Response selection in prosaccades, antisaccades, and other volitional saccades

Saccades made to the opposite side of a visual stimulus (antisaccades) and to central cues (simple volitional saccades) both require active response selection but whether the mechanisms of response selection differ between these tasks is unclear. Response selection can be assessed by increasing the number of response alternatives: this leads to increased reaction times when response selection is more demanding. We compared the reaction times of prosaccades, antisaccades, saccades cued by a central arrow, and saccades cued by a central number, in blocks of either two or six possible responses. In the two-response blocks, reaction times were fastest for prosaccades and antisaccades, and slowest for arrow-cued and number-cued saccades. Increasing response alternatives from two to six caused a paradoxical reduction in reaction times of prosaccades, had no effect on arrow-cued saccades, and led to a large increase in reaction times of number-cued saccades. For antisaccade reaction times, the effect of increasing response alternatives was intermediate, greater than that for arrow-cued saccades but less than that for number-cued saccades. We suggest that this pattern of results may reflect two components of saccadic processing: (a) response triggering, which is more rapid with a peripheral stimulus as in the prosaccade and antisaccade tasks and (b) response selection, which is more demanding for the antisaccade and number-cued saccade tasks, and more automatic when there is direct stimulus–response mapping as with prosaccades, or over-learned symbols as with arrow-cued saccades.     

Prosaccades and antisaccades to onsets and color singletons: evidence that erroneous prosaccades are not reflexive

In the present study participants searched for an onset target or a color singleton target and were required to execute a saccade toward (prosaccade) or away (antisaccade) from the search target. The results showed that participants often made erroneous saccades toward the onset or color singleton when they were the search target in the antisaccade condition, but not when they were presented as task-irrelevant distractors. This suggests that task-relevance plays a critical role in the production of erroneous prosaccades and provides evidence that these saccades are not completely reflexive. Furthermore, it was found that the antisaccade cost (latency difference between prosaccades and antisaccades) was greater for color singleton search targets than for onset search targets. The present findings have implications for our understanding of the processes involved in the programming of antisaccades and the causes of erroneous prosaccades.     

The inter-trial effects of stimulus and saccadic direction on prosaccades and antisaccades, in controls and schizophrenia patients

We investigated the influence of the direction of preceding saccadic trials on the latency of current prosaccades and antisaccades, in healthy subjects and patients with schizophrenia. When prosaccades and antisaccades were performed in separate, single-task blocks, we found that only prosaccades were delayed if the saccade in the prior trial was in the same direction, consistent with the expected directional effect from an ‘inhibition of return’-like alternation advantage. However, both types of saccades were executed more quickly when the saccade in the penultimate trial was in the same direction, consistent with previous demonstrations of directional plasticity in monkeys. In blocks of randomly mixed prosaccades and antisaccades, the directional effects in healthy subjects were greatest when a prosaccade was preceded by an antisaccade, consistent with a summation of effects of alternation advantage (from the prior stimulus) and directional plasticity (from the prior saccade). Schizophrenic patients showed an additional phenomenon, a directionally specific inhibition of upcoming saccades by preceding antisaccades. These results suggest that saccades in humans are modulated by inter-trial effects attributable to both an ‘inhibition of return’-like alternation advantage and directional plasticity.     

Effects of switching between leftward and rightward pro- and antisaccades

Previous studies suggested that random switching between pro- and antisaccades increases errors in both tasks. However, little is known about the effects of switching between leftward and rightward saccades (response switching). The present study investigated task and response switching using an alternating runs procedure. Tasks (i.e., prosaccades versus antisaccades) were switched every second trial. Response switches (i.e., leftward saccades versus rightward saccades) were counterbalanced across tasks and task-switching conditions. Task switching increased errors in both tasks. Response switching increased errors when antisaccades were preceded by antisaccades but not when antisaccades were preceded by prosaccades or for prosaccades regardless of the preceding saccade type. The task-switch effects suggest that both pro- and antisaccade trials activate specific production rules that can persist in a subsequent trial. The differential response-switch effects may reflect different modes of response activation in pro- and antisaccades (sensorimotor transformation of visual information versus selection of motor programs).     

Abnormal mechanisms of antisaccade generation in schizophrenia patients and unaffected biological relatives of schizophrenia patients

Although errant saccadic eye movements may mark genetic factors in schizophrenia, little is known about abnormal brain activity that precedes saccades in individuals with genetic liability for schizophrenia. We investigated electrophysiological activity preceding prosaccades and antisaccades in schizophrenia patients, first‐degree biological relatives of schizophrenia patients, and control subjects. Prior to antisaccades, patients had reduced potentials over lateral prefrontal cortex. Smaller potentials were associated with worse antisaccade performance. Relatives also exhibited reduced pre‐saccadic potentials over lateral frontal cortex but additionally had reduced potentials over parietal cortex. Both patients and relatives tended toward increased activity over orbital frontal cortex prior to saccades. Results are consistent with lateral prefrontal dysfunction marking genetic liability for schizophrenia and underlying deficient saccadic control.     

The relationship of saccadic peak velocity to latency: evidence for a new prosaccadic abnormality in schizophrenia

Antisaccades have not only longer latencies but also lower peak velocities than prosaccades. It is not known whether these latency and velocity differences are related. Studies of non-human primates suggest that prosaccade peak velocity declines as latency from target appearance increases. We examined whether a similar relationship between peak velocity and latency existed in human saccades, whether it accounted for the difference in peak velocity between antisaccades and prosaccades, and whether it was affected by schizophrenia, a condition that affects antisaccade performance. Sixteen control and 21 schizophrenia subjects performed prosaccade and antisaccade trials in the same test session. In both groups antisaccades had lower peak velocities than prosaccades. Latency did not influence the peak velocities of antisaccades in either subject group. At short latencies, the peak velocities of prosaccades were also similar in the two groups. However, while prosaccade peak velocities declined minimally with increasing latency in control subjects, those in the schizophrenia group declined significantly until they reached a value similar to antisaccade peak velocities. We conclude that, in normal subjects, the effect of latency on prosaccade peak velocity is minimal and cannot account for the lower velocity of antisaccades. In schizophrenia, we hypothesize that the latency-related decline in prosaccade peak velocity may reflect either an increased rate of decay of the effect of the transient visual signal at the saccadic goal, or a failure of the continuing presence of the target to sustain neural activity in the saccadic system.     

Switching, plasticity, and prediction in a saccadic task-switch paradigm

Several cognitive processes are involved in task-switching. Using a prosaccade/antisaccade paradigm, we manipulated both the interval available for preparation between the cue and the target and the predictability of trial sequences, to isolate the contributions of foreknowledge, an active switching (reconfiguration) process, and passive inhibitory effects persisting from the prior trial. We tested 15 subjects with both a random and a regularly alternating trial sequence. Half of the trials had a short cue–target interval of 200 ms, and half a longer cue–target interval of 2,000 ms. When there was only a short preparatory interval, switching increased the latencies for both prosaccades and antisaccades. With a long preparatory interval, switching was associated with a smaller latency increase for prosaccades and, importantly, a paradoxical reduction in latency for antisaccades. Foreknowledge of a predictable sequence did not allow subjects to reduce switch costs in the manner that a long preparatory cue–target interval did. In the trials with short preparatory intervals, the effects on latency attributable to active reconfiguration processes were similar for prosaccades and antisaccades. We propose a model in which the passive inhibitory effects that persist from the prior saccadic trial are due not to task-set inertia, in which one task-set inhibits the opposite task-set, but to inhibition of the saccadic response-system by the antisaccade task, to account for the paradoxical set-switch benefit for antisaccades at long cue–target intervals. Our findings regarding foreknowledge show that previous studies used to support task-set inertia may have conflated the effects of both active reconfiguration and passive inhibitory processes on latency. While our model of response-system plasticity can explain a number of effects of dominance asymmetry in switching, other models fail to account for the paradoxical set-switch benefit for antisaccades.     

Antisaccades and task-switching: interactions in controlled processing

Smaller latency costs for switching from dominant (habitual) to non-dominant (unusual) tasks compared to the reverse direction have been noted in some studies of task-switching. This asymmetry has been cited as evidence of inhibitory effects from the prior trial. We examined accuracy and latency costs of task-switching between prosaccades and antisaccades, where task-switching is limited to stimulus-response re-mapping and occurs between tasks highly asymmetric in dominance. Eighteen subjects executed prosaccades and antisaccades in single-task and mixed-task blocks. In mixed-task blocks, antisaccade and prosaccade trials were ordered randomly, resulting in 'repeated' trials that were preceded by the same type of trial (i.e. antisaccade-antisaccade), and 'switched' trials that were preceded by the opposite type of trial. Comparisons of the single-task blocks and repeated trials of the mixed-task blocks indexed the mixed-list costs, which were small for prosaccades and insignificant for antisaccades. Comparison of the repeated and switched trials from the mixed-task blocks indexed the residual task-switch cost. Accuracy costs of task-switching and antisaccades were equivalent. The accuracy of trials incorporating both switching and antisaccades in a single response (i.e. switched antisaccade) equalled the product of the accuracies of doing each operation alone, supporting independence of these two functions. In contrast, the latency cost of antisaccade performance was 3 times greater than that of task-switching. Task-switching from prosaccades to antisaccades resulted in a paradoxical decrease in antisaccade latency. This decrease correlated with other indices of vigilance, with the paradoxical effect minimized in more attentive observers. The latency data suggest that either an antisaccade on the prior trial perturbs saccadic responses more than a task-switch, or concurrent task-switching specifically facilitates antisaccades. In either case, the paradoxical benefit of task-switching for antisaccades challenges current models of task-switching.     

Task-switching with antisaccades versus no-go trials: a comparison of inter-trial effects

Antisaccades involve the suppression of a pre-potent prosaccade and a vector inversion to generate the novel ocular motor response of looking away from the target. Antisaccades have also been found to prolong the latencies of saccades in upcoming trials, an effect that we attribute to a form of immediate plasticity in the ocular motor system. Our goal was to determine whether the inter-trial effects of antisaccades were similar to that of no-go trials, where subjects must suppress making a saccade when the target appears without substituting a novel ocular motor response. We tested 12 subjects with two different blocks of saccadic trials. In one, prosaccades randomly alternated with antisaccades. In the other, prosaccades alternated with no-go trials. We analyzed the error rates and latencies of prosaccades that followed antisaccades versus no-go trials, compared to repeated prosaccades, to determine if inter-trial effects were present for both types of responses that required prosaccade suppression. No-go responses increased the error rates of prosaccades in the following trial less than antisaccades did. However, no-go trials had the same effect on the latencies of upcoming prosaccades as antisaccades. The inhibitory effect that prolongs the latencies of prosaccades after antisaccades likely stems from the need to inhibit a prosaccade, a function that is also required in no-go trials. The greater impairment of prosaccade accuracy after an antisaccade may reflect either additional control mechanisms involved in vector inversion or a different form of inhibitory control that operates during antisaccades and not during no-go responses.     

Effects of aging on switching the response direction of pro- and antisaccades

The present study investigated effects of task switching between pro- and antisaccades and switching the direction of these saccades (response switching) on performance of younger and older adults. Participants performed single-task blocks, in which only pro- or only antisaccades had to be made as well as mixed-task blocks, in which pro- and antisaccades were required. Analysis of specific task switch effects in the mixed-task blocks showed switch costs for error rates for prosaccades for both groups, suggesting that antisaccade task rules persisted and affected the following prosaccade. The comparison between single- and mixed-task blocks showed that mixing costs were either equal or smaller for older than younger participants, indicating that the older participants were well able to keep task sets in working memory. The most prominent age difference that was observed for response switching was that for the older but not younger group task switching and response switching interacted, resulting in less errors when two consecutive antisaccades were made in the same direction. This finding is best explained with a facilitation of these consecutive antisaccades. The present study clearly demonstrated the impact of response switching and a difference between age groups, underlining the importance of considering this factor when investigating pro- and antisaccades, especially antisaccades, and when investigating task switching and aging.     

The relation between antisaccade errors,fixation stability and prosaccade errors in schizophrenia

Whether antisaccade errors in schizophrenia are due to defects in implementing saccadic inhibition or difficulty in generating novel responses is uncertain. We investigated whether antisaccade errors were related to difficulty in inhibiting saccades when subjects were asked to maintain steady fixation, a situation that does not require a novel response. We examined the ocular motor data of 15 schizophrenia subjects and 16 healthy subjects. We assessed fixation in two situations: first, during the period before target onset during each saccadic trial, and second, during fixation trials that were interspersed with saccadic trials. We found that schizophrenia subjects had higher rates of fixation losses than control subjects in both situations. Second, both in healthy and schizophrenia subjects, antisaccade error rate was positively correlated with the frequency of fixation losses in the preparatory period of saccadic trials, but not with the frequency of fixation losses during fixation trials. Third, antisaccade errors were more likely to occur in trials with unstable fixation than in trials with stable fixation. Last, antisaccade error rate was also correlated with prosaccade error rate. We conclude that antisaccade errors are related to difficulties with implementing inhibitory control in the saccadic system. However, the finding of a correlation between the error rates for antisaccades and prosaccades suggests that this is not specifically concerned with inhibiting the automatic prosaccade, but a more general deficit in implementing goal-oriented behavior.     

Event-related potentials associated with correct and incorrect responses in a cued antisaccade task

In an antisaccade task, subjects are instructed to inhibit a reflexive saccade towards a peripheral stimulus flash and to generate a saccade in the opposite direction. It has been shown recently that normal subjects will generate a high number of incorrect prosaccades in an antisaccade task if the fixation point is extinguished 200 ms before the stimulus appears and if a valid cue for the subsequent antisaccade is given during this gap period. In the present study we recorded cerebral event-related potentials from 19 scalp electrodes from normal subjects prior to correct and incorrect responses in a cued antisaccade task to investigate the neural processes associated with correct antisaccades and incorrect prosaccades in this task. Correct antisaccades and incorrect prosaccades were associated with a negative potential with a maximal amplitude around stimulus onset over the dorsomedial frontal cortex. This potential was higher prior to correct antisaccades than prior to incorrect prosaccades. The execution of a correct antisaccade was preceded by a shift of a negative potential from the parietal hemisphere contralateral to the visual stimulus towards the parietal hemisphere ipsilateral to the stimulus. These results support the view that the supplementary eye fields participate in the inhibition of incorrect saccades in a cued antisaccade task and show that the parietal cortex participates in generating a neural representation of the visual stimulus in the hemifield ipsilateral to the stimulus before generating a motor response. Received: 20 December 1996 / Accepted: 18 June 1997     

Development of prosaccade and antisaccade task performance in participants aged 6 to 26 years

There are few studies on the development of oculomotor functions during childhood. B. Fischer, M. Biscaldi, and S. Gezeck (1997) reported improvement of antisaccade task performance between ages 6 and 16 years. The present study is a replication and extension of those results. In three age groups (6-7, 10-11, 18-26 years), saccades during pro- and antisaccade tasks with 200-ms gap and overlap and during a fixation task were measured. Adults exhibited faster saccades and less prosaccades during the antisaccade tasks than 10-11-year-old children; these two groups had faster saccades during all tasks and less prosaccades during the anti- and the fixation task than 6-7-year-old subjects. Both children groups made more express saccades than adults. Results suggest different degrees of age-related improvement for different saccadic parameters, the effects being greatest for prosaccade inhibition during the antisaccade task and in line with the assumed protracted development of prefrontal functions.     

Effects of procues on error rate and reaction times of antisaccades in human subjects

In a gap paradigm, where the saccadic reaction times are usually short, the number of express saccades can be further increased and their latency decreased when a valid transient peripheral cue is given 100 ms before target occurrence. In the present study we measured the saccadic reaction times of seven human subjects who had been instructed to make antisaccades (saccades to the side opposite to stimulus presentation) in the gap paradigm. In the first experiment, we presented a 100% valid cue with 100 ms cue lead time. To explore whether the cue reduced the reaction times of the antisaccades, the cue was always presented on the opposite side to where the stimulus occurred (stimulus direction was randomized between 4° to the left and right), and it was thus indicated in each trial to which side the antisaccade was required (procue). In the second set of experiments the cue was consistently presented on either the left or the right side in two different blocks; it was thus noninformative with respect to the direction of the antisaccade. In the first experiment, a significant increase in mean reaction times of correct antisaccades and a considerable increase in erratic prosaccades to the stimulus were obtained compared with a control session with no cue. In the two experimental blocks with noninformative cues, the reaction times of correct antisaccades were decreased when cue and stimulus were on at the same side, while large numbers of erratic prosaccades were again obtained when cue and stimulus were presented on opposite sides. These results suggest that the orienting mechanism elicited by a transient peripheral cue relates to the command and to the decision to make a proversus an antisaccade. Since the subjects reported that they could not prevent, or, moreover, in some cases did not even realize that they were making erratic prosaccades, we conclude that this orienting mechanism occurs automatically, being largely beyond voluntary control.     

Less attention is more in the preparation of antisaccades, but not prosaccades

To make a saccadic eye movement to a target we must first attend to it. It is therefore not surprising that diverting attention increases saccade latency, but is latency increased in all cases? We show that attending to a peripheral discrimination task has a paradoxical effect. If the stimulus to be attended appears shortly (100 to 300 ms) before an eye movement is made in a direction opposite to that of a presented stimulus (an antisaccade), its latency is reduced to well below baseline performance. In contrast, latencies for saccades toward the stimulus (prosaccades) are increased under similar conditions. This paradoxical effect may arise from competition between the processes mediating prosaccades and antisaccades. When the discrimination task is presented at the critical moment, it interferes with a reflexive prosaccade, allowing faster antisaccades. The results suggest that the suppression of sensorimotor reflexes can facilitate volitional motor acts.     

The global effect for antisaccades

In the global effect, prosaccades are deviated to a position intermediate between two targets or between a distractor and a target, which may reflect spatial averaging in a map encoded by the superior colliculus. Antisaccades differ from prosaccades in that they dissociate the locations of the stimulus and goal and generate weaker collicular activity. We used these antisaccade properties to determine whether the global effect was generated in stimulus or goal computations, and whether the global effect would be larger for antisaccades, as predicted by collicular averaging. In the first two experiments, human subjects performed antisaccades while distractors were placed in the vicinity of either the stimulus or the saccadic goal. Global effects occurred only for goal-related and not for stimulus-related distractors, indicating that this effect emerges from interactions with motor representations. In the last experiment, subjects performed prosaccades and antisaccades with and without goal-related distractors. When the results were adjusted for differences in response latency, the global effect for rapid responses was three to four times larger for antisaccades than for prosaccades. Finally, we compared our findings with predictions from collicular models, to quantitatively test the spatial averaging hypothesis: we found that our results were consistent with the predictions of a collicular model. We conclude that the antisaccade global effect shows properties compatible with spatial averaging in collicular maps and likely originates in layers with neural activity related to goal rather than stimulus representations.     

Is the relationship of prosaccade reaction times and antisaccade errors mediated by working memory?

The mechanisms that control eye movements in the antisaccade task are not fully understood. One influential theory claims that the generation of antisaccades is dependent on the capacity of working memory. Previous research also suggests that antisaccades are influenced by the relative processing speeds of the exogenous and endogenous saccadic pathways. However, the relationship between these factors is unclear, in particular whether or not the effect of the relative speed of the pro and antisaccade pathways is mediated by working memory. The present study contrasted the performance of healthy individuals with high and low working memory in the antisaccade and prosaccade tasks. Path analyses revealed that antisaccade errors were strongly predicted by the mean reaction times of prosaccades and that this relationship was not mediated by differences in working memory. These data suggest that antisaccade errors are directly related to the speed of saccadic programming. These findings are discussed in terms of a race competition model of antisaccade control.     

Abnormalities of internally generated saccades in obsessive-compulsive disorder

BACKGROUND: We aimed to utilize tests of saccadic function to investigate whether cognitive abnormalities in obsessive-compulsive disorder (OCD) arise from a dysfunction of inhibitory processes or whether they reflect a more general difficulty in guiding behaviour on the basis of an internal representation of task goal. METHODS: Twelve patients with OCD and 12 matched controls performed a visually-guided saccade task, a volitional prosaccade task and an antisaccade task. The latency and gain of saccades was compared between groups for the three saccade tasks. The number of antisaccade errors was also calculated and compared between groups. RESULTS: There was no difference for antisaccade error rates between the groups. The latency of visually guided saccades did not differ between groups, however the latency of both volitional prosaccades and antisaccades was significantly slower in the patients with OCD than in controls. The difference in latency between volitional prosacades and antisaccades, however, was equal between groups. CONCLUSIONS: These results suggest that patients with OCD have an abnormality in guiding behaviour on the basis of an internal representation of the task goal, rather than a problem with inhibiting reflexive behaviour.     

Microstimulation of monkey dorsolateral prefrontal cortex impairs antisaccade performance

The dorsolateral prefrontal cortex (DLPFC) has been implicated in various cognitive functions, including response suppression. This function is frequently probed with the antisaccade task, which requires suppression of the automatic tendency to look toward a flashed peripheral stimulus (prosaccade), and instead generate a voluntary saccade to the mirror location. To test whether activity in the DLPFC is causally linked to antisaccade performance, we applied electrical microstimulation to sites in the DLPFC of two monkeys, while they performed randomly interleaved pro- and antisaccade trials. Microstimulation resulted in significantly longer saccadic reaction times for ipsilaterally directed prosaccades and antisaccades, and increased the error rate on ipsilateral antisaccade trials. These findings provide causal evidence that activity in the DLPFC influences saccadic eye movements.     

Event-related potentials before saccades and antisaccades and their relation to reaction time

In the present study, reaction time (RT) was measured in 12 healthy subjects in a saccade and antisaccade task while recording electroencephalographic activity (EEG) from 62 electrodes on the scalp. Event-related potentials averaged both on target appearance and on saccade onset were larger in amplitude (increased negativity) for the antisaccade task compared to the saccade task. The relation of RT variability to EEG amplitude was studied by averaging stimulus-aligned and movement-aligned individual trials for each subject into four RT quartile groups. The analysis showed a relation of EEG amplitude to RT for both saccades and antisaccades. More specifically, the ERP negativity at 100–120 ms after stimulus onset in the saccade task and at 160–200 ms after stimulus onset in the antisaccade task for stimulus-aligned ERPs decreased monotonically with increasing RT as would be expected if this signal would be related to the eye movement preparation processes. This was much more pronounced and wide spread for the antisaccades than for visually triggered saccades. The peak negativity before movement onset for movement-aligned ERPs also covaried with RT suggesting no relation of this activity to movement preparation processes. This study then confirmed that only a particular ERP signal variation was related to the saccadic eye movement preparatory processes while other components of the ERP have no specific relation to the movement preparation. This particular signal was more prominent for antisaccades compared to visually triggered saccades supporting previous evidence for the cortical involvement in the preparation of these voluntary eye movements. In conclusion, this study validates the use of ERPs in the study of the planning and execution of saccadic eye movements.