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.     

Human express saccades: extremely short reaction times of goal directed eye movements

Summary Human subjects were asked to execute a saccade from a central fixation point to a peripheral target at the time of its onset. When the fixation point is turned off some time ( 200 ms) before target onset, such that there is a gap where subjects see nothing, the distribution of their saccadic reaction times is bimodal with one narrow peak around 100 ms (express saccades) and another peak around 150 ms (regular saccades) measured from the onset of the target. Express saccades have been described earlier for the monkey.     

Separate populations of visually guided saccades in humans: reaction times and amplitudes

Summary The saccadic eye movements of 20 naive adults, 7 naive teenagers, 12 naive children, and 4 trained adult subjects were measured using two single target saccade tasks; the gap and the overlap task. In the gap task, the fixation point was switched off before the target occurred; in the overlap task it remained on until the end of each trial. The target position was randomly selected 4° to the left or 4° to the right of the fixation point. The subjects were instructed to look at the target when it appeared, not to react as fast as possible. They were not given any feedback about their performance. The results suggest that, in the gap task, most of the naive subjects exhibit at least two (the teenagers certainly three) clearly separated peaks in the distribution of the saccadic reaction times. The first peak occurs between 100 and 135 ms (express saccades), the second one between 140 and 180 ms (fast regular), and a third peak may follow at about 200 ms (slow regular). Other subjects did not show clear signs of two modes in the range of 100 to 180 ms, and still others did not produce any reaction times below 135 ms. In the overlap task as well three or even more peaks were obtained at about the same positions along the reaction time scale of many, but not all subjects. Group data as well as those of individual subjects were fitted by the superposition of three gaussian functions. Segregating the reaction time data into saccades that over- or undershoot the target indicated that express saccades almost never overshoot. The results are discussed in relation to the different neural processes preceding the initiation of visually-guided saccades.     

Fixation and saccade control in an express-saccade maker

In express-saccade makers a large incidence of express saccades (latencies around 100 ms) is paralleled by a reduced ability to suppress saccade generation when required. Such a behavior occurs frequently in dyslexies. We studied the latencies and the metrical properties of saccades in the very rare case of an adult, nondyslexic express-saccade maker (male, age 29 years). The subject produced 65–95% express saccades in the gap (fixation point removed 200 ms before target onset) as well as in the overlap (fixation point not removed) paradigm, which qualified the subject as the most clear case of an express-saccade maker found so far. The number of express saccades increased rather than decreased when fixation foreperiod, gap duration, and target location were randomized from trial to trial as compared to when they remained constant. In the memory-guided saccade and in the antisaccade paradigms in which immediate saccade execution to a visual target had to be suppressed, the subject often reacted to the target with express saccades in an involuntary way. The amplitudes of express saccades were — in some conditions — found to progressively decrease with increasing latency, giving rise to amplitude transition functions. The present findings disprove the notion that express saccades are generated based on the prediction of the time and location of target appearance and support the notion that they are the result of an optomotor reflex. It is argued that the operation of the reflex is gated by a separate fixation system. Express-saccade makers are described as subjects with a dysfunction of the fixation system. Recent neurophysiological findings suggest that the subject studied in the present study has a selective dysfunction of the fixation system at the level of the superior colliculus.     

Relationship between directed visual attention and saccadic reaction times

Summary Saslow (1967) and Fischer and Ramsperger (1984) found that saccadic reaction time (SRT) depends on the interval between the fixation point offset and the target onset. Using a continuously visible fixation point, we asked whether a similar function would be obtained if subjects attended to a peripherally viewed point extinguished at variable intervals before or after the target onset. The interval was varied between -500ms (i.e., attention stimulus offset after saccade target onset = overlap trials) and 500ms (i.e., attention stimulus offset before saccade target onset = gap trials). The results show a constant mean SRT of about 240 ms for overlap trials, and a U-shaped function with a minimum of 140 ms, at a gap duration of 200 ms, for gap trials. These findings suggest that saccadic latencies do not depend on the cessation of fixation per se, but rather on the disengagement of attention from any location in the visual field. The time required for subjects to disengage their attention is approximately 100 ms. This disengaged state of attention — during which short latency (express) saccades can be made — can be sustained only for a gap duration of 300 ms. At longer gap durations mean SRTs increase again.     

Reaction times of the eye and the hand of the monkey in a visual reach task

Two monkeys were trained to execute saccadic eye movements and reach movements with the hand from a central fixation point to a peripheral target. Reaction times for both movements were compared on a trial-by-trial basis. If the fixation point was extinguished before the target appeared (gap condition), extremely short latency saccades (85 ms) (express saccades) were obtained, that were followed by short latency reach movements (250 ms), but there was no correlation between them on a trial-by-trial basis. If the fixation point remained visible (overlap condition), very short (100 ms) and rather long (220 ms) latency saccades were observed. Long saccadic latencies correlated strongly with the reach reaction times. Short latency saccades were followed by reach movements of reaction times longer than those observed after express saccades in the gap condition; there was no correlation between them. All reaction times varied systematically with practice.     

Dead zone for express saccades

Summary The saccadic eye movements of three humans and one non-human primate (a male rhesus monkey) have been measured for target eccentricities between 0.3 and 15 deg. With a gap task (fixation point offset precedes target onset by 200 ms) and a target at 4 deg, all subjects produced reasonable amounts of express saccades as indicated by a clear peak in the distribution of their saccadic reaction times (SRT): about 100 ms in human subjects and 70 ms in the monkey. This peak disappeared with decreasing target eccentricity below 2 deg, but saccades of longer (regular) reaction times were still present. Thus it was found that there exists a dead zone for express saccades. In addition, small saccades have a much stronger tendency to overshoot the target and their velocity falls above the main sequence as defined by the least square fit of an exponential v=vo(1-exp(-a/ao)) to the maximal velocity (v) versus amplitude (a) relationship (vo and ao are constants fitted). It is concluded that for small saccades the express way is blocked functionally or does not exist anatomically.     

Effects of pre-cues on voluntary and reflexive saccade generation I. Anti-cues for pro-saccades

Experiments on visual attention have employed both physical cues and verbal instructions to enable subjects to allocate attention at a location that becomes relevant within a perceptual or motor task some time later (cue lead time, CLT). In this study we have used valid visual peripheral cues (CLT between 100 and 700 ms) to indicate the direction and location of the next saccade. A cue is considered valid or invalid if its meaning with respect to the next saccade is correct or incorrect. A cue is called an anti- or pro-cue if the side of its presentation is opposite to or the same as the direction of the saccade required on a given trial. Correspondingly, a saccade is called an anti- or pro-saccade if it is directed to the side opposite to or the same as the stimulus presentation. A condition in which the cue and the stimulus are presented on opposite sides provides a simple way of dissociating voluntary attention allocation from automatic orienting. This paper considers the anti-cue pro-saccade task: the subjects were instructed to use the cue to direct attention to the opposite side, i.e. the location, where on valid trials the saccade target would occur. In the companion paper we have used the same physical condition, but we have reversed the instructions as to saccade direction and we have reversed the meaning of the cue, i.e. we designed a pro-cue anti-saccade task. In this first paper, the saccadic reaction times (SRTs) of pro-saccades of five adult subjects were measured in the gap paradigm (fixation point offset precedes target onset by 200 ms). With a CLT of 100 ms, valid anti-cues reduced the number of express saccades (i.e. saccades with SRTs in the range 80–120 ms) significantly compared with the control values (no cues). Valid anti-cues with increasingly long CLTs (100–700 ms) resulted in an increasing incidence of anticipatory saccades and saccades with longer SRTs (more than 120 ms), while the frequency of express saccades remained below the control value. When cue and saccade target were dissociated in location or in both location and direction, the effects of the cueing revealed a much lower spatial selectivity as compared to the effects that have been described for voluntary attention allocation by means of central cues. The results suggest that voluntary allocation of attention and cue-induced automatic orienting not only have different time courses but also have opposite effects on the generation of express saccades, and different spatial selectivities. A possible neuronal basis of these results is discussed considering related findings from electrophysiological studies in monkeys. Received: 27 March 1997 / Accepted: 17 December 1997     

Further observations on the occurrence of express-saccades in the monkey

Summary Express-saccades, i.e. goal directed eye movements with extremely short saccadic reaction times (SRT) have recently been observed in rhesus monkey (70–80 ms) and human subjects (around 100 ms). In the gap task which has been used so far, a central fixation point (Fp) was turned off a short time before a new target (Tg) in the near periphery was presented. Therefore, express-saccades occurred when the goal of fixation was no longer visible. To determine whether or not the absence of the Fp is a necessary condition for the execution of an express-saccade, we used an overlap task in which the monkeys had to change the direction of gaze in the presence of the Fp. The results for this overlap task were compared to those found in the gap task. Three major observations have emerged from the present study. (a) Even though the Fp remained visible, a suddenly appearing peripheral target could be reached by an express-saccade. (b) Express-saccades persisted if the location as well as the time of the appearance of the target was randomized. It appears that for an express-saccade to occur, the process of interruption of previous active fixation must be completed at the time when a new target becomes visible. (c) The spectrum of the monkey's saccadic reaction times contains at least three different peaks: express-saccades with reaction times below 100 ms, fast regular saccades with reaction times around 130 ms, and slow regular saccades with reaction times around 180 ms.     

Effects of reappearance of fixated and attended stimuli upon saccadic reaction time

Summary The effects of visual attention and fixation upon the distribution of saccadic latencies: express (E-), fast regular (FR-), and slow regular (SR-) saccades were investigated. Extinguishing a fixation or an attention point 200–300 ms before target onset increases the incidence of E-saccades while concurrently decreasing the proportion of SR-saccades. Since this extinction forces a disengaging of attention, these changes in relative proportions of saccades reflect the elimination of one of the steps involved in programming saccades. It is shown that a previously attended stimulus has a favored status relative to other stimuli in the visual field. If, after being turned off, the previously attended fixation point or a peripheral attention stimulus is turned on near the time of the target's appearance, the occurrence of the E-saccades is greatly reduced. However, the appearance of any other stimulus in the visual field at or near the time of the target onset does not inhibit E-saccades. Contrary to the conclusions reached by Posner and Cohen (1984), a stimulus presented at the formerly attended location can attract attention more efficiently than a stimulus presented at another, new location.     

Influences of motor instructions on the reaction times of saccadic eye movements

When a gap period is inserted between the fixation point extinction and the target presentation, the distribution of saccadic reaction times has two distinct peaks: one at 150-250 ms (ordinary saccades) and another at approximately 100 ms (express saccades). The distribution of saccadic reaction times can be explained by the linear approach to threshold with ergodic rate (LATER) model, in which the value of a decision signal increases linearly from a start level to initiate a saccade when the signal value reaches a threshold. We hypothesized that a gap period and/or an instruction signal can modulate the parameters of the model to determine when a saccade is initiated. Two reciprobit plots of reaction times, one for ordinary and the other for express saccades, for a task with both a gap period and visuospatial instruction, were constrained by a common infinite-time intercept, although no such constraint was observed during task performance without a visuospatial instruction. We interpreted the results that either the threshold, the start level, or the rate of increase of the decision signal of the model was switched in a bistable manner by both the visuospatial instruction and a gap period, but not by the gap period alone.     

Effects of pre-cues on voluntary and reflexive saccade generation II. Pro-cues for anti-saccades

The reaction times of saccades (SRT) to a suddenly presented visual stimulus (pro-saccade) can be decreased and a separate mode of express saccades can occur when a gap paradigm is used (i.e. fixation-point offset precedes target onset by 200 ms). A valid peripheral cue, presented briefly (100 ms) before target onset, has been found to facilitate the generation of saccades to the target, thereby increasing the frequency of express saccades and decreasing the mean latency. This facilitation occurs only for cues that correctly indicate the direction of the subsequent target presentation (valid cues). The present study investigates the effects of valid cues on SRTs and error rate in the anti-saccade task (saccades in the direction opposite to the stimulus) by systematically varying the cue lead time (CLT) and using the gap and overlap conditions, i.e. fixation point remains on throughout the trial. For a CLT of 100 ms, both reaction times and error rates were significantly increased. With increasing CLT (200–500 ms), both the reaction times of the anti-saccades and the error rates returned to approximately control level, with CLT more than 200 ms in both the gap and the overlap condition. Additional experiments using non-informative cues in the overlap task showed that the reaction times of correct anti-saccades and the error rate were decreased when cue and stimulus appeared at the same side. Analysis of the erratic pro-saccades revealed that almost all of them were corrected, i.e. they were followed by a second saccade towards the required location. It is found that the correction times were usually very short, with intersaccadic intervals between 0 and 150 ms. We suggest that the orienting mechanism, elicited by a transient peripheral cue, relates to the command and the decision to make a pro- rather than an anti-saccade. The cue elicits pro-orienting towards its position when a pro-saccade is required, and anti-orienting when an anti-saccade is required. The orienting effect is transient and decays with CLTs of more than 200 ms; this result holds for both anti-saccades and pro-saccades. Since subjects reported that they could not prevent the erratic pro-saccades or were often not aware of them, we conclude that this orienting mechanism occurs automatically, beyond voluntary control.     

Effect of a local ibotenic acid lesion in the visual association area on the prelunate gyrus (area V4) on saccadic reaction times in trained rhesus monkeys

Summary Two rhesus monkeys were trained to make saccadic eye movements from a central fixation point towards a peripheral target. Saccadic reaction times (SRTs) were measured in the gap paradigm (200 ms pause between offset of fixation point and onset of peripheral target). Target position for extensive training (SRTs of 150 to 250 saccades were collected per day) was four degrees eccentric in the lower quadrant of the visual field contralateral to the intended lesion site in area V4. For control the monkeys were also trained for target positions either in the lower quadrant ipsilateral to the intended lesion site or in the upper visual half field. After several weeks of training a bimodal distribution of saccadic reaction times, one peak at 85 ms (express saccades) and the other around 160 ms (regular saccades) was obtained for each target position. Local injection of ibotenic acid into the 4 deg representation of area V4 resulted in a unimodal distribution of saccadic reaction times (over 90% express saccades) towards the corresponding target position, leaving the distribution of reaction times for the control position unchanged. Recovery began after 5 days and was complete 8 to 10 days after the injection. From these results we conclude that V4 is involved in the generation of the longer latency peak in the distribution of saccadic reaction times by delaying the initiation of visually guided saccades.     

The ability to produce express saccades as a function of gap interval among schizophrenia patients

The ability to produce express sacccades is associated with adequate functioning of saccadic burst cells in the superior colliculus. Saccadic burst cells appear to be under the inhibitory control of both the collicular and the dorsolateral frontal fixation systems. Twenty schizophrenia patients and 20 nonpsychiatric subjects were presented a saccade task that included five different gap intervals (0, 100, 200, 300, and 400 ms) between fixation point offset and peripheral target onset (at ±4°). All subjects generated the highest frequency of express saccades in trials with a gap interval of 200 ms. Schizophrenia patients had an increased frequency of express saccades across gap intervals, especially for targets presented in the right visual field. The groups did not differ in the percentages of anticipatory saccades or saccadic amplitudes. These results suggest that schizophrenia patients' saccadic burst cells in the superior colliculus are functioning adequately, but may be consistent with dys-function of dorsolateral frontal cortex and/or its interconnecting subcortical circuitry.     

Express-saccades of the monkey: Reaction times versus intensity,size, duration,and eccentricity of their targets

Summary Monkeys were trained to fixate a small spot of light (fixation spot) and to saccade to a peripheral target if and only if the fixation spot was turned off. If the offset of the fixation spot preceded the onset of the peripheral target by a temporal gap of more than 140 ms the animals could change their direction of gaze after saccadic reaction times of no more than 70–80 ms (express-saccades). The reaction times of the express-saccades depend on the luminance and the size of the target and decrease from about 120 ms for near threshold targets by about 50 ms in a range of 2,5 log units above threshold (gap duration 200 ms). The minimum reaction time and the target size for which the minimum is reached are functions of the retinal eccentricity of the target. Comparison with response latencies of afferent visual neurons suggests that the dependence of the reaction times of express-as well as regular-saccades on the physical parameters of the target is mostly determined by retinal factors. The short reaction times of the express-saccades are discussed in relation to the reaction times of other visually-guided goal-directed movements.     

The effect of transcranial magnetic stimulation on the latencies of vertical saccades

In this study, we investigated the effect of transcranial magnetic stimulation (TMS) over the right posterior parietal cortex (PPC) on the latency of two different types of visually-guided vertical saccades: reflexive saccades triggered by the sudden onset of a target, and saccades towards target locations known in advance. For this reason, we used two oculomotor tasks: a gap and a delay task, respectively. Nine normal subjects performed vertical saccades at ±7.5 and ±15°. TMS was applied at 80 and 100 ms after target onset in the gap task, and after fixation offset in the delay task. Without TMS, we confirmed a latency asymmetry in the gap task favouring upward saccades at the lower eccentricity (7.5°), and a latency symmetry in the delay task. TMS increased the latencies of all saccades in the delay task, when delivered at 100 ms. This effect was mostly pronounced for downward saccades at 7.5°. As a result, saccade latencies showed an asymmetry in this condition, similar to the one observed in the gap task without TMS. The gap task with TMS resulted in a variable latency distribution and no significant overall effect on saccade latency. Our results indicate that the right PPC is involved in the initiation of vertical saccades in the delay task, and that this involvement appears to be enhanced for downward saccades. A conclusion for the involvement of this area in the gap task could not be drawn from this study.     

The role of fixation point and subjects' readiness in the occurrence of express saccades as revealed by the self-initiation paradigm

The role of fixation and the subjects' response preparedness in producing express saccades were explored in seven human subjects. The occurrence frequencies of the express saccades were compared in the overlap (continuous presentation of fixation point), gap (fixation point offset 0-400 ms prior to target onset) and no-fixation tasks under the conventional and self-initiation paradigms. In the latter paradigm, the subjects, when ready, touched a sensor in order to ignite the target lamp with a delay time of 0-400 ms (target onset delay time). Therefore, the subjects' response preparedness might be expected to be higher than that in the normal paradigm and equated in each subject at the time when the subjects touched a sensor regardless of the paradigms. Although express saccades were produced neither in the normal overlap nor in the normal no-fixation tasks, they could be produced at the rate of 24 and 48% in the overlap and no-fixation tasks under the self-initiation paradigm, respectively. The highest occurrence frequency of express saccades was obtained when the gap paradigm was combined with the self-initiation paradigm with a delay time of 100 ms (62%). The value was higher by 20% than in the normal gap task. At a target onset delay time of 0 ms under the self-initiation paradigm, the occurrence frequency of express saccades was higher in the overlap task than in the gap task. These results suggest that the subjects' response preparedness has a potentiality to produce express saccades without fixation point offset and that fixation point offset at the same time of the target stimulus onset has an interference, rather than facilitatory, influence on the generation of express saccades.     

Cortical potentials during the gap prior to express saccades and fast regular saccades

When a temporal gap is introduced between the offset of the central fixation point and the appearance of a new target, saccadic reaction time is reduced (gap effect) and a special population of extremely fast saccades occurs (express saccades). It has been hypothesized that the gap triggers a readiness signal, which is responsible for the reduced saccadic reaction times. Here we recorded event-related potentials during the gap to in vestigate the central processes associated with the gener ation of fast regular saccades and express saccades. Prior to the execution of fast regular saccades, subjects pro duced a slow negative shift, with a maximum at frontal and central channels that started 40 ms after fixation offset. This widespread negativity is similar to a readiness potential. Anticipatory saccades were preceded by an increased frontal and parietal negativity. Prior to express saccades, a frontal negativity was observed, which started 135 ms after the disappearance of the fixation point. It is assumed that the frontal negativity prior to express saccades corresponds to the fixation-disengagement dis charge described in the frontal eye field of monkeys. Therefore, we hypothesize that fast regular saccades are the result of an increased readiness signal, while express saccades are the result of specific preparatory processes.     

Hypometric primary saccades of schizophrenics in a delayed-response task

In this study, the execution of delayed saccades in 15 DSM-III-R-schizophrenic patients and 15 normal subjects was investigated. While looking at a central fixation cross, a peripheral target was randomly presented at 10° eccentricity. Subjects were instructed to saccade to the target when the fixation cross was switched off after 500 ms. Two experiments were conducted: (a) a delayed-saccade task and, (b) a memoryguided saccade task, that is, the peripheral target was switched off together with the fixation cross. In the delayed-saccade task, amplitudes of regular saccades did not differ between schizophrenic patients and normals. In the memory-guided saccade task, schizophrenic subjects showed marked hypometric saccades. Incorrect delayed saccades (while the fixation cross was on) were also hypometric in schizophrenics, but not in normal controls. The final eye position, i.e., the position reached after the execution of correction saccades, however, did not differ between patients and controls. This means that schizophrenics show a deficit in the programming of primary saccades, if the fixation point and the peripheral target are (a) both visually presented or (b) both memorized. The results support the hypothesis that these saccades are the result of an averaging effect between the fixation point and the peripheral target. It is further hypothesized that these deficits might be explained by a lack of prefrontal inhibition of ocular fixation areas.     

Covert attention regulates saccadic reaction time by routing between different visual-oculomotor pathways

Covert attention modulates saccadic performance, e.g., the abrupt onset of a task-irrelevant visual stimulus grabs attention as measured by a decrease in saccadic reaction time (SRT). The attentional advantage bestowed by the task-irrelevant stimulus is short-lived: SRT is actually longer ~200 ms after the onset of a stimulus than it is when no stimulus appears, known as inhibition of return. The mechanism by which attention modulates saccadic reaction is not well-understood. Here, we propose two possible mechanisms: by selective routing of the visuomotor signal through different pathways (routing hypothesis) or by general modulation of the speed of visuomotor transformation (shifting hypothesis). To test them, we designed a cue gap paradigm in which a 100-ms gap was introduced between the fixation point disappearance and the target appearance to the conventional cued visual reaction time paradigm. The cue manipulated the location of covert attention, and the gap interval resulted in a bimodal distribution of SRT, with an early mode (express saccade) and a late mode (regular saccade). The routing hypothesis predicts changes in the proportion of express saccades vs. regular saccades, whereas the shifting hypothesis predicts a shift of SRT distribution. The addition of the cue had no effect on mean reaction time of express and regular saccades, but it changed the relative proportion of two modes. These results demonstrate that the covert attention modification of the mean SRT is largely attributed to selective routing between visuomotor pathways rather than general modulation of the speed of visuomotor transformation.