Target similarity affects saccade curvature away from irrelevant onsets

Saccade curvature away from visual distractors is a measure of the salience of these distractors for the oculomotor system. Three experiments are reported in which the integration of luminance onset signals and target similarity signals is examined, using a saccade curvature paradigm. Observers made saccades to a no-onset colour target in one of two positions on the vertical meridian. On most trials, an abrupt onset distractor that was either similar or dissimilar to the target appeared left or right on the horizontal midline. Saccades curved away from the irrelevant onsets; however, the amount of curvature was modulated by target similarity only when the onset appeared before the target (experiment 2) or when saccade initiation was delayed (experiment 3). These results suggest that the initial response to the onset is stimulus-driven and mediated by its transient component. Over time, the response is integrated with and augmented by top-down inputs. Visual and non-visual signals converge onto a common motor map to determine an item's salience.     

Multisensory interactions in saccade target selection: Curved saccade trajectories

In a series of experiments, we examined the change in saccade trajectories observed when distractors are presented at non-target locations. The primary aim of the experiments was to examine multisensory interaction effects between the visual, auditory and somatosensory modalities in saccade generation. In each experiment observers made saccades to visual targets above and below fixation in the presence of visual, auditory or tactile stimuli to the left or right of fixation. In experiment 1 distractor location indicated which of two stimuli was the target for the saccade. Saccade trajectories showed strong leftward curvature following right-side distractors and showed rightward curvature following left-side distractors. The largest effects on trajectories were observed for visual distractors, but significant curvature was observed with auditory and somatosensory distractors. In experiment 2 saccades were made following the onset of a visual target (reflexive) or following presentation of an arrow at fixation (voluntary), and task-irrelevant crossmodal distractors were presented simultaneously with target onset. Both voluntary and reflexive saccades were found to curve away from task-irrelevant visual distractors, but auditory and somatosensory distractors did not modulate saccade trajectories. In experiment 3 task-irrelevant distractors preceded the onset of the target by 100 ms. Reflexive saccades were found to curve away from visual, auditory and somatosensory distractors, but voluntary saccades curved away from visual distractors only. The modulation of saccade trajectories by distractors from different modalities is interpreted in terms of inhibitory processes operating in neural structures involved in saccade generation. Our findings suggest that visual, auditory and somatosensory distractors can all modulate saccade trajectories. Such effects could be related to the inhibition of populations of neurons, in a common motor map, for the selection of a saccade target.     

Distractor modulation of saccade trajectories: spatial separation and symmetry effects

The trajectories of saccadic eye movements can be modulated by the presence of a competing visual distractor. In the present study the trajectories of vertical saccades curved away from a single visual distractor presented in one visual field, but tended to be straight when two distractors were presented at mirror symmetric locations in both visual fields. The spatial nature of the mirror distractor effect was examined by presenting a second distractor at mirror and non-mirror locations. Saccade trajectories also tended to be straight with both mirror and non-mirror symmetrical distractors. The relationship between the distractor location and saccade curvature was examined in a third experiment by manipulating the distractor-to-target spatial separation. Although there was a tendency for greater curvature when the distractor was presented in the same hemifield as the target there was no clear relationship between curvature and distractor location. The results show that the distractor modulation of saccade trajectory is not highly spatially specific and that it can be balanced by a second bilateral distractor in the opposite visual field. The results are interpreted in terms of a model in which the initial saccade direction and curvature back towards the saccade goal are controlled by separate processes. Initial saccade direction is modulated by the inhibition of distractor locations within a motor map specifying saccade direction. Curvature back towards the saccade goal may be attributed to a feedback system, with a separate representation of the visual target location, that enables an on-line correction of the saccade during mid-flight.     

The intrinsic value of visual information affects saccade velocities

Let us assume that the purpose of any movement is to position our body in a more advantageous or rewarding state. For example, we might make a saccade to foveate an image because our brain assigns an intrinsic value to the information that it expects to acquire at the endpoint of that saccade. Different images might have different intrinsic values. Optimal control theory predicts that the intrinsic value that the brain assigns to targets of saccades should be reflected in the trajectory of the saccade. That is, in anticipation of foveating a highly valued image, our brain should produce a saccade with a higher velocity and shorter duration. Here, we considered four types of images: faces, objects, inverted faces, and meaningless visual noise. Indeed, we found that reflexive saccades that were made to a laser light in anticipation of viewing an image of a face had the highest velocities and shortest durations. The intrinsic value of visual information appears to have a small but significant influence on the motor commands that guide saccades.     

Curved saccade trajectories: Voluntary and reflexive saccades curve away from irrelevant distractors

In this study we examined the impact of irrelevant distractors upon trajectories of reflexive and voluntary saccades. Observers made saccades to visual targets above and below fixation as directed by target appearance (reflexive) or by a central directional cue (voluntary) in the presence of an irrelevant distractor stimulus (a cross) whose appearance was simultaneous with target onset. We recorded saccade latency, amplitude and the magnitude of saccade curvature relative to the direct route from the start-to-end of the saccade. Previous studies of saccades curvature have used distractors to provide information about the saccade task and, as a result, have only examined trajectories of voluntary saccades. However, we have shown that both reflexive and voluntary saccades curved away from irrelevant distractors. The effect of irrelevant distractors indicates that observers do not need to attend to distractors in a voluntary fashion for distractors to modify saccade trajectories. Furthermore, it highlights an important parallel in curvature of saccades and reach trajectories, namely that both curve away from irrelevant distractors. The second important observation was that reflexive, as well as voluntary, saccades curved away from distractors. This suggests that curvature is not solely a consequence of voluntary control. These results have been considered within the context of inhibition-based theories of curvature derived from studies of saccade and manual reach trajectories. Electronic Publication     

Distractor effects on saccade trajectories: a comparison of prosaccades, antisaccades, and memory-guided saccades

The present study investigated the contribution of the presence of a visual signal at the saccade goal on saccade trajectory deviations and measured distractor-related inhibition as indicated by deviation away from an irrelevant distractor. Performance in a prosaccade task where a visual target was present at the saccade goal was compared to performance in an anti- and memory-guided saccade task. In the latter two tasks no visual signal is present at the location of the saccade goal. It was hypothesized that if saccade deviation can be ultimately explained in terms of relative activation levels between the saccade goal location and distractor locations, the absence of a visual stimulus at the goal location will increase the competition evoked by the distractor and affect saccade deviations. The results of Experiment 1 showed that saccade deviation away from a distractor varied significantly depending on whether a visual target was presented at the saccade goal or not: when no visual target was presented, saccade deviation away from a distractor was increased compared to when the visual target was present. The results of Experiments 2–4 showed that saccade deviation did not systematically change as a function of time since the offset of the target. Moreover, Experiments 3 and 4 revealed that the disappearance of the target immediately increased the effect of a distractor on saccade deviations, suggesting that activation at the target location decays very rapidly once the visual signal has disappeared from the display.

Significance of attentive fixation for the selection of saccade targets in different parts of the visual field of the rhesus monkey

Summary Two monkeys were presented with a task in which they were free to make a saccade to one of two simultaneously presented targets. The data from both animals show that the preference for one of the targets depends on at least two factors: (i) active and attentive fixation of the central fixation point at the time when the two targets occur; (ii) relative position of the two targets in the visual field. The results were different for the two monkeys with respect to the role of stimulus position in the visual field. However, both animals changed their preference systematically when the fixation point was turned off before the two targets occurred as compared to the case in which the fixation point remained visible. With respect to the paradigm (fixation point off versus fixation point on) the stimulus selection of either animal was constant throughout the several weeks of testing.     

Competition between saccade goals in the superior colliculus produces saccade curvature

When saccadic eye movements are made in a search task that requires selecting a target from distractors, the movements show greater curvature in their trajectories than similar saccades made to single stimuli. To test the hypothesis that this increase in curvature arises from competitive interactions between saccade goals occurring near the time of movement onset, we performed single-unit recording and microstimulation experiments in the superior colliculus (SC). We found that saccades that ended near the target but curved toward a distractor were accompanied by increased presaccadic activity of SC neurons coding the distractor site. This increased activity occurred approximately 30 ms before saccade onset and was abruptly quenched on saccade initiation. The magnitude of increased activity at the distractor site was correlated with the amount of curvature toward the distractor. In contrast, neurons coding the target location did not show any significant difference in discharge for curved versus straight saccades. To determine whether this pattern of SC discharge is causally related to saccade curvature, we performed a second series of experiments using electrical microstimulation. Monkeys made saccades to single visual stimuli presented without distractors, and we stimulated sites in the SC that would have corresponded to distractor sites in the search task. The stimulation was subthreshold for evoking saccades, but when its temporal structure mimicked the activity recorded for curved saccades in search, the subsequent saccades to the visual target showed curvature toward the location coded by the stimulation site. The effect was larger for higher stimulation frequencies and when the stimulation site was in the same colliculus as the representation of the visual target. These results support the hypothesis that the increased saccade curvature observed in search arises from rivalry between target and distractor goals and are consistent with the idea that the SC is involved in the competitive neural interactions underlying saccade target selection.     

Visual mislocalization during saccade sequences

Visual objects briefly presented around the time of saccadic eye movements are perceived compressed towards the saccade target. Here, we investigated perisaccadic mislocalization with a double-step saccade paradigm, measuring localization of small probe dots briefly flashed at various times around the sequence of the two saccades. At onset of the first saccade, probe dots were mislocalized towards the first and, to a lesser extent, also towards the second saccade target. However, there was very little mislocalization at the onset of the second saccade. When we increased the presentation duration of the saccade targets prior to onset of the saccade sequence, perisaccadic mislocalization did occur at the onset of the second saccade.     

Obligatory adaptation of saccade gains

We tested the hypothesis that saccade gains adapt to minimize error between the visual target and the saccade endpoint of every saccade we make even when the errors on sequential saccades are not directionally consistent. We utilized a state-space model that estimated the degree to which saccade gains were modified by the magnitude and direction of errors made on the previous trial. Importantly, to show that learning did not depend on the accumulation of directionally consistent errors, we fit the model to saccades made to targets that were displaced in a random direction during the saccade, thereby inducing errors with directions that were not sequentially the same. Saccade gains clearly adapted on a trial-by-trial basis despite that the perturbations were random, and the average amount of learning per trial was of similar magnitude as that found in a constant displacement of the target. These results indicate that saccade adaptation is a rapid and obligatory process that does not require conscious awareness.     

Bilateral interactions in saccade programming

Subjects were required to make a saccade to a target appearing randomly 4° to the left or right of the current fixation position (1280 trials per experiment). Location cues were used to direct visual attention and start saccade preparation to one of the two locations before target onset. When the cue indicated the target location (valid trials), the generation of express saccades (visually guided saccades with latencies around 100 ms) was strongly facilitated. When the opposite location was cued (invalid trials), express saccades were abolished and replaced by a population of mainly fast-regular saccades (latencies around 150 ms). This was found with a peripheral cue independently of whether the fixation point was removed before target onset (gap condition; experiment 1) or remained on throughout the trial (overlap condition; experiment 2). The same pattern also was observed with a central cue that did not involve any visual stimulation at a peripheral location (experiment 3). In the case where the primary saccade was executed in response to the cue and the target appeared at the opposite location, continuous amplitude transition functions were observed: starting at about 60–70 ms from target onset onward, the amplitude of the cue-elicited saccades continuously decreased from 4° to values below 1°. The results are explained by a fixation-gating model, according to which the antagonism between fixation and saccade activity gives rise to multimodal distributions of saccade latencies. It is argued that allocation of visual attention and saccade preparation to one location entails a successive disengagement of the fixation system controlling saccade preparation within the hemifield to which the saccade is prepared and a partial engagement of the opposite fixation system.     

Context-specific adaptation of saccade gain

Previous studies established that vestibular reflexes can have two adapted states (e.g., gain) simultaneously, and that a context cue (e.g., vertical eye position) can switch between the two states. The present study examined this phenomenon of context-specific adaptationfor horizontal saccades, using a variety of contexts. Our overall goal was to assess the efficacy of different context cues in switching between adapted states. A standard double-step paradigm was used to adapt saccade gain. In each experiment, we asked for a simultaneous gain decrease in one context and gain increase in another context, and then determined if a change in the context would invoke switching between the adapted states. Horizontal eye position worked well as a context cue: saccades with the eyes deviated to the right could be made to have higher gains while saccades with the eyes deviated to the left could be made to have lower gains. Vertical eye position was less effective. This suggests that the more closely related a context cue is to the response being adapted, the more effective it is. Roll tilt of the head, and upright versus supine orientations, were somewhat effective in context switching; these paradigms contain orientation of gravity with respect to the head as part of the context.     

Reaching beyond reach

 The analysis of errors in two-joint reaching movements has provided clues about sensorimotor processing algorithms. The present study extends this focus to situations where the head, trunk, and legs join with the arm to help reach targets placed slightly beyond arm’s length. Subjects reached accurately to touch ”real targets” or reached to the remembered locations of ”virtual targets” (i.e., targets removed at the start of the reach). Subjects made large errors in the virtual-target condition and these errors were analyzed with the aim of revealing the implications for whole-body coordination. Subjects were found to rotate the head less in the virtual-target condition (when compared with accurate movements to real targets). This resulted in a more limited range of head postures, and the final head angles at the end of the movements were geometrically related to the incorrect hand locations, perhaps accounting for some portion of the errors. This suggests that head-eye-hand coordination plays an important role in the organization of these movements and leads to the hypothesis that a representation of current gaze direction may serve as a reference signal for arm motor control. Received: 1 October 1998 / Accepted: 7 January 1999     

Verbal instructions and top-down saccade control

Few studies have addressed the interaction between instruction content and saccadic eye movement control. To assess the impact of instructions on top-down control, we instructed 20 healthy volunteers to deliberately delay saccade triggering, to make inaccurate saccades or to redirect saccades—i.e. to glimpse towards and then immediately opposite to the target. Regular pro- and antisaccade tasks were used for comparison. Bottom-up visual input remained unchanged and was a gap paradigm for all instructions. In the inaccuracy and delay tasks, both latencies and accuracies were detrimentally impaired by either type of instruction and the variability of latency and accuracy was increased. The intersaccadic interval (ISI) required to correct erroneous antisaccades was shorter than the ISI for instructed direction changes in the redirection task. The word-by-word instruction content interferes with top-down saccade control. Top-down control is a time consuming process, which may override bottom-up processing only during a limited time period. It is questionable whether parallel processing is possible in top-down control, since the long ISI for instructed direction changes suggests sequential planning.     

The development of reactive saccade latencies

Saccadic reaction time (SRT) of 4-, 6- and 8-month-old infants' was measured during tracking of abruptly changing trajectories, using a longitudinal design. SRTs decreased from 595 ms (SE=30) at 4 months of age to 442 ms (SE=13) at 8 months of age. In addition, SRTs were lower during high velocities (comparing 4.5 and 9 degrees/s) and vertical (compared to horizontal) saccades.     

Visual-tactile spatial interaction in saccade generation

Saccadic reaction times to visual targets tend to be faster when non-visual stimuli are presented in close temporal or spatial proximity even if subjects are instructed to ignore the accessory input. The effect tends to decrease with increasing spatial distance between the stimuli. Multisensory interaction effects measured in neural structures involved in saccade generation have demonstrated a similar spatial dependence. The present study investigated visual-tactile interaction effects on saccadic reaction time using a focused attention paradigm. Compared to unimodal visual targets saccadic reaction time to bimodal stimuli was reduced by up to 30 ms. The effect was larger for ipsi- than for contralateral presentations, and it increased with the eccentricity of the visual target. The results are consistent with attributing part of the facilitation to a multisensory effect of bimodal neurons with overlapping visual and tactile receptive field structures in the deep layers of the superior colliculus. Electronic Publication     

Identifying sites of saccade amplitude plasticity in humans: transfer of adaptation between different types of saccade

To view different objects of interest, primates use fast, accurate eye movements called saccades. If saccades become inaccurate, the brain adjusts their amplitudes so they again land on target, a process known as saccade adaptation. The different types of saccades elicited in different behavioral circumstances appear to utilize different parts of the oculomotor circuitry. To gain insight into where adaptation occurs in different saccade pathways, we adapted saccades of one type and examined how that adaptation affected or transferred to saccades of a different type. If adaptation of one type of saccade causes a substantial change in the amplitude of another, that adaptation may occur at a site used in the generation of both types of saccade. Alternatively, if adaptation of one type of saccade transfers only partially, or not at all, to another, adaptation occurs at least in part at a location that is not common to the generation of both types of saccade. We produced significant amplitude reductions in memory-guided, delayed, targeting and express saccades by moving the target backward during the saccade. After memory-guided saccades were adapted, the amplitude of express, targeting and delayed saccades exhibited only a partial reduction. In contrast, when express, targeting, or delayed saccades were adapted, amplitude transfer to memory-guided saccades was more substantial. These results, combined with previously published data, suggest that there are at least two sites of adaptation within the saccadic system. One is used communally in the generation of express, targeting, delayed and memory-guided saccades, whereas the other is specific for the generation of memory-guided saccades.