Time course of oculomotor inhibition revealed by saccade trajectory modulation

Selecting a stimulus as the target for a goal-directed movement involves inhibiting other competing possible responses. Both target and distractor stimuli activate populations of neurons in topographic oculomotor maps such as the superior colliculus. Local inhibitory interconnections between these populations ensure only one saccade target is selected. Suppressing saccades to distractors may additionally involve inhibiting corresponding map regions to bias the local competition. Behavioral evidence of these inhibitory processes comes from the effects of distractors on oculomotor and manual trajectories. Individual saccades may initially deviate either toward or away from a distractor, but the source of this variability has not been investigated. Here we investigate the relation between distractor-related deviation of trajectory and saccade latency. Targets were presented with, or without, distractors, and the deviation of saccade trajectories arising from the presence of distractors was measured. A fixation gap paradigm was used to manipulate latency independently of the influence of competing distractors. Shorter- latency saccades deviated toward distractors and longer-latency saccades deviated away from distractors. The transition between deviation toward or away from distractors occurred at a saccade latency of around 200 ms. This shows that the time course of the inhibitory process involved in distractor related suppression is relatively slow.

Spatial and temporal aspects of oculomotor inhibition as revealed by saccade trajectories

The spatial and temporal effect of distractor related inhibition on stimulus elicited (reflexive) and goal driven (voluntary) saccades, was examined using saccade trajectory deviations as a measure. Subjects made voluntary and reflexive saccades to a target location on the vertical midline, while the distance of a distractor from the target was systematically manipulated. The trajectory curvature of both voluntary and reflexive saccades was found to be subject to individual differences. Saccade curvature was found to decrease monotonically with increasing distractor distance from target for some subjects while for others no reduction in curvature or even an increase was found. These results could not be explained by latency differences or landing position effects. The different patterns of distractor effects on saccade trajectories suggest the additional influence of a non-spatial inhibitory mechanism. (c) 2005 Elsevier Ltd. All rights reserved.

The remote distractor effect in saccade programming: channel interactions and lateral inhibition

We explored the dependency of the saccadic remote distractor effect (RDE) on the spatial frequency content of target and distractor Gabor patches. A robust RDE was obtained with low-medium spatial frequency distractors, regardless of the spatial frequency of the tat-get. High spatial frequency distractors interfered to a similar extent when the target was of the same spatial frequency. We developed a quantitative model based on lateral inhibition within an oculomotor decision unit. This lateral inhibition mechanism cannot account for the interaction observed between target and distractor spatial frequency, pointing to the existence of channel interactions at an earlier level. (C) 2004 Elsevier Ltd. All rights reserved.

Evidence that indirect inhibition of saccade initiation improves saccade accuracy

Saccadic eye-movements to a visual target are less accurate if there are distracters close to its location (local distracters). The addition of more distracters, remote from the target location (remote distracters), invokes an involuntary increase in the response latency of the saccade and attenuates the effect of local distracters on accuracy. This may be due to the target and distracters directly competing (direct route) or to the remote distracters acting to impair the ability to disengage from fixation (indirect route). To distinguish between these we examined the development of saccade competition by recording saccade latency and accuracy responses made to a target and local distracter compared with those made with an addition of a remote distracter. The direct route would predict that the remote distracter impacts on the developing competition between target and local distracter, while the indirect route would predict no change as the accuracy benefit here derives from accessing the same competitive process but at a later stage. We found that the presence of the remote distracter did not change the pattern of accuracy improvement. This suggests that the remote distracter was acting along an indirect route that inhibits disengagement from fixation, slows saccade initiation, and enables more accurate saccades to be made.

Driving saccade to pursuit using image motion

Within the context of active vision, scant attention has been paid to the execution of motion saccades—rapid re-adjustments of the direction of gaze to attend to moving objects. In this paper we first develop a methodology for, and give real-time demonstrations of, the use of motion detection and segmentation processes to initiate capture saccades towards a moving object. The saccade is driven by both position and velocity of the moving target under the assumption of constant target velocity, using prediction to overcome the delay introduced by visual processing. We next demonstrate the use of a first order approximation to the segmented motion field to compute bounds on the time-to-contact in the presence of looming motion. If the bound falls below a safe limit, a panic saccade is fired, moving the camera away from the approaching object. We then describe the use of image motion to realize smooth pursuit, tracking using velocity information alone, where the camera is moved so as to null a single constant image motion fitted within a central image region. Finally, we glue together capture saccades with smooth pursuit, thus effecting changes in both what is being attended to and how it is being attended to. To couple the different visual activities of waiting, saccading, pursuing and panicking, we use a finite state machine which provides inherent robustness outside of visual processing and provides a means of making repeated exploration. We demonstrate in repeated trials that the transition from saccadic motion to tracking is more likely to succeed using position and velocity control, than when using position alone.

ERP correlates of shared control mechanisms involved in saccade preparation and in covert attention

We investigated whether attention shifts and eye movement preparation are mediated by shared control mechanisms, as claimed by the premotor theory of attention. ERPs were recorded in three tasks where directional cues presented at the beginning of each trial instructed participants to direct their attention to the cued side without eye movements (Covert task), to prepare an eye movement in the cued direction without attention shifts (Saccade task) or both (Combined task). A peripheral visual Go/Nogo stimulus that was presented 800 ms after cue onset signalled whether responses had to be executed or withheld. Lateralised ERP components triggered during the cue–target interval, which are assumed to reflect preparatory control mechanisms that mediate attentional orienting, were very similar across tasks. They were also present in the Saccade task, which was designed to discourage any concomitant covert attention shifts. These results support the hypothesis that saccade preparation and attentional orienting are implemented by common control structures. There were however systematic differences in the impact of eye movement programming and covert attention on ERPs triggered in response to visual stimuli at cued versus uncued locations. It is concluded that, although the preparatory processes underlying saccade programming and covert attentional orienting may be based on common mechanisms, they nevertheless differ in their spatially specific effects on visual information processing.

Manual response preparation and saccade programming are linked to attention shifts: ERP evidence for covert attentional orienting and spatially specific modulations of visual processing

The premotor theory of attention claims that attentional shifts are triggered during response programming, regardless of which response modality is involved. To investigate this claim, event-related brain potentials (ERPs) were recorded while participants covertly prepared a left or right response, as indicated by a precue presented at the beginning of each trial. Cues signalled a left or right eye movement in the saccade task, and a left or right manual response in the manual task. The cued response had to be executed or withheld following the presentation of a Go/Nogo stimulus. Although there were systematic differences between ERPs triggered during covert manual and saccade preparation, lateralised ERP components sensitive to the direction of a cued response were very similar for both tasks, and also similar to the components previously found during cued shifts of endogenous spatial attention. This is consistent with the claim that the control of attention and of covert response preparation are closely linked. N1 components triggered by task-irrelevant visual probes presented during the covert response preparation interval were enhanced when these probes were presented close to cued response hand in the manual task, and at the saccade target location in the saccade task. This demonstrates that both manual and saccade preparation result in spatially specific modulations of visual processing, in line with the predictions of the premotor theory.

The spatial impact of visual distractors on saccade latency

Remote transient changes in the environment, such as the onset of visual distractors, impact on the exe- cution of target directed saccadic eye movements. Studies that have examined the latency of the saccade response have shown conflicting results. When there was an element of target selection, saccade latency increased as the distance between distractor and target increased. In contrast, when target selection is minimized by restricting the target to appear on one axis position, latency has been found to be slowest when the distractor is shown at fixation and reduces as it moves away from this position, rather than from the target. Here we report four experiments examining saccade latency as target and distractor posi- tions are varied. We find support for both a dependence of saccade latency on distractor distance from target and from fixation: saccade latency was longer when distractor is shown close to fixation and even longer still when shown in an opposite location (180°) to the target. We suggest that this is due to inhib- itory interactions between the distractor, fixation and the target interfering with fixation disengagement and target selection.

The influence of distractors on saccade­ target selection: saccade trajectory effects

It has long been known that the path (trajectory) taken by the eye to land on a target is rarely straight (Yarbus, 1967). Furthermore, the magnitude and direction of this natural tendency for curvature can be modulated by the presence of a competing distractor stimu­ lus presented along with the saccade target. The distractor­related modulation of saccade trajectories provides a subtle measure of the underlying competitive processes involved in saccade target selection. Here we review some of our own studies into the effects distract­ ors have on saccade trajectories, which can be regarded as a way of probing the competit­ ive balance between target and distractor salience.

Bilateral impairment of concurrent saccade programming in hemispatial neglect

When healthy observers make a saccade that is erroneously directed toward a distracter stimulus, they often produce a corrective saccade within 100ms after the end of the primary saccade. Such short inter-saccadic intervals indicate that programming of the secondary saccade has been initiated prior to the execution of the primary saccade and hence that the two saccades have been programmed concurrently. Here we show that concurrent saccade programming is bilaterally impaired in left spatial neglect, a strongly lateralized disorder of visual attention resulting from extensive right cerebral damage. Neglect patients were asked to make saccades to targets presented left or right of fixation while disregarding a distracter presented in the opposite hemifield. We examined those experimental trials on which participants first made a saccade to the distracter, followed by a secondary (corrective) saccade to the target. Compared to healthy and right-hemisphere damaged control participants the proportion of secondary saccades directing gaze to the target instead of bringing it even closer to the distracter was bilaterally reduced in neglect patients. In addition, the characteristic reduction of secondary saccade latency observed in both control groups was absent in neglect patients, whether the secondary saccade was directed to the left or right hemifield. This pattern is consistent with a severe, bilateral impairment of concurrent saccade programming in left spatial neglect.

One-Hertz transcranial magnetic stimulation over the frontal eye field induces lasting inhibition of saccade triggering

The aim of the study was to examine the effect of low-frequency repetitive transcranial magnetic stimulation on saccade triggering. In five participants, a train of 600 pulses with a frequency of 1 Hz was applied over the right frontal eye field and--as control condition--over the vertex. After repetitive transcranial magnetic stimulation application, oculomotor performance was evaluated with an overlap paradigm. The results show that the repetitive transcranial magnetic stimulation effect was specific for frontal eye field stimulation. Saccade latencies were found to be increased bilaterally for several minutes after the stimulation, and the time course of recovery was different for the ipsilateral and contralateral sides. The results are discussed in the light of possible local and remote repetitive transcranial magnetic stimulation effects on the oculomotor network.

Inhibitory control of the human dorsolateral prefrontal cortex during the anti-saccade paradigm--a transcranial magnetic stimulation study

In the anti-saccade paradigm, subjects are instructed not to make a reflexive saccade to an appearing lateral target but to make an intentional saccade to the opposite side instead. The inhibition of reflexive saccade triggering is under the control of the dorsolateral prefrontal cortex (DLPFC). The critical time interval at which this inhibition takes place during the paradigm, however, is not exactly known. In the present study, we used single-pulse transcranial magnetic stimulation (TMS) to interfere with DLPFC function in 15 healthy subjects. TMS was applied over the right DLPFC either 100 ms before the onset of the visual target (i.e. -100 ms), at target onset (i.e. 0 ms) or 100 ms after target onset (i.e. +100 ms). Stimulation 100 ms before target onset significantly increased the percentage of anti-saccade errors to both sides, while stimulation at, or after, target onset had no significant effect. All three stimulation conditions had no significant influence on saccade latency of correct or erroneous anti-saccades. These findings show that the critical time interval at which the DLPFC controls the suppression of a reflexive saccade in the anti-saccade paradigm is before target onset. In addition, the results suggest the view that the triggering of correct anti-saccades is not under direct control of the DLPFC.

The role of the human posterior parietal cortex in memory-guided saccade execution: a double-pulse transcranial magnetic stimulation study

The present study investigated the role of the right posterior parietal cortex (PPC) in the triggering of memory-guided saccades by means of double-pulse transcranial magnetic stimulation (dTMS). Shortly before saccade onset, dTMS with different interstimulus intervals (ISI; 35, 50, 65 or 80 ms) was applied. For contralateral saccades, dTMS significantly decreased saccadic latency with an ISI of 80 ms and increased saccadic gain with an ISI of 65 and 80 ms. Together with the findings of a previous study during frontal eye field (FEF) stimulation the present results demonstrate similarities and differences between both regions in the execution of memory-guided saccades. Firstly, dTMS facilitates saccade triggering in both regions, but the timing is different. Secondly, dTMS over the PPC provokes a hypermetria of contralateral memory-guided saccades that was not observed during FEF stimulation. The results are discussed within the context of recent neurophysiological findings in monkeys.