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.     

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.     

Human express saccades: effects of randomization and daily practice

Summary When human subjects are asked to execute saccades from a fixation point to a peripheral target, if the fixation point is turned off some time (200 ms) before the target is turned on, the distribution of the saccadic reaction times is bimodal. The first peak occurs at about 100 ms and represents the population of express saccades. If the target location is kept constant the express saccades have reaction times of about 100 ms. If the target location is randomized between right and left (distance from fixation point constant at 4 deg) the reaction times of the express saccades are increased by about 15 ms. If the target location is randomized between 4 deg and 8 deg (direction constant to the right) no increase of the reaction time is observed. The proportion of express saccades increases with daily practice and their reaction times decrease slightly from 105 ms to 98 ms. If an anticipatory saccade was made after reaction times below 75 ms, it frequently undershot the target by more than 20% and was followed by a corrective saccade. The corrections could be executed at times where usually an express saccade would have occurred such that all of these corrections began at about the same time, i.e. 100 ms after target onset, implying intersaccadic intervals between 100 ms and zero (!)     

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.     

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.     

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.     

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.     

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.     

The remembered pursuit task: evidence for segregation of timing and velocity storage in predictive oculomotor control

Regular, repeated presentation of identical constant-velocity target motion stimuli (ramps) appears to allow build up of an internal store, release of which can be used to generate anticipatory smooth pursuit prior to subsequent target onset. Here, we examine whether release of the anticipatory response can be controlled by timing cues unrelated to the motion stimulus itself. In experiment 1, the target moved in alternate directions and was exposed for 480 ms as it passed through centre; otherwise subjects were in darkness. Inter-stimulus interval (ISI) was either regular (3.6 s) or randomized (2.7–4.3 s). Presentations were given with or without audio cues that occurred at a constant cue time (CT) prior to target appearance. Even when ISI was randomized, cues could be used to generate anticipatory smooth pursuit. Eye velocity (V100) measured 100 ms after target onset (just prior to visual feedback influence) was greater with cues than without and decreased significantly as CT increased from 240–960 ms. In experiment 2, we assessed the effects of fixation between presentations and eccentricity of target starting position, using unidirectional ramps. The target was visible for 400 ms and started on, ended on or straddled the midline. Subjects held fixation on the midline until an audio cue signalled that preparation for ensuing target appearance could begin. There was no difference in V100 between starting positions or between presence/absence of fixation. In experiment 3, we compared the effects of using audio, visual or tactile cues. All types of cue evoked anticipatory smooth pursuit, but the response to the visual cue was significantly delayed compared with the others. However, V100 was not significantly different between cues. In all experiments, V100 was scaled in proportion to target velocity over the range 12.5–50°/s, showing that this was a truly predictive response. The results provide evidence that timing and velocity storage can be independently controlled through different sensory channels and suggest that the two functions are probably carried out by separate neural mechanisms. Received: 3 December 1998 / Accepted: 11 May 1999     

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.     

Facilitatory effects of an auditory warning stimulus in a visual location identification task and a visual shape identification task

The occurrence of a weak auditory warning stimulus increases the speed of the response to a subsequent visual target stimulus that must be identified. This facilitatory effect has been attributed to the temporal expectancy automatically induced by the warning stimulus. It has not been determined whether this results from a modulation of the stimulus identification process, the response selection process or both. The present study examined these possibilities. A group of 12 young adults performed a reaction time location identification task and another group of 12 young adults performed a reaction time shape identification task. A visual target stimulus was presented 1850 to 2350 ms plus a fixed interval (50, 100, 200, 400, 800, or 1600 ms, depending on the block) after the appearance of a fixation point, on its left or right side, above or below a virtual horizontal line passing through it. In half of the trials, a weak auditory warning stimulus (S1) appeared 50, 100, 200, 400, 800, or 1600 ms (according to the block) before the target stimulus (S2). Twelve trials were run for each condition. The S1 produced a facilitatory effect for the 200, 400, 800, and 1600 ms stimulus onset asynchronies (SOA) in the case of the side stimulus-response (S-R) corresponding condition, and for the 100 and 400 ms SOA in the case of the side S-R non-corresponding condition. Since these two conditions differ mainly by their response selection requirements, it is reasonable to conclude that automatic temporal expectancy influences the response selection process.     

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.     

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.     

Neural correlates of inter- and intra-individual saccadic reaction time differences in the gap/overlap paradigm

To examine the neural correlates of contextually differing control mechanisms in saccade initiation, we studied 18 subjects who performed two saccade paradigms in a pseudo-random order, while their eye movements were recorded in the MRI scanner (1.5 T). In the gap task the fixation point was extinguished 200 ms before target onset, and in the overlap task the fixation point vanished 500 ms after target onset. Subjects were asked to maintain stable fixation in the fixation period and to quickly saccade to peripherally presented targets. Inter-individual activation differences were assessed using regression analyses at the second level, with mean saccadic reaction time (SRT) of subjects as a covariate. To identify brain regions varying with trial-by-trial changes in SRTs, we included SRTs as a parametric modulation regressor in the general linear model. All analyses were regions of interest based and were performed separately for the gap and overlap conditions. For the gap paradigm, we did not obtain activation in regions previously shown to be involved in preparatory processes with much longer gap periods. Interestingly, both inter- and intra-individual variability analyses revealed a positive correlation of activation in frontal and parietal eye-movement regions with SRTs, indicating that slower saccade performance is possibly associated with higher cortical control. For the overlap paradigm, the trial-by-trial variability analysis revealed a positive correlation of activation in the right opercular inferior frontal gyrus with SRTs, possibly linked to fixation-related processes that have to be overcome to perform a speeded saccade in presence of a fixation point.     

Adaptive changes in smooth pursuit eye movements induced by cross-axis pursuit-vestibular interaction training in monkeys

The smooth pursuit system interacts with the vestibular system to maintain the accuracy of eye movements in space. To understand neural mechanisms of short-term modifications of the vestibulo-ocular reflex (VOR) induced by pursuit-vestibular interactions, we used a cross-axis procedure in trained monkeys. We showed earlier that pursuit training in the plane orthogonal to the rotation plane induces adaptive cross-axis VOR in complete darkness. To further study the properties of adaptive responses, we examined here the initial eye movements during tracking of a target while being rotated with a trapezoidal waveform (peak velocity 30 or 40°/s). Subjects were head-stabilized Japanese monkeys that were rewarded for accurate pursuit. Whole body rotation was applied either in the yaw or pitch plane while presenting a target moving in-phase with the chair with the same trajectory but in the orthogonal plane. Eye movements induced by equivalent chair rotation with or without the target were examined before and after training. Before training, chair rotation alone resulted only in the collinear VOR, and smooth eye movement-tracking of orthogonal target motion during rotation had a normal smooth pursuit latency (ca 100 ms). With training, the latency of orthogonal smooth tracking eye movements shortened, and the mean latency after 1 h of training was 42 ms with a mean gain, at 100 ms after stimulus onset, of 0.4. The cross-axis VOR induced by chair rotation in complete darkness had identical latencies with the orthogonal smooth tracking eye movements, but its gains were <0.2. After cross-axis pursuit training, target movement alone without chair rotation induced smooth pursuit eye movements with latencies ca 100 ms. Pursuit training alone for 1 h using the same trajectory but without chair rotation did not result in any clear change in pursuit latency (ca 100 ms) or initial eye velocity. When a new target velocity was presented during identical chair rotation after training, eye velocity was correspondingly modulated by just 80 ms after rotation onset, which was shorter than the expected latency of pursuit (ca 100 ms). These results indicate that adaptive changes were induced in the smooth pursuit system by pursuit-vestibular interaction training. We suggest that this training facilitates the response of pursuit-related neurons in the cortical smooth pursuit pathways to vestibular inputs in the orthogonal plane, thus enabling smooth eye movements to be executed with shorter latencies and larger eye velocities than in normal smooth pursuit driven only by visual feedback. Electronic Publication     

Cognitive control can modulate intersensory facilitation: speeding up visual antisaccades with an auditory distractor

Although saccadic reaction times to a visual stimulus are facilitated if an auditory accompanying stimulus is presented at the same location, this intersensory facilitation effect (IFE) has not been explored for antisaccades (saccades directed opposite to a visual target). In this study participants were asked to make an antisaccade opposite to a point of light presented right or left of fixation while accompanied by an auditory stimulus either at the same or at the opposite location with different stimulus onset asynchronies. Antisaccade reaction times for unimodal auditory and bimodal stimuli were shorter than for unimodal visual stimulation, in line with prosaccade studies. The auditory accompanying stimulus afforded antisaccade reaction times approximately as fast as prosaccades in the direction of a visual target, especially when it was presented 40 ms before the spatially congruent visual target. Moreover, predictiveness of the target position facilitated performance only when the auditory stimulus was presented at the opposite location and 40 ms before the visual target (interstimulus contingency effect). We conclude that intersensory facilitation is a mandatory, bottom-up process, but in the particular case of a response conflict due to a visual target, IFE can be shown to be modulated by the predictability of the target location.     

Differential effects of target probability on saccade latencies in gap and warning tasks

Saccade latencies are significantly reduced by extinguishing a foveal fixation stimulus before the appearance of a saccade target. It has been shown recently that this fixation offset effect (FOE) can be modulated by varying target probability. Cortico-collicular top-down effects have been assumed to mediate this strategic FOE modulation. Here, we have investigated strategic FOE modulation in 14 healthy human subjects performing gap and warning tasks. In the former task, the central fixation point was extinguished 200 ms before target onset. In the latter task, the central fixation point changed its colour 200 ms before target onset, but remained illuminated until the target appeared. Target probability was varied block-wise between 25 and 75%. In both tasks, mean latencies decreased with increasing target probability. However, in contrast with what can be expected from preceding studies, we found no differential modulation of mean latencies by target probability between tasks. Instead, we observed differential probability-dependent changes in latency distributions. In the gap task, discrete changes of saccade latencies were found, with a probability-dependent change in frequency of express and regular latencies. By contrast, in the warning task a shift of the entire latency distribution towards longer latencies with low target probability was found. We conclude that strategic modulation of saccade latencies by target probability may be mediated by two distinct neural mechanisms. Selection of either mechanism seems to depend critically on activation of the fixation system.     

Estimating the components of the gap effect

The gap effect refers to the finding that saccadic latencies are typically reduced when a fixation point is removed prior to the appearance of a peripheral target. This reduction in saccadic reaction time (SacRT) is thought to be due to a general warning effect and an oculomotor specific fixation offset that occur when the fixation point is removed. In order to estimate the contribution of each of these effects to the overall gap effect, this paper introduces a new manipulation, the partial-gap trial, where the fixation point undergoes a change in size prior to the presentation of the target. The partial-gap trial is presumed to provide the visual warning effect of the fixation offset (i.e. similar to that in a gap trial) but does not provide the fixation offset effect (FOE). When the fixation point was abruptly reduced in size before the presentation of the target, the estimated decrease in SacRT due to the visual warning effect was 5-7% and did not differ in the presence or absence of an auditory warning signal. It was found that auditory warning effect and the FOE interacted in reducing SacRTs. Additionally, when the fixation point was abruptly increased in size before the presentation of the target, SacRTs were slower than when the fixation point did not change in size and remained present for the entire trial (i.e. an overlap trial). We conclude that this new partial-gap paradigm is a useful method for researchers wishing to separately examine FOE and visual warning effects.     

Possible role of pirenzepine on the release of pancreatic polypeptide in duodenal ulcer patients: preliminary results of a randomized cross-over study

The effects of repeated oral doses of pirenzepine (100 mg daily for 7 days) and antacid (Maalox, 105 ml daily for 7 days) on the test-meal-stimulated release of pancreatic polypeptide (PP) were evaluated in 7 duodenal ulcer outpatients by means of a randomized cross-over study, with a wash-out period of one week between pirenzepine and antacid administration. The effects of pirenzepine (100 mg daily for 7 days) were also evaluated in 5 healthy adult volunteers. The stimulus test was performed on each fasting patient two days before the treatment started and after a 7-day treatment. Venous blood samples were obtained before the test meal (basal) and 3, 10 and 30 minutes after it. Plasma PP levels were estimated by means of a specific RIA. The results obtained showed that pirenzepine significantly inhibits the PP response to the test meal in the duodenal ulcer patients and in the healthy volunteers. The above-mentioned effects suggest that one of the mechanisms of action on the therapeutic activity of pirenzepine on peptic ulcer might be explained by the preservation of pancreatic secretion unimpaired by an increase in PP release after meal stimulus.