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.     

Eye movements can cause item-specific visual recognition advantages

Prior research suggests that spontaneous saccades localized towards blank regions of space during memory storage and recall improve memory for items at the saccade locations. In the present study, we examined whether a recognition advantage can be observed when a single, exogenously directed saccade occurs during memory maintenance. We manipulated whether participants made a saccade to an item’s previous location or maintained fixation, as well as whether tested items reappeared in their original location or not. The results of three experiments showed that visual recognition was better after a saccade to the location of a probed object than after no saccade or after a saccade to the location of a non-probed object, so long as saccades went to the to-be-tested location more often than chance. Taken together, our findings demonstrate that eye movements can elicit an item-specific recognition advantage in visual working memory.     

Programming of endogenous and exogenous saccades: evidence for a competitive integration model

Participants were required to make a saccade to a uniquely colored target while ignoring the presentation of an onset distractor. The results provide evidence for a competitive integration model of saccade programming that assumes endogenous and exogenous saccades are programmed in a common saccade map. The model incorporates a lateral interaction structure in which saccade-related activation at a specific location spreads to neighboring locations but inhibits distant locations. In addition, there is top-down, location-specific inhibition of locations to which the saccade should not go. The time course of exogenous and endogenous activation in the saccade map can explain a variety of eye movement data, including endpoints, latencies, and trajectories of saccades and the well-known global effect.     

Expedited suppression signal in ocular go/no-go decision

When scrutinizing the visual world, complex and unexpected stimuli often lead to prolonged eye fixations to enhance cognitive processing, likely by temporarily suppressing a planned saccade. The present study examined whether the suppression signal is tightly linked to a specific planned saccade and if it conforms to the viewer's intention. A novel Go/No-go task was devised where participants made consecutive saccades to fixate a stimulus appearing across the screen horizontal meridian in 4° steps. At times, the features of the stimulus (colour and/or shape) were altered when it reappeared at a new location. Participants had to suppress the saccade that would otherwise leave the stimulus if its features matched instructed criteria. Saccade suppression was determined by the reduced probability for saccades towards and away from a target stimulus. Results show both correct suppression to saccades leaving the target and erroneous suppression to saccades towards it. The erroneous suppression was initially observed for any change in features but later lifted. The suppression shortened the length of saccades leaving a target but not those towards it. The initial suppression during previewing the target appears to be based on expedited but incomplete evaluation of visual stimulus, and is not linked to any specific saccade. These properties might reflect the stage of ocular decision based on which the suppression signal is generated. They also account for the phenomenon of “peripheral-to-foveal” effect on eye movements in reading.     

What are human express saccades?

When a fixation point is removed 200 msec prior to target onset (the gap condition), human subjects are said to produce eye movements that have a short latency (80–120 msec), that form the early peak of a bimodal latency distribution, and that have been labeled “human express saccades” (see, e.g., Fischer, 1987; Fischer & Breitmeyer, 1987; Fischer & Ramsperger, 1984, 1986). In three experiments, we sought to obtain this express saccade diagnostic pattern in the gap condition, We orthogonally combined target location predictability with the presence versus absence of catch trials (Experiment 1). When target location was fixed and catch trials were not used, we found mostly anticipations. In the remaining conditions, where responses were under stimulus control, bimodality was not frequently observed, and, whether it was or not, latencies were not in the express saccade range. Using random target locations, we then varied stimulus luminance and the mode of stimulus presentation (LEDs vs. oscilloscope) in the gap and overlap (fixation is not removed) conditions (Experiment2). Bimodality was rarely observed, the gap effect (overlap minus gap reaction time) was additive with luminance, and only the brightest targets elicited saccades in the express range. When fixed locations and no catch trials were combined with latency feedback (Experiment 3), we observed many responses in the express saccade range and some evidence for bimodality, but the sudden introduction of catch trials revealed that many early responses were not under stimulus control. Humanscan make stimulus-controlled saccades that are initiated very rapidly (80–120 msec), but unless catch trials or choice reaction time is used, it is not possible to distinguish such saccades from anticipatory responses that are prepared in advance and timed to occur shortly after target onset. Because the express saccade diagnostic pattern is not a characteristic feature of human saccadic performance, we urge investigators to focus their attention on the robustgap effect     

The control of saccade trajectories: direction of curvature depends on prior knowledge of target location and saccade latency

Recent reports have shown that saccades can deviate either toward or away from distractors. However, the specific conditions responsible for the change in initial saccade direction are not known. One possibility, examined here, is that the direction of curvature (toward or away from distractors) reflects preparatory tuning of the oculomotor system when the location of the target and distractor are known in advance. This was investigated by examining saccade trajectories under predictable and unpredictable target conditions. In Experiment 1, the targets and the distractors appeared unpredictably, whereas in Experiment 2 an arrow cue presented at fixation indicated the location of the forthcoming target prior to stimulus onset. Saccades were made to targets on the horizontal, vertical, and principal oblique axis, and distractors appeared simultaneously at an adjacent location (a separation of +/- 45 degrees of visual angle). On average, saccade trajectories curved toward distractors when target locations were unpredictable and curved away from distractors when target locations were known in advance. There was no overall difference in mean saccade latencies between the two experiments. The magnitude of the distractor modulation of saccade trajectory (either toward or away from) was comparable across the different saccade directions (horizontal, vertical, and oblique). These results are interpreted in terms of the time course of competitive interactions operating in the neural structures involved in the suppression of distractors and the selection of a saccade target. A relatively slow mechanism that inhibits movements to distractors produces curvature away from the distractor. This mechanism has more time to operate when target location is predictable, increasing the likelihood that the saccade trajectory will deviate away from the distractor.     

Parallel allocation of attention prior to the execution of saccade sequences

In a series of 5 experiments, the allocation of attention prior to the execution of saccade sequences was examined by using a dual-task paradigm. In the primary task, participants were required to execute a sequence of 2 endogenous saccades. The secondary task was a forced-choice letter identification task. During the programming of the saccade sequences, letters were briefly presented at the saccade goals and at no-saccade locations. The results showed that performance was better for letters presented at any of the saccade goals than for letters presented at any of the no-saccade locations. The results support a spatial model that assumes that prior to the execution of a saccade sequence, attention is allocated in parallel to all saccade goals. ((c) 2003 APA, all rights reserved)     

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.     

The relationship between inhibition of return and saccade trajectory deviations

After presentation of a peripheral cue, a subsequent saccade to the cued location is delayed (inhibition of return: IOR). Furthermore, saccades typically deviate away from the cued location. The present study examined the relationship between these inhibitory effects. IOR and saccade trajectory deviations were found after central (endogenous) and peripheral (exogenous) cuing of attention, and both effects were larger with an onset cue than with a color singleton cue. However, a dissociation in time course was found between IOR and saccade trajectory deviations. Saccade trajectory deviations occurred at short delays between the cue and the saccade, but IOR was found at longer delays. A model is proposed in which IOR is caused by inhibition applied to a preoculomotor attentional map, whereas saccade trajectory deviations are caused by inhibition applied to the saccade map, in which the final stage of oculomotor programming takes place.     

The mechanism underlying inhibition of saccadic return

Human observers take longer to re-direct gaze to a previously fixated location. Although there has been some exploration of the characteristics of inhibition of saccadic return (ISR), the exact mechanisms by which ISR operates are currently unknown. In the framework of accumulation models of response times, in which evidence is integrated over time to a response threshold, ISR could reflect a reduction in the rate of accumulation for saccades to return locations or an increase in the effective criterion for response. In two experiments, participants generated sequences of three saccades, in response to a peripheral or a central cue. ISR occurred across these manipulations: saccade latency was consistently increased for movements to the immediately previously fixated location. Latency distributions from individual observers were fit with a Linear Ballistic Accumulator model. ISR was best accounted for as a change in the accumulation rate. We suggest this parameter represents the overall desirability of a particular course of action, the evidence for which may be derived from a variety of sensory and non-sensory sources.     

Visual memory and the perception of a stable visual environment

The visual world appears stable and continuous despite eye movements. One hypothesis about how this perception is achieved is that the contents of successive fixations are fused in memory according to environmental coordinates. Two experiments failed to support this hypothesis; they showed that one's ability to detect a grating presented after a saccade is unaffected by the presentation of a grating with the same spatial frequency in the same spatial location before the saccade. A third experiment tested an alternative explanation of perceptual stability that claims that the contents of successive fixations are compared, rather than fused, across saccades, allowing one to determine whether the world has remained stable. This hypothesis was supported: Experienced subjects could accurately determine whether two patterns viewed in successive fixations were identical or different, even when the two patterns appeared in different spatial positions across the saccade. Taken together, these results suggest that perceptual stability and information integration across saccades rely on memory for the relative positions of objects in the environment, rather than on the spatiotopic fusion of visual information from successive fixations.     

A predictive coding model of gaze shifts and the underlying neurophysiology

A comprehensive model of gaze control must account for a number of empirical observations at both the behavioural and neurophysiological levels. The computational model presented in this article can simulate the coordinated movements of the eye, head, and body required to perform horizontal gaze shifts. In doing so it reproduces the predictable relationships between the movements performed by these different degrees of freedom (DOFs) in the primate. The model also accounts for the saccadic undershoot that accompanies large gaze shifts in the biological visual system. It can also account for our perception of a stable external world despite frequent gaze shifts and the ability to perform accurate memory-guided and double-step saccades. The proposed model also simulates peri-saccadic compression: the mis-localization of a briefly presented visual stimulus towards the location that is the target for a saccade. At the neurophysiological level, the proposed model is consistent with the existence of cortical neurons tuned to the retinal, head-centred, body-centred, and world-centred locations of visual stimuli and cortical neurons that have gain-modulated responses to visual stimuli. Finally, the model also successfully accounts for peri-saccadic receptive field (RF) remapping which results in reduced responses to stimuli in the current RF location and an increased sensitivity to stimuli appearing at the location that will be occupied by the RF after the saccade. The proposed model thus offers a unified explanation for this seemingly diverse range of phenomena. Furthermore, as the proposed model is an implementation of the predictive coding theory, it offers a single computational explanation for these phenomena and relates gaze shifts to a wider framework for understanding cortical function.     

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.     

Perceiving stimulus displacements across saccades

The visual world appears stable despite frequent retinal image movements caused by saccades. Many theories of visual stability assume that extraretinal eye position information is used to spatially adjust perceived locations across saccades, whereas others have proposed that visual stability depends upon coding of the relative positions of objects. McConkie and Currie (1996) proposed a refined combination of these views (called the Saccade Target Object Theory) in which the perception of stability across saccades relies on a local evaluation process centred on the saccade target object rather than on a remapping of the entire scene, with some contribution from memory for the relative positions of objects as well. Three experiments investigated the saccade target object theory, along with an alternative hypothesis that proposes that multiple objects are updated across saccades, but with variable resolution, with the saccade target object (by virtue of being the focus of attention before the saccade and residing near the fovea after the saccade) having priority in the perception of displacement. Although support was found for the saccade target object theory in Experiment 1, the results of Experiments 2 and 3 found that multiple objects are updated across saccades and that their positions are evaluated to determine perceived stability. There is an advantage for detecting displacements of the saccade target, most likely because of visual acuity or attentional focus being better near the fovea, but it is not the saccade target alone that determines the perception of stability and of displacements across saccades. Rather, multiple sources of information appear to contribute.     

Attention doesn’t slide: spatiotopic updating after eye movements instantiates a new, discrete attentional locus

During natural vision, eye movements can drastically alter the retinotopic (eye-centered) coordinates of locations and objects, yet the spatiotopic (world-centered) percept remains stable. Maintaining visuospatial attention in spatiotopic coordinates requires updating of attentional representations following each eye movement. However, this updating is not instantaneous; attentional facilitation temporarily lingers at the previous retinotopic location after a saccade, a phenomenon known as the retinotopic attentional trace. At various times after a saccade, we probed attention at an intermediate location between the retinotopic and spatiotopic locations to determine whether a single locus of attentional facilitation slides progressively from the previous retinotopic location to the appropriate spatiotopic location, or whether retinotopic facilitation decays while a new, independent spatiotopic locus concurrently becomes active. Facilitation at the intermediate location was not significant at any time, suggesting that top-down attention can result in enhancement of discrete retinotopic and spatiotopic locations without passing through intermediate locations.     

Averaging saccades are repelled by prior uninformative cues at both short and long intervals

When two spatially proximal stimuli are presented simultaneously, a first saccade is often directed to an intermediate location between the stimuli (averaging saccade). In an earlier study, Watanabe (2001) showed that, at a long cue–target onset asynchrony (CTOA; 600 ms), uninformative cues not only slowed saccadic response times (SRTs) to targets presented at the cued location in single target trials (inhibition of return, IOR), but also biased averaging saccades away from the cue in double target trials. The present study replicated Watanabe's experimental task with a short CTOA (50 ms), as well as with mixed short (50 ms) and long (600 ms) CTOAs. In all conditions on double target trials, uninformative cues robustly biased averaging saccades away from cued locations. Although SRTs on single target trials were delayed at previously cued locations at both CTOAs when they were mixed, this delay was not observed in the blocked, short CTOA condition. We suggest that top-down factors, such as expectation and attentional control settings, may have asymmetric effects on the temporal and spatial dynamics of oculomotor processing.     

How longer saccade latencies lead to a competition for salience

It has been suggested that independent bottom-up and top-down processes govern saccadic selection. However, recent findings are hard to explain in such terms. We hypothesized that differences in visual-processing time can explain these findings, and we tested this using search displays containing two deviating elements, one requiring a short processing time and one requiring a long processing time. Following short saccade latencies, the deviation requiring less processing time was selected most frequently. This bias disappeared following long saccade latencies. Our results suggest that an element that attracts eye movements following short saccade latencies does so because it is the only element processed at that time. The temporal constraints of processing visual information therefore seem to be a determining factor in saccadic selection. Thus, relative saliency is a time-dependent phenomenon.     

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.     

Remapping versus short-term memory in visual stability across saccades

Saccadic eye movements cause displacements of the image of the visual world projected on the retina. Despite the ubiquitous nature of saccades, subjective experience of the world is continuous and stable. In five experiments, we addressed the mechanisms that may support visual stability: matching of pre- and postsaccadic locations of the target by an internal copy of the saccade, or retention of the visual attributes of the target in short-term memory across the saccade. Healthy human adults were instructed to make a saccade to a peripheral Gabor patch. While the saccade was in midflight, the patch could change location, orientation, or both. The change occurred either immediately or following a 250-ms blank during which no visual stimuli were available. In separate experiments, subjects had to report either whether the patch stepped to the left or right or whether the orientation rotated clockwise or counterclockwise. Consistent with previous findings, we found that transsaccadic displacement discrimination was enhanced by the addition of the blank. However, contrary to previous findings reported in the literature, the feature change did not improve performance. Transsaccadic orientation change discrimination did not depend on either an irrelevant temporal blank or a simultaneous irrelevant target displacement. Taken together, these findings suggest that orientation is not a relevant visual feature for transsaccadic correspondence.     

Inhibition of return generated by voluntary saccades is independent of attentional momentum

Summoning attention to a peripheral location, either by a peripheral cue with the eyes fixed or when a voluntary saccade is made to it and gaze is then returned to the centre, delays detection of subsequent targets at that location compared to a location in the opposite visual field. It has been proposed that oculomotor activation generates this inhibition of return (IOR). This account presupposes that the asymmetry in detection results from inhibition at the cued location rather than facilitation at the uncued location. This has been confirmed for exogenously generated IOR. However, it has not, heretofore, been confirmed for “IOR” generated by voluntary saccades. The current study investigated whether the asymmetry in target detection, elicited either by a peripheral flash or by an eye movement generated in response to a central arrowhead, reflects facilitation at the opposite location due to the path of attentional momentum. Reaction times at the cued location were slower than reaction times at the opposite or perpendicular locations, which did not differ. Opposite facilitation due to attentional momentum requires that opposite be faster than perpendicular, which was not obtained. The results were the same whether IOR was generated by an exogenous cue or by a saccade executed endogenously to a central arrow.