Gap effects on saccade and vergence latency

To explore visual space, we make saccades, vergence, and, most frequently, combined saccade–vergence eye movements. The initiation of saccades is well studied, while that of vergence is less explored. Saccade latency is influenced by the fixation task: when the target appears simultaneously with the offset of the fixation point, latencies tend to be regular, whereas the introduction of a gap period before target onset causes the emergence of express latencies (80- to 120-ms). This study examines in ten normal adults whether the gap paradigm has a similar effect on the latency of vergence and combined eye movements. The second goal is to identify contextual factors that favor the emergence of short latencies, by comparing a condition in which gap and simultaneous trials were performed in separate blocks (pure blocks) with a condition in which the two types of trials were interleaved randomly (mixed blocks). The results are: (1) the gap paradigm reduced similarly (by approximately –30 ms) the mean latency of saccades, convergence, divergence, and both the saccadic and vergence components of combined eye movements; (2) the gap paradigm was responsible for the emergence of 80– to 120-ms latencies for saccades and divergence (pure or combined), but rarely for convergence; (3) inspection of the latency distributions showed that such short latencies formed a clearly distinct population, different from anticipatory responses or regular latencies, for saccades (pure or combined) but not for pure vergence; importantly, distinct express latencies were found also for the convergence and divergence components of combined eye movements; (4) no difference was found for the group of subjects between pure and mixed blocks, but the latter yielded shorter latencies for some subjects, suggesting an idiosyncratic phenomenon. We suggest that distinct express latencies are specific to saccades and could correspond to a specific mode of saccade initiation. Interestingly, the express mode of triggering can be transferred to the vergence component in the ecological condition in which saccade is combined with vergence.     

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.     

The time of secondary saccades to primary targets

When a first saccade is made in response to a single, suddenly appearing stimulus it often misses the target. The retinal error may be very large, in particular in those cases where the subject anticipates the target location and initiates a saccade to a wrong position. We have analyzed the time of the occurrence of the secondary saccades by which the subject corrects these errors. Using the gap task with random target locations we found that large errors after anticipatory saccades — especially those after direction errors — can be corrected very fast. The latencies of these corrective saccades (being measured from target onset, not from the end of the primary saccade) form bimodal distributions with a first peak at 100 ms. It is therefore concluded that large errors can be corrected by express secondary saccades.     

Characteristics of contralesional and ipsilesional saccades in hemianopic patients

In order to further our understanding of action-blindsight, four hemianopic patients suffering from visual field loss contralateral to a unilateral occipital lesion were compared to six healthy controls during a double task of verbally reported target detection and saccadic responses toward the target. Three oculomotor tasks were used: a fixation task (i.e., without saccade) and two saccade tasks (eliciting reflexive and voluntary saccades, using step and overlap 600 ms paradigms, respectively), in separate sessions. The visual target was briefly presented at two different eccentricities (5° and 8°), in the right or left visual hemifield. Blank trials were interleaved with target trials, and signal detection theory was applied. Despite their hemifield defect, hemianopic patients retained the ability to direct a saccade toward their contralesional hemifield, whereas verbal detection reports were at chance level. However, saccade parameters (latency and amplitude) were altered by the defect. Saccades to the contralesional hemifield exhibited longer latencies and shorter amplitudes compared to those of the healthy group, whereas only the latencies of reflexive saccades to the ipsilesional hemifield were altered. Furthermore, healthy participants showed the expected latency difference between reflexive and voluntary saccades, with the latter longer than the former. This difference was not found in three out of four patients in either hemifield. Our results show action-blindsight for saccades, but also show that unilateral occipital lesions have effects on saccade generation in both visual hemifields.     

The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey

Rhesus monkeys were trained to make saccadic eye movements to visual targets using detection and discrimination paradigms in which they were required to make a saccade either to a solitary stimulus (detection) or to that same stimulus when it appeared simultaneously with several other stimuli (discrimination). The detection paradigm yielded a bimodal distribution of saccadic latencies with the faster mode peaking around 100 ms (express saccades); the introduction of a pause between the termination of the fixation spot and the onset of the target (gap) increased the frequency of express saccades. The discrimination paradigm, on the other hand, yielded only a unimodal distribution of latencies even when a gap was introduced, and there was no evidence for short-latency "express" saccades. In three monkeys either the frontal eye field or the superior colliculus was ablated unilaterally. Frontal eye field ablation had no discernible long-term effects on the distribution of saccadic latencies in either the detection or discrimination tasks. After unilateral collicular ablation, on the other hand, express saccades obtained in the detection paradigm were eliminated for eye movements contralateral to the lesion, leaving only a unimodal distribution of latencies. This deficit persisted throughout testing, which in one monkey continued for 9 mo. Express saccades were not observed again for saccades contralateral to the lesion, and the mean latency of the contralateral saccades was longer than the mean latency of the second peak for the ipsiversive saccades. The latency distribution of saccades ipsiversive to the collicular lesion was unaffected except for a few days after surgery, during which time an increase in the proportion of express saccades was evident. Saccades obtained with the discrimination paradigm yielded a small but reliable increase in saccadic latencies following collicular lesions, without altering the shape of the distribution. Unilateral muscimol injections into the superior colliculus produced results similar to those obtained immediately after collicular lesions: saccades contralateral to the injection site were strongly inhibited and showed increased saccadic latencies. This was accompanied by a decrease of ipsilateral saccadic latencies and an increase in the number of saccades falling into the express range. The results suggest that the superior colliculus is essential for the generation of short-latency (express) saccades and that the frontal eye fields do not play a significant role in shaping the distribution of saccadic latencies in the paradigms used in this study.(ABSTRACT TRUNCATED AT 400 WORDS)     

Peak velocities of visually and nonvisually guided saccades in smooth-pursuit and saccadic tasks

 Smooth pursuit typically includes corrective catch-up saccades, but may also include such intrusive saccades away from the target as anticipatory or large overshooting saccades. We sought to differentiate catch-up from anticipatory and overshooting saccades by their peak velocities, to see whether the higher velocities of visually rather than nonvisually guided saccades in saccadic tasks may be found also in saccades in pursuit. In experiment 1, 12 subjects showed catch-up, anticipatory, and overshooting saccades to comprise 70.4% of all saccades in pursuit of periodic, 30°/s constant-velocity targets. Catch-up saccades were faster than the others. Saccadic tasks were run as well, on 19 subjects, including the 12 whose pursuit data were analyzed, with target-onset, target-remaining (saccade to the remaining target when the other three extinguish), and antisaccade tasks. For 17 of the 19 subjects, antisaccade velocities were lower than for either target-onset or target-remaining tasks. Velocities for the target-remaining task were near those for target onset, indicating that target presence, not its onset, defines visually guided saccades. Error and reaction-time data suggest greater cognitive difficulty for target remaining than for target onset, so that the cognitive difficulty of typical nonvisually guided saccade tasks is not sufficient to produce their lowered velocity. To produce reliably, in each subject, catch-up and anticipatory saccades with comparable amplitude distributions, nine new subjects were asked in experiment 2 to make intentional catch-up and anticipatory saccades in pursuit, and were presented with embedded target jumps to elicit catch-up saccades, all with periodic target trajectories of 15°/s and 30°/s. Velocities of intentional anticipatory saccades were lower than velocities of intentional catch-up saccades, while velocities of intentional and embedded catch-up saccades were similar. Target-onset and remembered-target saccadic tasks were run, showing the expected higher velocity for the target-onset task in each subject. Both experiments demonstrate higher peak velocities for catch-up saccades than for anticipatory saccades, suggesting that cortical structures preferentially involved in nonvisually guided saccades may initiate the anticipatory and overshooting saccades in pursuit. Received: 1 December 1995 / Accepted: 25 February 1997     

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.     

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 (!)     

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.     

Saccadic instabilities and voluntary saccadic behaviour

Primary gaze fixation is never perfectly stable but can be interrupted by involuntary, conjugate saccadic intrusions (SI). SI have a high prevalence in the normal population and are characterised by a horizontal fast eye movement away from the desired eye position, followed, after a variable duration, by a return saccade or drift. Amplitudes are usually below 1° and they often exhibit a directional bias. The aim of the present study was to investigate the aetiology of SI in relation to saccadic behaviour. It was hypothesised that if SI resulted from deficits in the saccadic system (i.e. reduced inhibitory mechanisms), changes in voluntary saccade behaviour may be apparent and related to SI frequency. To examine this, synchrony (no gap), gap, overlap and antisaccade tasks were conducted on ten normal subjects. No significant correlations were found between SI frequency and voluntary saccade latencies, the percentage of express saccades, or the percentage of antisaccade errors. In addition, no significant correlations were found between SI directional biases and saccade latency directional biases, express saccade biases or antisaccade error biases. These results suggest that an underlying alteration to saccadic behaviour is unlikely to be involved in SI production, and that the SI command signal may arise from the influence of attention on an intact saccadic system. Specifically, descending corticofugal signals relating to attention level and orientation may alter the balance between fixation and saccade generation, so determining SI characteristics.     

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

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

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.     

Occurrence of human express saccades depends on stimulus uncertainty and stimulus sequence

Summary Saccadic latencies measured in response to a step-wise displacement of the target may be substantially reduced if a gap separates the offset of the initial fixation point and the onset of the peripheral target. According to Fischer and Ramsperger (1984) this paradigm provokes a bimodal latency distribution which consists of a peak of very fast saccadic responses (express saccades) at about 110 ms and another peak arising from somewhat slower saccades (regular saccades). Using again the gap paradigm, we investigated the effect of an additional go/no-go (i.e. target trial/catch trial) decision on saccadic latencies. The experiments yielded the following results: (i) the distribution between the peaks of express and regular saccades strongly depends on the proportion of catch trials introduced into the trial sequence, which suggests the existence of different modes of operation of the decision processes for express and regular saccades. (ii) The catch trial effect on saccadic latency proved to be a local phenomenon in time: saccades which follow catch trials tend to be slower than those following target trials.     

Motion processing for saccadic eye movements in humans

Summary 1. We studied the latencies and amplitudes of saccades to moving targets in normal human subjects. Targets underwent ramp or step-ramp motions. The goal was to determine how the saccadic system uses information about target velocity. 2. For simple ramp motion saccadic latency decreased as target speed increased. A threshold distance model, which assumes that the target has to move a minimum distance before saccadic processing starts, provided a good fit to the responses of all four subjects and explains discrepancies between previously published findings. 3. A double step experiment showed that target position may have some effect on saccadic amplitude when sampled 70 ms before saccade onset, but it must be sampled at least 140 ms before onset for an accurate saccade to occur. 4. Saccades to simple ramp targets approximated the target position 55 ms before saccade onset. Based on our double step results, this is more compensation than possible by a simple position estimate and implies extrapolation of target motion by the saccadic system. The lack of complete compensation may be due to an underestimate of the target speed and/or of the saccadic latency. 5. A delayed-saccade paradigm resulted in saccades with a longer, constant latency and allowed longer viewing of target motion. These saccades accounted for all but 20 ms of target motion, suggesting that with more processing time of target motion a better extrapolation may be generated. 6. In a step-ramp paradigm the target stepped in one direction, then moved smoothly in the opposite direction. Saccades in this paradigm could be made in either the direction of the step or in the direction of target motion: the direction and latency were determined solely by the time at which the target crossed the fixation point. This time must be calculated from target speed and position, implying that the saccadic system must use speed information to adjust latency or to cancel unnecessary saccades.     

Electroencephalographic cortical oscillations and saccadic eye movements in humans

A model predicting different types of saccades has suggested that the presence of rhythmic brain activity determines whether a subject will produce regular or express saccades. We studied cortical oscillations preceding saccadic eye movements. Brain electrical activity was recorded in nine healthy adults continuously from 30 electrodes while subjects performed saccades. In a so-called gap condition multimodal latency distributions resulted. Express saccades were preceded by different oscillatory activity than regular saccades. This was a highly significant finding restricted to the alpha and beta bands of the EEG. Step-wise discriminant analysis showed that cortical oscillations measured from only few electrode sites allowed to predict reliably which type of saccade a subject will make. These findings support the notion that stimulus-induced oscillations of the human EEG may modulate thresholds for triggering saccades.     

Deficits of cortical oculomotor mechanisms in cerebellar atrophy patients

Commonly, the cerebellum is not associated with cortical components of saccadic eye movement programming. The present study investigates cerebellar effects on visually guided saccades in reflexive tasks (step, gap, overlap) and on internally driven saccades in intentional tasks (anti, memory, short memory sequences of four targets) in five patients with isolated cerebellar atrophy. The cerebellar dysfunction led to impairments in both reflexive and intentional saccades. Cerebellar atrophy patients showed an increase in the gain variability and an increase in the saccade latency. Furthermore, in the memory and anti task, suppression and pro-saccade errors were more frequent in the atrophy group compared to the control group. In the sequence task, patients had difficulties reproducing all four target locations in the order of the displayed sequence. The high variability of the saccade gain is a common observation in cerebellar atrophy patients and can be explained by the general variability present in the saccadic system. The increase in the saccade latency could be due to a cerebellar contribution to cortical processes related to fixation and target selection preceding the initiation of a saccade. Furthermore, the frequent occurrence of saccade errors in the memory and anti task suggests a cerebellar involvement in frontal inhibition of unwanted reflexive saccades. The impaired reproduction of saccade sequences in atrophy patients points to a deficit in short-term memory processes. Thus, this study provides further evidence that the cerebellum is involved in different cortical mechanisms related to the control of saccadic eye movements.     

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     

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.     

The differentiation of visually guided and anticipatory saccades in gap and overlap paradigms

Summary Saslow and others have shown that the latency of foveating saccades can be altered by changing the offset time of the current fixation point relative to the onset of the peripheral target. Whether anticipatory saccades contributed to these results was not known. By the criteria of direction error and amplitude error the minimum latency for visually guided saccades is 110–130 ms for three subjects and 160 ms for a longer latency subject. Excluding anticipatory responses did not eliminate offset-onset effects. The genesis of express saccades and the role of higher neural levels is discussed.     

Modification of saccadic gain by reinforcement

Control of saccadic gain is often viewed as a simple compensatory process in which gain is adjusted over many trials by the postsaccadic retinal error, thereby maintaining saccadic accuracy. Here, we propose that gain might also be changed by a reinforcement process not requiring a visual error. To test this hypothesis, we used experimental paradigms in which retinal error was removed by extinguishing the target at the start of each saccade and either an auditory tone or the vision of the target on the fovea was provided as reinforcement after those saccades that met an amplitude criterion. These reinforcement procedures caused a progressive change in saccade amplitude in nearly all subjects, although the rate of adaptation differed greatly among subjects. When we reversed the contingencies and reinforced those saccades landing closer to the original target location, saccade gain changed back toward normal gain in most subjects. When subjects had saccades adapted first by reinforcement and a week later by conventional intrasaccadic step adaptation, both paradigms yielded similar degrees of gain changes and similar transfer to new amplitudes and to new starting positions of the target step as well as comparable rates of recovery. We interpret these changes in saccadic gain in the absence of postsaccadic retinal error as showing that saccade adaptation is not controlled by a single error signal. More generally, our findings suggest that normal saccade adaptation might involve general learning mechanisms rather than only specialized mechanisms for motor calibration.