Burkhart Fischer

Express Saccades and Visual Attention

One of the most intriguing and controversial observations in oculomotor research in recent years is the phenomenon of express saccades in monkeys and man. These are saccades with such short reaction times (100 msec in man, 70 msec in monkeys) that some experts on eye movements still regard them as artifacts or as anticipatory reactions that do not need any further explanation. On the other hand, some research groups consider them not only authentic but also a valuable means of investigating the mechanisms of saccade generation, the coordination of vision and eye movements, and the mechanisms of visual attention. This target article puts together pieces of experimental evidence in oculomotor and related research – with special emphasis on the express saccade – to enhance our present understanding of the coordination of vision, visual attention, and the eye movements subserving visual perception and cognition. We hypothesize that an optomotor reflex is responsible for the occurrence of express saccades, one that is controlled by higher brain functions involved in disengaged visual attention and decision making. We propose a neural network as the basis for more elaborate mathematical models or computer simulations of the optomotor system in primates.

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

SummaryHuman 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.

The antisaccade: a review of basic research and clinical studies

The ability to suppress reflexive responses in favor of voluntary motor acts is crucial for everyday life. Both abilities can be tested with an oculomotor task, the antisaccade task. This task requires subjects to suppress a reflexive prosaccade to a flashed visual stimulus and instead to generate a voluntary saccade to the opposite side. This article reviews what is currently known about the neural structures and processes which are involved in the performance of this task. Current data show that a variety of brain lesions, neurological diseases and psychiatric disorders result in errors, i.e. prosaccades towards the stimulus, in this task. Brain imaging studies have shown that a widely distributed cortical and subcortical network is active during the generation of antisaccades. These findings are discussed and the potential of the antisaccade task for diagnostic purposes is evaluated.

Saccadic eye movements after extremely short reaction times in the monkey.

Monkeys were trained to change their direction of gaze from one point (fixation point) to another (target). If the fixation point was extinguished at the same time when the new target occurred the saccadic reaction times (SRT) were in the order of 200 ms. If the fixation point disappeared 150-250 ms before the new target occurred (gap with no visible stimulus) monkeys made regular saccades after shorter reaction times of about 140 ms. In addition animals in the gap situation made saccades that had reaction times of no more than 70-80 ms measured from the onset of the new target (Express-Saccades). The reaction times of the E-saccades have standard deviations of only +/- 3 ms. E-saccades occurred with a frequency of up to 80% for gaps of 200-240 ms. If the gap was shorter than 180 ms increasingly more regular saccades were made with reaction times of 140-160 ms. With gap duration decreasing from 140 ms to zero all saccades were regular with SRTs increasing linearly to more than 200 ms. In one animal almost all E-saccades fell short and were corrected after less than 250 ms depending on the size of the error: large errors were corrected faster than small ones.

On the development of voluntary and reflexive components in human saccade generation

The saccadic performance of a large number (n = 281) of subjects of different ages (8-70 years) was studied applying two saccade tasks: the prosaccade overlap (PO) task and the antisaccade gap (AG) task. From the PO task, the mean reaction times and the percentage of express saccades were determined for each subject. From the AG task, the mean reaction time of the correct antisaccades and of the erratic prosaccades were measured. In addition, we determined the error rate and the mean correction time, i.e. the time between the end of the first erratic prosaccade and the following corrective antisaccade. These variables were measured separately for stimuli presented (in random order) at the right or left side. While strong correlations were seen between variables for the right and left sides, considerable side asymmetries were obtained from many subjects. A factor analysis revealed that the seven variables (six eye movement variables plus age) were mainly determined by only two factors, V and F. The V factor was dominated by the variables from the AG task (reaction time, correction time, error rate) the F factor by variables from the PO task (reaction time, percentage express saccades) and the reaction time of the errors (prosaccades!) from the AG task. The relationship between the percentage number of express saccades and the percentage number of errors was completely asymmetric: high numbers of express saccades were accompanied by high numbers of errors but not vice versa. Only the variables in the V factor covaried with age. A fast decrease of the antisaccade reaction time (by 50 ms), of the correction times (by 70 ms) and of the error rate (from 60 to 22%) was observed between age 9 and 15 years, followed by a further period of slower decrease until age 25 years. The mean time a subject needed to reach the side opposite to the stimulus as required by the antisaccade task decreased from approximately 350 to 250 ms until age 15 years and decreased further by 20 ms before it increased again to approximately 280 ms. At higher ages, there was a slight indication for a return development. Subjects with high error rates had long antisaccade latencies and needed a long time to reach the opposite side on error trials. The variables obtained from the PO task varied also significantly with age but by smaller amounts. The results are discussed in relation to the subsystems controlling saccade generation: a voluntary and a reflex component the latter being suppressed by active fixation. Both systems seem to develop differentially. The data offer a detailed baseline for clinical studies using the pro- and antisaccade tasks as an indication of functional impairments, circumscribed brain lesions, neurological and psychiatric diseases and cognitive deficits.

Characteristics of "anti" saccades in man.

SummaryFour subjects — all made large numbers of Express saccades in the normal gap task — were instructed to make saccades in the direction opposite to the side where a visual stimulus appeared (“anti” task). Gap and overlap trials were used. Saccadic reaction time (SRT), velocity and amplitude of the corresponding eye movements were analysed and compared to those of saccades made in the normal task. The velocity of “anti saccades” was found to be slightly (up to 15%) but significantly slower in two subjects. The distributions of SRTs in normal gap tasks show a small group of anticipatory saccades (with SRT below 80 ms and slower velocities) followed by a group of saccades with fast reaction times between 80 ms and 120 ms (Express saccades) followed by another large group ranging up to 180 ms (regular saccades). In the gap anti task there are anticipatory saccades and saccades with SRTs above 100 ms; Express saccades are missing. The distribution of SRTs obtained in the overlap anti task was unimodal with a mean value of 231 ms as compared to 216 ms in the normal task. The introduction of the gap therefore clearly decreases the reaction times of the anti saccades. Control experiments show that the delay of anti saccades is not due to an interhemispheric transfer time but must be attributed to the saccade generating system taking more time to program a saccade to a position where no visual stimulus appears. These data are discussed as providing further evidence for the existence of a reflex-like pathway connecting the retina to the oculomotor nuclei mediating the Express saccade.

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

SummaryThe 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 and visual attention in the occurrence of express saccades in man.

SummaryThe differential influence of fixation and directed visual attention on reaction times of goal-directed saccades and especially on the occurrence of express saccades was investigated.In all the experiments the subjects were instructed first to keep their direction of gaze at the center of a translucent screen with or without a central fixation point. When a new stimulus appeared, the subjects had to look at it as soon as possible. In some control experiments the subjects had to direct their gaze to the screen center and simultaneously direct their attention to a peripheral light spot before the target for the saccade appeared.Many express saccades occurred when either active fixation of a central fixation point or attention directed to a peripheral visual target (regardless of its position) was interrupted 200 ms before the target for the saccade appeared.Express saccades were almost completely abolished in the presence of fixation and/or directed visual attention at the moment in which the saccade target appeared.We conclude that express saccades occur if visual attention has already been released at the moment when the target for the saccade appears. This disengagement needs some time which adds to the reaction time.

Human express saccades: effects of randomization and daily practice

SummaryWhen 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 (!)

Enhanced activation of neurons in prelunate cortex before visually guided saccades of trained rhesus monkeys

SummarySingle unit recording from trained rhesus monkeys demonstrate that the activity of the prelunate cortex is enhanced when a visual stimulus becomes a target of saccadic eye movement. As a rule, the enhancement is spatially selective: it does not occur if the animal makes an eye movement away from, rather than towards the stimulus. The results show that the prelunate cortex has access to an extraretinal signal which is activated in association with events preceding visually guided eye movements. Whether the signal reflects the initiation of eye movement or the animals interest in the stimulus, which he usually selects to initiate an eye movement, remains uncertain.