Saccadic Suppression Research Articles

Eye movement control during visual pursuit in Parkinson's disease.

BackgroundPrior studies of oculomotor function in Parkinson’s disease (PD) have either focused on saccades without considering smooth pursuit, or tested smooth pursuit while excluding saccades. The present study investigated the control of saccadic eye movements during pursuit tasksand assessed the quality of binocular coordinationas potential sensitive markers of PD.MethodsObservers fixated on a central cross while a target moved toward it. Once the target reached the fixation cross, observers began to pursue the moving target. To further investigate binocular coordination, the moving target was presented on both eyes (binocular condition), or on one eye only (dichoptic condition).ResultsThe PD group made more saccades than age-matched normal control adults (NC) both during fixation and pursuit. The difference between left and right gaze positions increased over time during the pursuit period for PD but not for NC. The findings were not related to age, as NC and young-adult control group (YC) performed similarly on most of the eye movement measures, and were not correlated with classical measures of PD severity (e.g., Unified Parkinson’s Disease Rating Scale (UPDRS) score).DiscussionOur results suggest that PD may be associated with impairment not only in saccade inhibition, but also in binocular coordination during pursuit, and these aspects of dysfunction may be useful in PD diagnosis or tracking of disease course.

Towards virtual reality infinite walking

Redirected walking techniques can enhance the immersion and visual-vestibular comfort of virtual reality (VR) navigation, but are often limited by the size, shape, and content of the physical environments. We propose a redirected walking technique that can apply to small physical environments with static or dynamic obstacles. Via a head- and eye-tracking VR headset, our method detects saccadic suppression and redirects the users during the resulting temporary blindness. Our dynamic path planning runs in real-time on a GPU, and thus can avoid static and dynamic obstacles, including walls, furniture, and other VR users sharing the same physical space. To further enhance saccadic redirection, we propose subtle gaze direction methods tailored for VR perception. We demonstrate that saccades can significantly increase the rotation gains during redirection without introducing visual distortions or simulator sickness. This allows our method to apply to large open virtual spaces and small physical environments for room-scale VR. We evaluate our system via numerical simulations and real user studies.

Probing transsaccadic correspondence with reverse correlation.

The phenomenon of visual stability is classically explained by an internal forward model predicting the sensory consequences of an eye movement based on efference copy. However, this model cannot explain why some object displacements go undetected, a phenomenon that may depend on a passive prior belief that the world is stable. With reverse correlation, we investigated saccadic suppression of displacement and found that transsaccadic correspondence operates differently depending on the position of the postsaccadic visual target relative to the primary landing position; when the signal falls within the extent of primary saccadic scatter, observers are less able to remap accurately. Furthermore, we observed that the neural representations driving perceptual and saccadic decisions are similar when saccading to a target, but that the representations driving transsaccadic correspondence are different from those driving secondary saccades.

Saccadic inhibition in a guided saccade task.

The eye movement system reacts very systematically to visual transients that are presented during the planning phase of a saccade. About 50 to 70 ms after the onset of a transient, the number of saccades that are started decreases, a phenomenon that has been termed saccadic inhibition. Saccades started just before this time window are hypometric compared to regular saccades, presumably because the presentation of the transient stops them in mid-flight. Recent research investigating the properties of repeated saccades to fixed locations found that these early saccades were additionally faster than expected from the main sequence relation, suggesting that a saccadic dead time during which saccades can no longer be modified does not exist. The present study investigated the properties of saccades to random locations in a guided saccade task. As expected, early saccades starting just before the saccadic inhibition dip in frequency were hypometric. Their velocity profiles implied that these saccades were actively stopped after reaching peak velocity. However, the peak velocities of these saccades did not generally deviate from the main sequence relation. The question whether an active stop of early saccades is incompatible with the idea of a saccadic dead time is open to debate.

The contribution of forward masking to saccadic inhibition of return

Inhibition of return is the name typically given to the prolonged latency of motor responses directed to a previously cued target location. There is intense debate about the origins of this effect and its function, but most take for granted (despite lack of evidence) that it depends little on forward masking. Therefore, we re-examined the role of forward masking in inhibition of return. Forward masking was indexed by slower saccadic reaction times (SRTs) when the target orientation repeated the cue orientation at the same location. We confirmed effects of orientation repetition in the absence of an attentional bias when cues were presented on both sides of fixation (bilateral presentation). The effect of orientation repetition was reduced with high target contrast, consistent with a low-level origin such as contrast gain control in early visual areas. When presenting cues on only one side of fixation (unilateral presentation), we obtained inhibition of return with longer cue-target intervals and facilitation with targets presented shortly after the cue. The effect of orientation repetition was reduced when facilitation was observed, but was as strong as with bilateral cues when inhibition of return was observed. Therefore, forward masking may contribute to the inhibition of return effect by delaying reaction times to repeated features at the same location, but is not a principal cause of inhibition of return; in agreement with previous views.Significance statementThe saccadic inhibition of return effect is a reaction-time cost when responding to a pre-cued location. Additional object updating costs are typically invoked to explain reaction-time costs observed when cue and target have the same shape. Yet, lower-level, forward masking of the target by the cue can not be ruled out. Importantly, we show an effect of orientation repetition that is consistent with low-level forward masking rather than object updating costs and that does not interact with inhibition of return.

Perception during double-step saccades

How the visual system achieves perceptual stability across saccadic eye movements is a long-standing question in neuroscience. It has been proposed that an efference copy informs vision about upcoming saccades, and this might lead to shifting spatial coordinates and suppressing image motion. Here we ask whether these two aspects of visual stability are interdependent or may be dissociated under special conditions. We study a memory-guided double-step saccade task, where two saccades are executed in quick succession. Previous studies have led to the hypothesis that in this paradigm the two saccades are planned in parallel, with a single efference copy signal generated at the start of the double-step sequence, i.e. before the first saccade. In line with this hypothesis, we find that visual stability is impaired during the second saccade, which is consistent with (accurate) efference copy information being unavailable during the second saccade. However, we find that saccadic suppression is normal during the second saccade. Thus, the second saccade of a double-step sequence instantiates a dissociation between visual stability and saccadic suppression: stability is impaired even though suppression is strong.

Perceptual enhancement as a result of a top-down attentional influence in a scene viewing task: Evidence from saccadic inhibition.

Prior research has shown that task instructions influence the locations and durations of eye fixations during scene viewing. These task-related changes in gaze patterns are likely to be associated with a top-down influence of attention. Presently we applied a saccadic-inhibition manipulation in order to detect another expected manifestation of top-down attention: perceptual enhancement. Participants viewed eight-item arrays containing photographs from two categories of scenes. Four of the photos depicted natural landscapes ("nature") and the other four depicted urban environments ("buildings"). Participants were instructed to memorize scenes from one of the categories in preparation for a later recognition memory test. During eye fixations the border around the fixated scene flickered briefly from black to white with a random interval between flickers ranging from 400 to 600 ms. We computed the likelihood of a saccade being initiated in the period following the flicker. Consistent with prior research, we found a strong saccadic inhibition effect with maximum saccadic inhibition occurring approximately 97 ms following the flicker. Importantly, the saccadic inhibition effect was stronger and longer lasting when the subject's eyes were fixated on a relevant scene compared to an irrelevant scene. These findings are consistent with perceptual enhancement as a result of top-down attention.

Saccade-based termination responses in macaque V1 and visual perception.

Neurons in visual areas of the brain are generally characterized by the increase in firing rate that occurs when a stimulus is flashed on in the receptive field (RF). However, neurons also increase their firing rate when a stimulus is turned off. These "termination responses" or "after-discharges" that occur with flashed stimuli have been observed in area V1 and they may be important for vision as stimulus terminations have been shown to influence visual perception. The goal of the present study was to determine the strength of termination responses in the more natural situation in which eye movements move a stimulus out of an RF. We find that termination responses do occur in macaque V1 when termination results from a saccadic eye movement, but they are smaller in amplitude compared to flashed-off stimuli. Furthermore, there are termination responses even in the absence of visual stimulation. These findings demonstrate that termination responses are a component of naturalistic vision. They appear to be based on both visual and nonvisual signals in visual cortex. We speculate that the weakening of termination responses might be a neural correlate of saccadic suppression, the loss of perceptual sensitivity around the time of saccades.

Increased gamma band activity for lateral interactions in humans.

Collinear facilitation of contrast sensitivity supported by lateral interactions within primary visual cortex is implicated in contour and object perception, with neural correlates in several frequency bands. Although higher component of the ERP power spectrum, the gamma-band, is postulated to reflect object representation, attention and memory, its neuronal source has been questioned, suggesting it is an artifact reflecting saccadic eye movements. Here we explored the gamma-band activity during collinear facilitation with no saccade-related confounds. We used single-trial spectral analysis of ERP in occipital channels in a time-window of nearly complete saccadic suppression and discarded sporadic trials containing saccades, in order to avoid saccadic artifacts. Although converging evidence suggests that gamma-band oscillations emerge from local excitatory–inhibitory balance involving GABAergic inhibition, here we show activity amplification during facilitatory collinear interactions, presumably dominated by excitations, in the gamma-band 150–350 milliseconds following onset of low near-threshold contrast stimulus. This result highlights the potential role of gamma-band oscillations in neuronal encoding of basic processes in visual perception. Thus, our findings suggest that gamma-band ERP spectrum analysis may serve as a useful and reliable tool for exploring basic perception, both in normal adults and in special populations.

Saccade Reorienting Is Facilitated by Pausing the Oculomotor Program.

As we look around the world, selecting our targets, competing events may occur at other locations. Depending on current goals, the viewer must decide whether to look at new events or to ignore them. Two experimental paradigms formalize these response options: double-step saccades and saccadic inhibition. In the first, the viewer must reorient to a newly appearing target; in the second, they must ignore it. Until now, the relationship between reorienting and inhibition has been unexplored. In three experiments, we found saccadic inhibition ∼100 msec after a new target onset, regardless of the task instruction. Moreover, if this automatic inhibition is boosted by an irrelevant flash, reorienting is facilitated, suggesting that saccadic inhibition plays a crucial role in visual behavior, as a bottom-up brake that buys the time needed for decisional processes to act. Saccadic inhibition may be a ubiquitous pause signal that provides the flexibility for voluntary behavior to emerge.

12. The Role of the Human Prefrontal Cortex in the Response Suppression of Eye Movements

Increased activity in a population of prefrontal cortex neurons has been shown, in previous studies, to precede correct anti‐saccades in primates. In addition, the time courses of two competing processes in these neurons, task selection (which prepares for an eye movement) and saccade suppression (which prepares for the suppression of an eye movement), intersect at a specific time after the presentation of a coloured instruction cue. The purpose of this study is to use eye tracking behaviour to investigate this intersection point and its role in response suppression in regard to the generation of anti‐saccades in humans. Subjects were instructed before a stimulus appears, using a colour cue, to either look towards the stimulus (pro‐saccade) or away from the stimulus (anti‐saccade). Instruction period times varied from 100ms to 1400ms, in 50ms steps. Based on previous primate electrophysiological data, the ratio of direction errors (pro‐saccades on anti‐saccade trials) to correct anti‐saccades was expected to increase around 400ms to 500ms, when the processes of task selection and saccade suppression diverge. A slight ratio increase was found and full results are forthcoming.

Eye Movements in Parkinson's Disease and Inherited Parkinsonian Syndromes.

Despite extensive research, the functions of the basal ganglia (BG) in movement control have not been fully understood. Eye movements, particularly saccades, are convenient indicators of BG function. Here, we review the main oculomotor findings reported in Parkinson’s disease (PD) and genetic parkinsonian syndromes. PD is a progressive, neurodegenerative disorder caused by dopaminergic cell loss within the substantia nigra pars compacta, resulting in depletion of striatal dopamine and subsequent increased inhibitory BG output from the internal globus pallidus and the substantia nigra pars reticulata. Eye movement abnormalities are common in PD: anomalies are more evident in voluntary than reflexive saccades in the initial stages, but visually guided saccades may also be involved at later stages. Saccadic hypometria (including abnormally fragmented saccades), reduced accuracy, and increased latency are among the most prominent deficits. PD patients show also unusually frequent and large square wave jerks and impaired inhibition of reflexive saccades when voluntary mirror saccades are required. Poor convergence ability and altered pursuit are common. Inherited parkinsonisms are a heterogeneous group of rare syndromes due to gene mutations causing symptoms resembling those of PD. Eye movement characteristics of some parkinsonisms have been studied. While sharing some PD features, each syndrome has a distinctive profile that could contribute to better define the clinical phenotype of parkinsonian disorders. Moreover, because the pathogenesis and the underlying neural circuit failure of inherited parkinsonisms are often well defined, they might offer a better prospect than idiopathic PD to understand the BG function.

Spatio-temporal dynamics of action-effect associations in oculomotor control

While there is ample evidence that actions are guided by anticipating their effects (ideomotor control) in the manual domain, much less is known about the underlying characteristics and dynamics of effect-based oculomotor control. Here, we address three open issues. 1) Is action-effect anticipation in oculomotor control reflected in corresponding spatial saccade characteristics in inanimate environments? 2) Does the previously reported dependency of action latency on the temporal effect delay (action-effect interval) also occur in the oculomotor domain? 3) Which temporal effect delay is optimally suited to develop strong action-effect associations over time in the oculomotor domain? Participants executed left or right free-choice saccades to peripheral traffic lights, causing an (immediate or delayed) action-contingent light switch in the upper vs. lower part of the traffic light. Results indicated that saccades were spatially shifted toward the location of the upcoming change, indicating anticipation of the effect (location). Saccade latency was affected by effect delay, suggesting that corresponding time information is integrated into event representations. Finally, delayed (vs. immediate) effects were more effective in strengthening action-effect associations over the course of the experiment, likely due to greater saliency of perceptual changes occurring during target fixation as opposed to changes during saccades (saccadic suppression). Overall, basic principles underlying ideomotor control appear to generalize to the oculomotor domain.

Saccadic Suppression during Voluntary vs Reactive Saccades

Saccadic Suppression during Voluntary vs Reactive Saccades

Visual features of Saccadic Suppression of Displacement

Visual features of Saccadic Suppression of Displacement

Probing saccadic suppression of displacement with reverse correlation.

Probing saccadic suppression of displacement with reverse correlation.

Fixational eye movements in Tourette syndrome.

Studies of saccadic eye movements in subjects with Tourette syndrome (TS) have provided additional evidence that there is a link between TS symptoms and deficits in fronto-striato-thalamic networks. These studies revealed impaired timing and inhibition of saccades. We compared fixational eye movements, such as microsaccades and ocular drifts, in subjects with TS and healthy controls.We measured horizontal and vertical eye positions with video-oculography in 14 subjects with Tourette syndrome. We found reduced microsaccade amplitude but increased time between adjacent microsaccades (intersaccadic interval). Hence, the rate of microsaccades was reduced in subjects with TS compared to controls. Measure of ocular stability during intersaccadic intervals revealed increased drift velocity and increased variance in eye position. We hypothesize that increased activity of the direct fronto-striatal pathway and the resulting reduction in basal ganglia outflow targeting the superior colliculus fixation zone affect the rate and amplitude of microsaccades in subjects with TS. The resulting impairment in frontal eye field fixation leads to increased drifts during intersaccadic interval in subjects with TS. Possible clinical implication for these results is that fixational eye movements can be objective biological markers of TS.

Saccade landing position prediction for gaze-contingent rendering

Gaze-contingent rendering shows promise in improving perceived quality by providing a better match between image quality and the human visual system requirements. For example, information about fixation allows rendering quality to be reduced in peripheral vision, and the additional resources can be used to improve the quality in the foveal region. Gaze-contingent rendering can also be used to compensate for certain limitations of display devices, such as reduced dynamic range or lack of accommodation cues. Despite this potential and the recent drop in the prices of eye trackers, the adoption of such solutions is hampered by system latency which leads to a mismatch between image quality and the actual gaze location. This is especially apparent during fast saccadic movements when the information about gaze location is significantly delayed, and the quality mismatch can be noticed. To address this problem, we suggest a new way of updating images in gaze-contingent rendering during saccades. Instead of rendering according to the current gaze position, our technique predicts where the saccade is likely to end and provides an image for the new fixation location as soon as the prediction is available. While the quality mismatch during the saccade remains unnoticed due to saccadic suppression, a correct image for the new fixation is provided before the fixation is established. This paper describes the derivation of a model for predicting saccade landing positions and demonstrates how it can be used in the context of gaze-contingent rendering to reduce the influence of system latency on the perceived quality. The technique is validated in a series of experiments for various combinations of display frame rate and eye-tracker sampling rate.

Pre- and post-saccadic stimulus timing in saccadic suppression of displacement – A computational model

When the target of a saccadic eye movement is displaced while the eyes move this displacement is often not noticed (saccadic suppression of displacement, SSD). We present a neurobiologically motivated, computational model of SSD and compare its simulation results to experimental data. The model offers a simple explanation of the effects of pre- and post-saccadic stimulus blanking on SSD in terms of peri-saccadic network dynamics. Under normal peri-saccadic conditions pre-and post-saccadic stimulus traces are recurrently integrated with reference to present and future eye position, whereas blanking diminishes the pre-saccadic stimulus trace and thus leads to an uninfluenced integration of the post-saccadic stimulus trace. We show that part of the intersubject variability in SSD can be explained by differences in decision thresholds of this integration process.

Saccadic suppression during voluntary versus reactive saccades.

Saccades are fast eye movements that reorient gaze. They can be performed voluntarily-for example, when viewing a scene-but they can also be triggered in reaction to suddenly appearing targets. The generation of these voluntary and reactive saccades have been shown to involve partially different cortical pathways. However, saccades of either type confront the visual system with a major challenge from massive image motion on the retina. Despite the fact that the whole scene is swept across the retina, a saccade usually does not elicit a percept of motion. This saccadic omission has been linked to a transient decrease of visual sensitivity during the eye movement, a phenomenon called saccadic suppression. A passive origin of saccadic suppression based on temporal masking has been proposed as well as an active central process that inhibits visual processing during the saccade. The latter one would need to include an extraretinal signal, which is generated already during saccade preparation. Since saccade generation differs for voluntary and reactive saccades, timing and nature of this extraretinal signal as well as its impact on visual sensitivity might also differ. We measured detection thresholds for luminance stimuli that were flashed during voluntary and reactive saccades and during fixation. Detection thresholds were higher during voluntary than during reactive saccades such that suppression appeared stronger during voluntary saccades. Stronger suppression in voluntary saccades could arise from a stronger extraretinal signal that activates suppression or could indicate that a suppression underlying process itself partially differs between voluntary and reactive saccades.