Long-lasting modifications of saccadic eye movements following adaptation induced in the double-step target paradigm

The adaptation of saccadic eye movements to environmental changes occurring throughout life is a good model of motor learning and motor memory. Numerous studies have analyzed the behavioral properties and neural substrate of oculomotor learning in short-term saccadic adaptation protocols, but to our knowledge, none have tested the persistence of the oculomotor memory. In the present study, the double-step target protocol was used in five human subjects to adaptively decrease the amplitude of reactive saccades triggered by a horizontally-stepping visual target. We tested the amplitude of visually guided saccades just before and at different times (up to 19 days) after the adaptation session. The results revealed that immediately after the adaptation session, saccade amplitude was significantly reduced by 22% on average. Although progressively recovering over days, this change in saccade gain was still statistically significant on days 1 and 5, with an average retention rate of 36% and 19%, respectively. On day 11, saccade amplitude no longer differed from the pre-adaptation value. Adaptation was more effective and more resistant to recovery for leftward saccades than for rightward ones. Lastly, modifications of saccade gain related to adaptation were accompanied by a decrease of both saccade duration and peak velocity. A control experiment indicated that all these findings were specifically related to the adaptation protocol, and further revealed that no change in the main sequence relationships could be specifically related to adaptation. We conclude that in humans, the modifications of saccade amplitude that quickly develop during a double-step target adaptation protocol can remain in memory for a much longer period of time, reflecting enduring plastic changes in the brain.     

Saccadic Eye Movements in Parkinson's Disease: I. Delayed Saccades

The saccadic eye movements of nine patients with Parkinson's disease were compared to those of nine age-matched controls in two paradigms generating volitional saccades. In both paradigms, subjects had to make delayed saccades to peripheral LED targets: a peripheral target appeared 700 msec before a buzzer sounded, the buzzer being the signal to make a saccade to the target. In the first paradigm (“centre-off”), the fixation target was extinguished simultaneously with buzzer onset. In the second (“centre-remain”) it was not extinguished until 1000 msec later. The results showed that for outward saccades in both paradigms, there was no difference between Parkinsonian patients and controls, but saccadic latencies were significantly shorter in the “centre-remain” paradigm. The initial outward saccades were indistinguishable from the normal, reflex saccades of the same subjects. However, saccades returning to the centre (a type of remembered target saccade) were hypometric and showed multistepping. Both effects were more pronounced in patients with Parkinson's disease. The significance of these findings in terms of current hypotheses about the nature of the Parkinsonian saccadic deficit is discussed.     

Bottom-up effects modulate saccadic latencies in well-known eye movement paradigm

A well-known eye movement paradigm combines saccades (fast eye movements) with a perceptual discrimination task. At a variable time after the onset of a central arrow cue indicating the target direction [the stimulus onset asynchrony (SOA)], discrimination symbols appear briefly at saccade target and non-target locations. A previous study revealed an unexpected effect of SOA on saccadic latencies: latencies were longer in trials with longer SOAs. It was suggested that this effect reflects a top-down process as observers may wait for the discrimination symbol to appear before executing saccades. However, symbol onsets may also modulate saccade latencies from the bottom-up. To clarify the origin of the SOA effect on latencies in this paradigm, we used a simplified version of the original task plus two new symbol onset conditions for comparison. The results indicate that the modulation of saccadic latencies was not due to a top-down strategy, but to a combination of two opposing bottom-up effects: the symbol onsets at the target location shortened saccade latencies, while symbol onsets at non-target locations lengthened saccade latencies.     

Quantifying the performance limits of human saccadic targeting during visual search.

In previous studies of saccadic targeting, the issue how visually guided saccades to unambiguous targets are programmed and executed has been examined. These studies have found different degrees of guidance for saccades depending on the task and task difficulty. In this study, we use ideal-observer analysis to estimate the visual information used for the first saccade during a search for a target disk in noise. We quantitatively compare the performance of the first saccadic decision to that of the ideal observer (ie absolute efficiency of the first saccade) and to that of the associated final perceptual decision at the end of the search (ie relative efficiency of the first saccade). Our results show, first, that at all levels of salience tested, the first saccade is based on visual information from the stimulus display, and its highest absolute efficiency is approximately 20%. Second, the efficiency of the first saccade is lower than that of the final perceptual decision after active search (with eye movements) and has a minimum relative efficiency of 19% at the lowest level of saliency investigated. Third, we found that requiring observers to maintain central fixation (no saccades allowed) decreased the absolute efficiency of their perceptual decision by up to a factor of two, but that the magnitude of this effect depended on target salience. Our results demonstrate that ideal-observer analysis can be extended to measure the visual information mediating saccadic target-selection decisions during visual search, which enables direct comparison of saccadic and perceptual efficiencies.     

Visual motion shifts saccade targets

Saccades are made thousands of times a day and are the principal means of localizing objects in our environment. However, the saccade system faces the challenge of accurately localizing objects as they are constantly moving relative to the eye and head. Any delays in processing could cause errors in saccadic localization. To compensate for these delays, the saccade system might use one or more sources of information to predict future target locations, including changes in position of the object over time, or its motion. Another possibility is that motion influences the represented position of the object for saccadic targeting, without requiring an actual change in target position. We tested whether the saccade system can use motion-induced position shifts to update the represented spatial location of a saccade target, by using static drifting Gabor patches with either a soft or a hard aperture as saccade targets. In both conditions, the aperture always remained at a fixed retinal location. The soft aperture Gabor patch resulted in an illusory position shift, whereas the hard aperture stimulus maintained the motion signals but resulted in a smaller illusory position shift. Thus, motion energy and target location were equated, but a position shift was generated in only one condition. We measured saccadic localization of these targets and found that saccades were indeed shifted, but only with a soft-aperture Gabor patch. Our results suggest that motion shifts the programmed locations of saccade targets, and this remapped location guides saccadic localization.     

The reduction of saccadic latency by prior offset of the fixation point: an analysis of the gap effect

The latency to initiate a saccade (saccadic reaction time) to an eccentric target is reduced by extinguishing the fixation stimulus prior to the target onset. Various accounts have attributed this latency reduction (referred to as the gap effect) to facilitated sensory processing, oculomotor readiness, or attentional processes. Two experiments were performed to explore the relative contributions of these factors to the gap effect. Experiment 1 demonstrates that the reduction in saccadic reaction time (RT) produced by fixation point offset is additive with the effect of target luminance. Experiment 2 indicates that the gap effect is specific for saccades directed toward a peripheral target and does not influence saccades directed away from the target (i.e., antisaccades) or choice-manual RT. The results are consistent with an interpretation of the gap effect in terms of facilitated premotor processing in the superior colliculus.     

Saccadic Eye Movements in Parkinson's Disease: II. Remembered Saccades— Towards a Unified Hypothesis?

Ten patients with mild to moderate Parkinson's disease were compared with ten age-matched normal controls in a series of saccadic paradigms in order to test various hypotheses relating to the origin of the Parkinsonian saccadic defect. The paradigms comprised a reflex saccade paradigm, a standard remembered saccade paradigm, a remembered saccade paradigm with delayed centre-offset, and a remembered saccade paradigm with a second target flash immediately prior to saccade execution. Finally, subjects executed both reflex and remembered saccades in a standard remembered paradigm (the “two-saccade” paradigm). As has been reported previously, Parkinsonian subjects demonstrated hypometria on all remembered saccade paradigms, particularly the “two-saccade” paradigm. There was, however, no significant difference between the first three remembered saccade paradigms. These studies serve to refute a simple attentional capture hypothesis, and a hypothesis that suggests that the abnormality of remembered saccades is due to concurrent reflex saccade suppression. On the basis of the results, further hypotheses are advanced in an attempt to explain all published work on Parkinsonian saccades.     

A model of saccadic landing positions in reading under the influence of sensory noise

During reading, saccadic eye movements are produced to move the high acuity foveal region of the eye to words of interest for efficient word processing. Distributions of saccadic landing positions peak close to a word's centre but are relatively broad compared to simple oculomotor tasks. Moreover, landing-position distributions are modulated both by distance of the launch site and by saccade type (e.g., one-step saccade, word skipping, refixation). Here we present a mathematical model for the computation of a saccade intended for a given target word. Two fundamental assumptions are related to (1) the sensory computation of the word centre from inter-word spaces and (2) the integration of sensory information and a priori knowledge using Bayesian estimation. Our model was developed for data from a large corpus of eye movements from normal reading. We demonstrate that the model is able simultaneously to account for a systematic shift of saccadic mean landing position with increasing launch-site distance and for qualitative differences between one-step saccades (i.e., from a given word to the next word) and word-skipping saccades.     

The Role of Emotional Content and Perceptual Saliency During the Programming of Saccades Toward Faces

Previous studies have shown that the human visual system can detect a face and elicit a saccadic eye movement toward it very efficiently compared to other categories of visual stimuli. In the first experiment, we tested the influence of facial expressions on fast face detection using a saccadic choice task. Face-vehicle pairs were simultaneously presented and participants were asked to saccade toward the target (the face or the vehicle). We observed that saccades toward faces were initiated faster, and more often in the correct direction, than saccades toward vehicles, regardless of the facial expressions (happy, fearful, or neutral). We also observed that saccade endpoints on face images were lower when the face was happy and higher when it was neutral. In the second experiment, we explicitly tested the detection of facial expressions. We used a saccadic choice task with emotional-neutral pairs of faces and participants were asked to saccade toward the emotional (happy or fearful) or the neutral face. Participants were faster when they were asked to saccade toward the emotional face. They also made fewer errors, especially when the emotional face was happy. Using computational modeling, we showed that this happy face advantage can, at least partly, be explained by perceptual factors. Also, saccade endpoints were lower when the target was happy than when it was fearful. Overall, we suggest that there is no automatic prioritization of emotional faces, at least for saccades with short latencies, but that salient local face features can automatically attract attention.     

Having to identify a target reduces latencies in prosaccades but not in antisaccades

In a princeps study, Trottier and Pratt (2005) showed that saccadic latencies were dramatically reduced when subjects were instructed to not simply look at a peripheral target (reflexive saccade) but to identify some of its properties. According to the authors, the shortening of saccadic reactions times may arise from a top-down disinhibition of the superior colliculus (SC), potentially mediated by the direct pathway connecting frontal/prefrontal cortex structures to the SC. Using a “cue paradigm” (a cue preceded the appearance of the target), the present study tests if the task instruction (Identify vs. Glance) also reduces the latencies of antisaccades (AS), which involve prefrontal structures. We show that instruction reduces latencies for prosaccade but not for AS. An AS requires two processes: the inhibition of a reflexive saccade and the generation of a voluntary saccade. To separate these processes and to better understand the task effect we also test the effect of the task instruction only on voluntary saccades. The effect still exists but it is much weaker than for reflexive saccades. The instruction effect closely depends on task demands in executive resources.     

Memory representations guide targeting eye movements in a natural task

The change blindness phenomenon suggests that visual representations retained across saccades are very limited. In this paper we sought to specify the kind of information that is in fact retained. We investigated targeting performance for saccadic eye movements, since one need for visual representations across eye and body positions may be to guide coordinated movements. We examined saccades in the context of an ongoing sensory motor task in order to make stronger generalizations about natural visual functioning and deployment of attention. Human subjects copied random patterns of coloured blocks on a computer display. Their eye movement pattern was consistent from block to block, including a precise saccade to a previously-placed, neighbouring block during each additional block placement. This natural, consistent eye movement allowed the previously-placed, neighbouring block to serve as an implicit target without instructions to the subject. On random trials, we removed the target object from the display during a preceding saccade, so that observers were required to make the targeting saccade without a currently visible target. Targeting performance was excellent, and appeared to be influenced by spatial information that was not visible during the preceding fixation. Subjects were generally unaware of the disappearance and reappearance of the target. We conclude that spatial information about visual targets is retained across eye movements and used to guide subsequent movements.     

Attention modulates saccadic inhibition magnitude

Visual transient events during ongoing eye movement tasks inhibit saccades within a precise temporal window, spanning from around 60–120 ms after the event, having maximum effect at around 90 ms. It is not yet clear to what extent this saccadic inhibition phenomenon can be modulated by attention. We studied the saccadic inhibition induced by a bright flash above or below fixation, during the preparation of a saccade to a lateralized target, under two attentional manipulations. Experiment 1 demonstrated that exogenous precueing of a distractor's location reduced saccadic inhibition, consistent with inhibition of return. Experiment 2 manipulated the relative likelihood that a distractor would be presented above or below fixation. Saccadic inhibition magnitude was relatively reduced for distractors at the more likely location, implying that observers can endogenously suppress interference from specific locations within an oculomotor map. We discuss the implications of these results for models of saccade target selection in the superior colliculus.     

Suppressing where but not what: the effect of saccades on dorsal- and ventral-stream visual processing

Some cognitive processes are suppressed during saccadic eye movements, whereas others are not. In two experiments, we investigated the locus of this interference effect. In one experiment, subjects decided whether pictured items were objects or nonobjects while making saccades of different lengths. Saccade distance had no effect on response time, indicating that saccades do not interfere with object recognition. However, in a second experiment, in which subjects decided whether pictured items faced to the left or to the right, response time increased with saccade distance, indicating that processing was suppressed during the saccade. These results (along with others) suggest that dorsal-stream (where) processes are suppressed during saccades, whereas ventral-stream (what) processes are not. Because the dorsal stream is instrumental in generating saccades, we propose that cognitive saccadic suppression results from dual-task interference within this visual subsystem.     

Endogenous saccades are preceded by shifts of visual attention: evidence from cross-saccadic priming effects

The present study examines whether endogenous saccades are preceded by shifts of attention. Three experiments are reported in which participants were required to execute a saccadic eye movement to a certain location and to subsequently identify the orientation of a target triangle. Prior to the execution of the saccade a prime was presented, which was compatible or incompatible with the target. A priming effect (faster responses in the compatible condition than in the incompatible condition) occurred only when the prime was presented at the saccade destination, and this effect was larger when the prime was presented during oculomotor programming than when it was presented prior to oculomotor programming. The results indicate that an endogenous shift of attention precedes endogenous saccades, providing further support for theories of visual selection that assume a tight coupling between attention and saccades.     

Mental rotation is suppressed during saccadic eye movements

We examined whether mental rotation is suppressed during saccadic eye movements. Subjects judged whether a character was normal or mirror-reversed while making no, short, or long saccades. Reaction time was longer under saccade than under no-saccade conditions and was longer when a long saccade rather than a short saccade was made, but only when the characters varied in orientation. These results indicate that mental rotation is suppressed during saccadic eye movements. The implications for theories of cognitive suppression during saccades are discussed.     

Enhanced saccadic control in young people with Tourette syndrome despite slowed pro‐saccades

Tourette syndrome (TS) is a neurodevelopmental disorder characterized by motor and vocal tics. Tics are repetitive and uncontrolled behaviours that have been associated with basal ganglia dysfunction. We investigated saccadic eye movements in a group of young people with TS but without co‐morbid ADHD. Participants performed two tasks. One required them to perform only pro‐saccade responses (pure pro‐saccade task). The other involved shifting, unpredictably, between executing pro‐ and anti‐saccades (mixed saccade task). We show that in the mixing saccade task, the TS group makes significantly fewer errors than an age‐matched control group, while responding equally fast. By contrast, on the pure pro‐saccade task, the TS group were shown to be significantly slower to initiate and to complete the saccades (longer movement duration and decreased peak velocity) than controls, while movement amplitude and direction accuracy were not different. These findings demonstrate enhanced shifting ability despite slower reflexive responding in TS and are discussed with respect to a disorder‐related adaptation for increased cognitive regulation of behaviour.     

Saccadic localization of visual targets by the very young human infant

The direction, latency, and form of the 1- and 2-month-old human infant’s saccadic eye movements toward peripheral targets were investigated. Infants of both ages reliably executed a directionally appropriate first saccade toward a peripheral target introduced as far as 30 deg from the line of sight along the horizontal and both diagonal axes, but only to 10 deg along the vertical axis. The presence of a second target in the central visual field reduced the probability of peripheral target localization. A significant inverse relation was found between target distance from the line of sight and probability of initiating a directionally appropriate saccade. Electro-oculography revealed that latency to first saccade, although highly variable, was less than 500 msec on a significant proportion of trials. Unlike the adult, the first saccade to target was grossly hypometric and was followed by one or more saccades of approximately equal amplitude to the first.     

The planning and execution of sequential eye movements: saccades do not show the one target advantage

The present experiment examined the one-target advantage (OTA) with regard to saccadic eye movements. The OTA, previously found with manual pointing responses, refers to the finding that movements are executed faster when the limb is allowed to stop on the target compared to the situation where it has to proceed and hit a second target. Using an adapted limb movement OTA task, saccades of 5 degrees and 15 degrees were made to (a) a single target (one-target), (b) one target and immediately to another target without a change in direction (two-target-extension), and (c) one target and immediately back to the start location (two-target-reversal). Unlike manual movements, the movement times for the initial saccade in the two-target-extension condition were not prolonged compared to either of the other two conditions. Moreover, this pattern of results was found for both the shorter and longer amplitude saccades. The results indicate that the OTA does not occur in the oculomotor system and therefore is not a general motor control phenomenon.     

Surface and Edge Information for Spatial Integration: A Saccadic-selection Search Task

Three experiments are described that investigate visual integration across space using a saccade selection paradigm. Subjects saccaded to a vertical target in the presence of a number of horizontal distractor items. Both horizontal and vertical items were composed of two identical elements, so, in order to locate the target, subjects had to integrate the pairs of elements together. We measured saccade accuracy, the proportion of saccades directed to the vertical target, together with saccade latency following display appearance. In Experiment 1 we found that saccade accuracy was improved by the items having either common surface properties or collinear edges. These effects were not a resultof increased display heterogeneity (Experiment 2), or a result of the introduction of a strong internal contour between the items (Experiment 3). These results show that for saccadic selection both surface and edge properties of items are processed. This in turn suggests thatearly visual processing encodes and exploits both types of information.     

Programming saccadic eye movements

This article addresses questions about the preparatory processes that immediately precede saccadic eye movements. Saccade latencies were measured in a task in which subjects were provided partial advance information about the spatial location of a target fixation. In one experiment, subjects were faster in initiating saccades when they knew either the direction or amplitude of the required movement in advance compared to a condition with equal uncertainty about the number of potential saccade targets but without knowledge of the parameters required to execute the movement. These results suggest that the direction and amplitude for an upcoming saccade were calculated separately, and not in a fixed serial order. In another experiment, subjects appear to have programmed the saccades more holistically--with computations of direction and amplitude parameters occurring simultaneously. The implications of these results for models of eye movement preparation are discussed.