern of results was consistent with both an early, general enhancement at the saccade target and a later, peri-saccadic compression/pooling towards the saccade target.

Interaction between stimulus contrast and pre-saccadic crowding.

Objects that are briefly flashed around the time of saccades are mislocalized. Previously, robust interactions between saccadic perceptual distortions and stimulus contrast have been reported. It is also known that crowding depends on the contrast of the target and flankers. Here, we investigated how stimulus contrast and crowding interact with pre-saccadic perception. We asked observers to report the orientation of a tilted Gabor presented in the periphery, with or without four flanking vertically oriented Gabors. Observers performed the task either following a saccade or while maintaining fixation. Contrasts of the target and flankers were independently set to either high or low, with equal probability. In both the fixation and saccade conditions, the flanked conditions resulted in worse discrimination performance—the crowding effect. In the unflanked saccade trials, performance significantly decreased with target-to-saccade onset for low-contrast targets but not for high-contrast targets. In the presence of flankers, impending saccades reduced performance only for low-contrast, but not for high-contrast flankers. Interestingly, average performance in the fixation and saccade conditions was mostly similar in all contrast conditions. Moreover, the magnitude of crowding was influenced by saccades only when the target had high contrast and the flankers had low contrasts. Overall, our results are consistent with modulation of perisaccadic spatial localization by contrast and saccadic suppression, but at odds with a recent report of pre-saccadic release of crowding.

Commentary: Attentional tradeoffs maintain the tracking of moving objects across saccades.

Commentary: Attentional tradeoffs maintain the tracking of moving objects across saccades.

Interference during eye movement preparation shifts the timing of perisaccadic compression.

Our perception of the surrounding environment remains stable despite the fact that we frequently change the retinal position of input by rapid gaze shifts (saccades). There is a long-standing debate whether visual stability depends on an active mechanism using an efference copy of the impending saccadic motor command. Behavioral studies showing changes in perception around the time of saccades are consistent with a predictive mechanism, but previous studies of perceptual effects in humans confounded saccade programming with the resulting physical eye movement. In three experiments, we used a saccadic inhibition (SI) paradigm to delay saccadic onset while participants were performing a perisaccadic localization task. As expected, the perceived position of the probe stimulus was systematically biased (compressed) toward the saccadic goal, already during the presaccadic interval. In the SI condition, the localization error was shifted in time, in line with it following saccade intention rather than execution. The pattern was not the consequence of the probe being captured by the timing of the flashed distractor, but depended instead on the delay in saccadic onset time caused by SI. Importantly, the same configurations of perceptual probes presented with a flashed backward mask when participants maintained fixation did not lead to similar localization errors as saccade trials. This pattern of results is consistent with an active, sensorimotor explanation for perisaccadic mislocalization and, more generally, theories emphasizing the role of motor prediction in visual stability.

Visual Crowding at a Distance during Predictive Remapping

When we move our eyes, images of objects are displaced on the retina, yet the visual world appears stable. Oculomotor activity just prior to an eye movement contributes to perceptual stability by providing information about the predicted location of a relevant object on the retina following a saccade. It remains unclear, however, whether an object's features are represented at the remapped location. Here, we exploited the phenomenon of visual crowding to show that presaccadic remapping preserves the elementary features of objects at their predicted postsaccadic locations. Observers executed an eye movement and identified a letter probe flashed just before the saccade. Flanking stimuli were flashed around the location that would be occupied by the probe immediately following the saccade. Despite being positioned in the opposite visual field to the probe, these flankers disrupted observers' ability to identify the probe. Crucially, this "remapped crowding" interference was stronger when the flankers were visually similar to the probe than when the flanker and probe stimuli were distinct. Our findings suggest that visual processing at remapped locations is featurally dependent, providing a mechanism for achieving perceptual continuity of objects across saccades.

Retrospective and prospective information coding by different neurons in the prefrontal cortex

Neurons in the lateral prefrontal cortex show sustained activity during the maintenance of visual memory. Previous studies have also indicated that prefrontal neurons show predictive activity in anticipation of upcoming visual stimuli. Because these retrospective and prospective coding of visual stimuli have been examined in separate experiments, how these processes interact in individual neurons remains unknown. To examine this, we recorded from single prefrontal neurons while monkeys performed two behavioural tasks. In one task, the animals passively viewed a moving object during fixation, whereas in the other, they remembered the location of a briefly presented visual cue for subsequent saccades. We found that many neurons were reactive and responded only after the visual stimulus appeared in their receptive field, while some neurons were predictive and increased their activity even before the moving stimulus entered the receptive field. In the memory-guided saccade trials, the reactive neurons exhibited sustained activity during the delay period, whereas the predictive neurons did not. Delays of visual response to a moving stimulus did not correlate with visual latency for a stationary stimulus. Instead, it correlated with the magnitude of sustained activity during the delay period in the memory-guided saccade task. Our data show that retrospective and prospective coding of visual information are represented by distinct neuronal populations, and that their temporal preferences are stable across different task conditions. Reactive signals may reflect the amount of temporal integration in short-term memory, whereas predictive signals may solely represent future events in isolation from the maintenance of past information.

The Fixation and Saccade P3

Although most instances of object recognition during natural viewing occur in the presence of saccades, the neural correlates of objection recognition have almost exclusively been examined during fixation. Recent studies have indicated that there are post-saccadic modulations of neural activity immediately following eye movement landing; however, whether post-saccadic modulations affect relatively late occurring cognitive components such as the P3 has not been explored. The P3 as conventionally measured at fixation is commonly used in brain computer interfaces, hence characterizing the post-saccadic P3 could aid in the development of improved brain computer interfaces that allow for eye movements. In this study, the P3 observed after saccadic landing was compared to the P3 measured at fixation. No significant differences in P3 start time, temporal persistence, or amplitude were found between fixation and saccade trials. Importantly, sensory neural responses canceled in the target minus distracter comparisons used to identify the P3. Our results indicate that relatively late occurring cognitive neural components such as the P3 are likely less sensitive to post saccadic modulations than sensory neural components and other neural activity occurring shortly after eye movement landing. Furthermore, due to the similarity of the fixation and saccade P3, we conclude that the P3 following saccadic landing could possibly be used as a viable signal in brain computer interfaces allowing for eye movements.

A possible human homologue of the macaque V6A

We have recently mapped the retinotopic organization of the area V6 in the human parieto-occipital sulcus thanks to a wide-field retinotopic stimulation, up to 168 degrees (Pitzalis et al., 2004). In monkey, dorsal and anterior to V6 there is the visuomotor area V6A. Monkey V6A is retinotopically less organized than V6, showing only a rough tendency for the eccentricity to increase dorso-ventrally in both the anterior bank of POS and the precuneate cortex (Galletti et al. 1996, 1999a). Visuomotor neurons in V6A have been found to respond more during reaches than during saccades to visual targets. Here we used phase-encoded fMRI, cortical flattening and wide-filed retinotopic mapping to detect the presence in the human POS of a visual area having retinotopic properties similar to those of the macaque area V6A. We also combined event-related fMRI with cortical surface reconstruction, in order to isolate movement-related activity for reaching and saccades in relation to the individual sulcal anatomy. We found an area in the POS located just anteriorly to V6 and medial to V3A which has an inconsistent polar angle representation but a clear trend in the eccentricity maps. In agreement with functional data on monkey V6A, this region of the human brain shows a marginal effect of cue location (contralateral side slightly preferred) and a transient activity during reaching trials stronger than during saccade trials. We propose that this region may be the putative homologous of area V6A.

The effects of natural scenes and saccades on V1 orientation selectivity

In many experiments, control over visual stimulation is obtained by sacrificing much of the complexity of the natural world and visual behavior. For example, stimuli are presented on iso-luminant backgrounds and they are flashed instead of swept into view via saccades. In this experiment, we investigated the influence of complex natural backgrounds and saccades on the development of orientation selectivity in macaque V1. Four conditions were compared: Bars of light were either flashed into the receptive field or brought into the RF through a saccade. Different flash and saccade trials were run with iso-luminant gray and natural image backgrounds. Average response amplitudes were usually lower with a natural than gray background. Comparing flash and saccade conditions gave more variable results. From cell-to-cell the flash response was higher or lower than the saccade response. The differences in average response amplitude across conditions appeared to be consistent with gain changes rather than changes in optimal orientation or tuning width. There were also significant effects of the presentation paradigm on the timing of selectivity. Orientation selectivity generally appeared slower with a natural than a gray background. Selectivity usually developed faster when stimuli appeared from a flash rather than a saccade. Comparing the least (flash/gray) and most natural (saccade/natural) paradigms, there was often a significant difference in the timing of maximal selectivity (tens of msec). These results indicate that the more natural paradigms recruit additional neural circuitry that decreases response amplitude and delays orientation selectivity. This suggests that in natural visual situations, the earliest form-selective V1 response carries potentially important information about stimulus context that is different from that available in reduced paradigms.

The Responses of Visual Neurons in the Frontal Eye Field Are Biased for Saccades

Previous research suggests that visually responsive neurons in the frontal eye field (FEF) respond to visual targets even when they are not the goal of a saccadic eye movement. These results raise the possibility that these neurons respond to visual targets independent of the effector that is to be used to acquire the target locations. In the present study, we examined whether a plan to execute a saccade or a reach to a visual target influenced the response to and the representation of targets in the FEF. We recorded single unit responses to the onset of the target, during the delay period, and around the time of the movement, on interleaved saccade and reach trials of a delayed-response task. We found that the responses of approximately equal percentages of visual, visuomovement, and movement neurons (50%, 58%, and 58%, respectively) were greater on saccade trials than on reach trials in at least one interval of the delayed-response task. Converse biases, in favor of reaches, were much less frequent (13%, 10%, and 19%, in visual, visuomovement, and movement neurons respectively). Thus, although visual neurons may not be directly involved in triggering saccadic eye movements, they are nonetheless highly saccade-biased, with percentages comparable to neurons that are directly involved in triggering saccadic eye movements.

The Relationship between Saccadic Suppression and Perceptual Stability

Introspection makes it clear that we do not see the visual motion generated by our saccadic eye movements. We refer to the lack of awareness of the motion across the retina that is generated by a saccade as saccadic omission [1]: the visual stimulus generated by the saccade is omitted from our subjective awareness. In the laboratory, saccadic omission is often studied by investigating saccadic suppression, the reduction in visual sensitivity before and during a saccade (see Ross et al. [2] and Wurtz [3] for reviews). We investigated whether perceptual stability requires that a mechanism like saccadic suppression removes perisaccadic stimuli from visual processing to prevent their presumed harmful effect on perceptual stability [4, 5]. Our results show that a stimulus that undergoes saccadic omission can nevertheless generate a shape contrast illusion. This illusion can be generated when the inducer and test stimulus are separated in space and is therefore thought to be generated at a later stage of visual processing [6]. This shows that perceptual stability is attained without removing stimuli from processing and suggests a conceptually new view of perceptual stability in which perisaccadic stimuli are processed by the early visual system, but these signals are prevented from reaching awareness at a later stage of processing.

Isolation of saccade inhibition processes: Rapid event-related fMRI of saccades and nogo trials

Previous functional magnetic resonance imaging (fMRI) studies have compared saccade trials and nogo trials, which required subjects to look at peripheral visual stimuli and to inhibit automatic saccades evoked by peripheral stimuli, respectively. These studies surprisingly reported no activation differences in cortical saccade regions between the two tasks, despite their opposite response requirements. Here, we re-examined this issue by comparing saccades and nogo trials using a rapid event-related fMRI design in which saccade trials were presented twice as frequently as nogo trials to make the saccade response more prepotent. We hypothesized that this should increase recruitment of response inhibition processes in the nogo task, thereby increasing fMRI activation on nogo trials. Saccade and nogo trials were presented in whole and half trial versions. Whereas whole trials included a trial type instruction followed by peripheral stimulus presentation and subject response, half trials included only the instruction component, allowing us to measure instruction-related activation separately from response-evoked signals for both saccades and nogo trials. Instruction-related activation was greater for nogo versus saccade trials in right frontal eye field, middle frontal gyrus, intraparietal sulcus, and precuneus, which we attribute to a mixture of preparatory and task switching processes. Response-related activation was greater for nogo trials in supplementary eye field, anterior cingulate cortex, inferior frontal gyrus, and right supramarginal gyrus, and we attribute these results to saccade inhibition and other processes associated with an increased requirement for inhibition of the automatic saccade in nogo trials.

Preparatory Delay Activity in the Monkey Parietal Reach Region Predicts Reach Reaction Times

To acquire something that we see, visual spatial information must ultimately result in the activation of the appropriate set of muscles. This sensory to motor transformation requires an interaction between information coding target location and information coding which effector will be moved. Activity in the monkey parietal reach region (PRR) reflects both spatial information and the effector (arm or eye) that will be used in an upcoming reach or saccade task. To further elucidate the functional role of PRR in visually guided movement tasks and to obtain evidence that PRR signals are used to drive arm movements, we tested the hypothesis that increased neuronal activity during a preparatory delay period would lead to faster reach reaction times but would not be correlated with saccade reaction times. This proved to be the case only when the type of movement and not the spatial goal of that movement was known in advance. The correlation was strongest in cells that showed significantly more activity on arm reach compared with saccade trials. No significant correlations were found during delay periods in which spatial information was provided in advance. These data support the idea that PRR constitutes a bottleneck in the processing of spatial information for an upcoming arm reach. The lack of a correlation with saccadic reaction time also supports the idea that PRR processing is effector specific, that is, it is involved in specifying targets for arm movements but not targets for eye movements.

Evidence for Ocular Motor Deficits in Developmental Dyslexia: Application of the Double-Step Paradigm

Dyslexia is a language-based learning disability characterized by difficulties with reading, spelling, and writing. Persons with dyslexia often have deficits in processing rapid temporal sensory information. There is also evidence of sensorimotor deficits in persons with dyslexia. Whether these deficits include ocular motor problems is still an open question. Some previous studies have shown an increased saccadic latency in dyslexics, whereas others have not reproduced this finding. The purpose of the present study was to investigate saccadic latency in young adults with dyslexia during the double-step paradigm, a task that requires rapid sequential visual information processing and saccade generation. The study hypothesis was that dyslexics have a longer saccadic latency in the second orthogonal saccade, a task that nondyslexics parallel process and perform rapidly. Eight students with dyslexia and eight age-matched control subjects participated in the study. Their eye movements were monitored with the scleral search coil technique in simple saccade trials and in the double-step paradigm. The second saccade was either orthogonal or colinear to the first. Intersaccadic interval and latency were calculated for the second saccade. No difference in saccadic latency was found for colinear second saccades; however, dyslexics had significantly longer latencies for orthogonal second saccades. This included a subset of subjects who had longer latencies for orthogonal than for colinear saccades. The findings indicate that under certain conditions, when the demand for rapid visual information processing is high and a rapid saccade sequence is required, some persons with dyslexia show ocular motor deficits manifested by longer saccadic latencies.