Fixation disengagement enhances peripheral perceptual processing: evidence for a perceptual gap effect

Temporal gaps between the offset of a central fixation stimulus and the onset of an eccentric target typically reduce saccade latencies (saccadic gap effect). Here, we test whether temporal gaps also affect perceptual performance in peripheral vision. In Experiment 1, subjects executed saccades to briefly presented peripheral target letters and reported letter identity afterwards. A central fixation stimulus either remained visible throughout the trial (overlap) or disappeared 200 ms before letter onset (gap). Experiment 2 tested perceptual performance without saccade execution, whereas Experiment 3 tested saccade execution without perceptual demands. Peripheral letter perception performance was enhanced in gap as compared to overlap conditions (perceptual gap effect) irrespective of concurrent oculomotor demands. Furthermore, the saccadic gap effect was modulated by concurrent perceptual demands. Experiment 4 ruled out a general warning explanation of the perceptual gap effect. These findings extend recent theories assuming a strong coupling between the preparation of goal-directed saccades and shifts of visual attention from the spatial to the temporal domain.     

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.     

Event-related potentials and saccadic reaction times: effects of fixation point offset or change

Previous studies have shown that saccadic reaction times (SRTs) are reduced if the initial fixation point (FP) disappears 200 ms (gap period) before a peripheral target is presented. This gap saccade task is associated with a negative cortical potential at the end of the gap period. To determine whether the neural processes underlying this potential account for the reduction of SRTs during gap saccade tasks, we recorded event-related potentials (ERPs) in 19 subjects performing a gap saccade task (gap duration 200 ms), a warning saccade task (the color of the FP changed 200 ms prior to target appearance) and an overlap task (the FP remained visible during the trial). SRTs were shortest during the gap task, longest during the overlap task and intermediate during the warning task. The gap and warning tasks were accompanied by the same widespread negative cortical potential with a maximum at the time of stimulus presentation. These findings indicate that the warning effect mediated by the disappearance of the FP during gap saccade tasks is responsible for the gap negativity which was observed by several authors. Our findings of shorter SRTs during the gap task than the warning task, however, suggest that the gap has an additional effect that probably depends on subcortical mechanisms. Received: 01 June 1998 / Accepted: 12 March 1999     

Look–don’t look! How emotional pictures affect pro- and anti-saccades

We investigated the effect of emotional target content on the generation of pro- and anti-saccades. Subjects had to generate saccades towards (pro-saccade) or away from (anti-saccade) peripherally presented pleasant, unpleasant or neutral pictures. Two different SOAs were used, either with simultaneous fixation offset and target onset (no gap) or with fixation offset preceding target onset by 200 ms (gap). In the pro-saccade task participants were faster to respond to emotional pictures in the left visual field. In the right visual field facilitation occurred only for pleasant pictures and saccadic reaction times towards unpleasant pictures were slowed. In the anti-saccade task more anti-saccade errors towards emotional pictures (pleasant and unpleasant) were made in the gap condition. On the whole, endogenous saccade generation appears facilitated by emotional target content, probably via increased input from extra-striate and parietal brain areas to the superior colliculus. Moderating factors such as the SOA or the visual field of presentation are discussed.     

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.     

Spatio-temporal contingency of saccade-induced chronostasis

During fast, saccadic eye movements visual perception is suppressed. This saccadic suppression prevents erroneous and distracting motion percepts resulting from saccade induced retinal slip. Although saccadic suppression occurs over a substantial time interval around the saccade, there is no “perceptual gap” during saccades. The mechanisms underlying this temporal perceptual filling-in are unknown. When subjects are asked to perform temporal interval judgements of stimuli presented at the time of saccades, the time interval following the termination of the saccade appears longer than subsequent intervals of identical length. This illusion is known as “chronostasis”, because a clock presented at the saccade target seemingly stops for a moment. We test whether chronostasis is a global mechanism that may compensate for the temporal gap associated with saccadic suppression. We show that a clock positioned halfway between the initial fixation point and the saccade target does not exhibit prolongation of the interval following the saccade. The characteristical distortion of temporal perception occurred only in the case of a clock being located at the saccade target. This result suggests a local, object-specific mechanism underlying the stopped clock illusion that might originate from a shift in attention immediately preceding the eye movement.     

Express saccades in cat: effects of task and target modality

Saccadic eye movements to visual, auditory, and bimodal targets were measured in four adult cats. Bimodal targets were visual and auditory stimuli presented simultaneously at the same location. Three behavioral tasks were used: a fixation task and two saccadic tracking tasks (gap and overlap task). In the fixation task, a sensory stimulus was presented at a randomly selected location, and the saccade to fixate that stimulus was measured. In the gap and overlap tasks, a second target (hereafter called the saccade target) was presented after the cat had fixated the first target. In the gap task, the fixation target was switched off before the saccade target was turned on; in the overlap task, the saccade target was presented before the fixation target was switched off. All tasks required the cats to redirect their gaze toward the target (within a specified degree of accuracy) within 500 ms of target onset, and in all tasks target positions were varied randomly over five possible locations along the horizontal meridian within the cat's oculomotor range. In the gap task, a significantly greater proportion of saccadic reaction times (SRTs) were less than 125 ms, and mean SRTs were significantly shorter than in the fixation task. With visual targets, saccade latencies were significantly shorter in the gap task than in the overlap task, while, with bimodal targets, saccade latencies were similar in the gap and overlap tasks. On the fixation task, SRTs to auditory targets were longer than those to either visual or bimodal targets, but on the gap task, SRTs to auditory targets were shorter than those to visual or bimodal targets. Thus, SRTs reflected an interaction between target modality and task. Because target locations were unpredictable, these results demonstrate that cats, as well as primates, can produce very short latency goal-directed saccades.     

Evidence for interactions between target selection and visual fixation for saccade generation in humans

We examined the processes controlling selective orientation, specifically the processes required for generating saccadic eye movements in humans. Before a saccadic eye movement can be initiated, active visual fixation must be disengaged from the current point of fixation and a new target selected. We investigated whether these neural processes occur independently or interactively by devising a simple, multimodal choice reaction task in which subjects were asked to direct their gaze away from a central visual fixation target to an eccentric visual target while ignoring a simultaneous auditory distractor. Subjects had more difficulty suppressing incorrect movements toward the distractor when the fixation target was extinguished prior to onset of the eccentric target than when the fixation target remained illuminated during eccentric target presentation. Subjects with the shortest saccadic reaction times produced the most incorrect movements. These results support a recent hypothesis suggesting that the processes of disengaging active visual fixation and selecting a new saccade target are interrelated and arise, at least in part, from a change of activity within the superior colliculus.     

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.     

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.     

Influence of previous visual stimulus or saccade on saccadic reaction times in monkey.

Influence of previous visual stimulus or saccade on saccadic reaction times in monkey. Saccadic reaction times (SRTs) to suddenly appearing targets are influenced by neural processes that occur before and after target presentation. The majority of previous studies have focused on how posttarget factors, such as target attributes or changes in task complexity, affect SRTs. Studies of pretarget factors have focused on how prior knowledge of the timing or location of the impending target, gathered through cueing or probabilistic information, affects SRTs. Our goal was to investigate additional pretarget factors to determine whether SRTs can also be influenced by the history of saccadic and visual activity even when these factors are spatially unpredictive as to the location of impending saccadic targets. Monkeys were trained on two paradigms. In the saccade-saccade paradigm, monkeys were required to follow a saccadic target that stepped from a central location, to an eccentric location, back to center, and finally to a second eccentric location. The stimulus-saccade paradigm was similar, except the central fixation target remained illuminated during presentation of the first eccentric stimulus; the monkey was required to maintain central fixation and to make a saccade to the second eccentric stimulus only on disappearance of the fixation point. In both paradigms, the first eccentric stimulus was presented at the same, opposite, or orthogonal location with respect to the final target location in a given trial. We measured SRTs to the final target under conditions in which all parameters were identical except for the location of the first eccentric stimulus. In the saccade-saccade paradigm, we found that the SRT to the final target was slowest when it was presented opposite to the initial saccadic target, whereas in the stimulus-saccade paradigm the SRT to the final target was slowest when it was presented at the same location as the initial stimulus. In both paradigms, these increases in SRTs were greatest during the shortest intervals between presentation of successive eccentric stimuli, yet these effects remained present for the longest intervals employed in this study. SRTs became faster as the direction and eccentricity of the two successive stimuli became increasingly misaligned from that which produced the maximal SRT slowing in each paradigm. The results of the stimulus-saccade paradigm are similar to the phenomenon of inhibition of return (IOR) in which human subjects are slower to respond to stimuli that are presented at previously cued locations. We interpret these findings in terms of overlapping representations of visuospatial and oculomotor activity in the same neural structures.     

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.     

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.     

Saccadic eye movements to visual and auditory targets

 Recent neurophysiological studies of the saccadic ocular motor system have lent support to the hypothesis that this system uses a motor error signal in retinotopic coordinates to direct saccades to both visual and auditory targets. With visual targets, the coordinates of the sensory and motor error signals will be identical unless the eyes move between the time of target presentation and the time of saccade onset. However, targets from other modalities must undergo different sensory-motor transformations to access the same motor error map. Because auditory targets are initially localized in head-centered coordinates, analyzing the metrics of saccades from different starting positions allows a determination of whether the coordinates of the motor signals are those of the sensory system. We studied six human subjects who made saccades to visual or auditory targets from a central fixation point or from one at 10° to the right or left of the midline of the head. Although the latencies of saccades to visual targets increased as stimulus eccentricity increased, the latencies of saccades to auditory targets decreased as stimulus eccentricity increased. The longest auditory latencies were for the smallest values of motor error (the difference between target position and fixation eye position) or desired saccade size, regardless of the position of the auditory target relative to the head or the amplitude of the executed saccade. Similarly, differences in initial eye position did not affect the accuracy of saccades of the same desired size. When saccadic error was plotted as a function of motor error, the curves obtained at the different fixation positions overlapped completely. Thus, saccadic programs in the central nervous system compensated for eye position regardless of the modality of the saccade target, supporting the hypothesis that the saccadic ocular motor system uses motor error signals to direct saccades to auditory targets. Received: 8 September 1995 / Accepted: 22 November 1996     

JN403, in vitro characterization of a novel nicotinic acetylcholine receptor alpha7 selective agonist

Concussion, or mild traumatic brain injury (mTBI), leads to a number of cognitive, attentional, and sensorimotor deficits that can last a surprisingly long time after the initial injury. We have previously shown that the ability to orient visuospatial attention is deficient in participants with mTBI within 2 days of their injury, but then recovers to normal levels within a week. Orienting attention requires disengagement from the point of fixation, movement of attention to the location of interest, and re-engagement at that location. Deficits in any or all of these processes could lead to the difficulties with orienting attention that we have observed in mTBI. To address this issue, we tested participants with mTBI using a gap saccade task. Because this task manipulates the temporal gap between the offset of the fixation target and the appearance of the peripheral saccade target, it isolates the contribution of the disengagement process to saccadic reaction time. We found that participants with mTBI had significantly longer saccadic reaction times than controls when the temporal gap was short but not when it was long. This gap-dependent difference in saccadic reaction time was present within 2 days of the injury and resolved within 1 week. This pattern of results suggests that as the contribution of the disengagement process is reduced, so too is the extent of the reaction time deficit in the participants with mTBI. Taken together, this is consistent with the idea that the deficits in orienting visuospatial attention in participants with mTBI are fully accounted for by difficulties with the initial disengagement process.     

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.     

Reaction time latencies of eye and hand movements in single- and dual-task conditions

The goal of this study was to investigate whether ocular and hand motor systems operate independently or whether they share processes. Using dualtask methodology, reaction time (RT) latencies of saccadic eye and hand motor responses were measured. In experiment 1, the hand and eye motor systems produced rapid, aimed pointing movements to a visual target, which could occur either to the left or right of a central fixation point. Results showed that RT latencies of the eye response were slower in the dual-task condition than in the single-task condition, whereas the RT latencies of the hand response were virtually the same in both conditions. This interference effect indicated that the ocular and manual motor systems are not operating independently when initiating saccadic eye and goal-directed hand movements. Experiment 2 employed the same experimental paradigm as experiment 1, except for one important modification. Instead of a goal-directed hand movement to the target stimulus, subjects had to make a button-press response with either the index or middle finger of the right hand dependent upon whether the stimulus occurred to the right or left of the control fixation point. The aim of experiment 2 was to investigate the issue whether the observed interference effect in experiment 1 was specific or non-specific (e.g. overhead costs due to coordinating any two responses). The finding that saccadic eye movements and button-press responses in the dual-task condition could be initiated without delay relative to the single-task conditions, supports the specific interference interpretation.     

Altered control of visual fixation and saccadic eye movements in attention-deficit hyperactivity disorder

Attention-deficit hyperactivity disorder (ADHD) is characterized by the overt symptoms of impulsiveness, hyperactivity, and inattention. A frontostriatal pathophysiology has been hypothesized to produce these symptoms and lead to reduced ability to inhibit unnecessary or inappropriate behavioral responses. Oculomotor tasks can be designed to probe the ability of subjects to generate or inhibit reflexive and voluntary responses. Because regions of the frontal cortex and basal ganglia have been identified in the control of voluntary responses and saccadic suppression, we hypothesized that children and adults diagnosed with ADHD may have specific difficulties in oculomotor tasks requiring the suppression of reflexive or unwanted saccadic eye movements. To test this hypothesis, we measured eye movement performance in pro- and anti-saccade tasks of 114 ADHD and 180 control participants ranging in age from 6 to 59 yr. In the pro-saccade task, participants were instructed to look from a central fixation point toward an eccentric visual target. In the anti-saccade task, stimulus presentation was identical, but participants were instructed to suppress the saccade to the stimulus and instead look from the central fixation point to the side opposite the target. The state of fixation was manipulated by presenting the target either when the central fixation point was illuminated (overlap condition) or at some time after it disappeared (gap condition). In the pro-saccade task, ADHD participants had longer reaction times, greater intra-subject variance, and their saccades had reduced peak velocities and increased durations. In the anti-saccade task, ADHD participants had greater difficulty suppressing reflexive pro-saccades toward the eccentric target, increased reaction times for correct anti-saccades, and greater intra-subject variance. In a third task requiring prolonged fixation, ADHD participants generated more intrusive saccades during periods when they were required to maintain steady fixation. The results suggest that ADHD participants have reduced ability to suppress unwanted saccades and control their fixation behavior voluntarily, a finding that is consistent with a fronto-striatal pathophysiology. The findings are discussed in the context of recent neurophysiological data from nonhuman primates that have identified important control signals for saccade suppression that emanate from frontostriatal circuits.     

Differences in intersaccadic adaptation transfer between inward and outward adaptation

Saccadic adaptation is a mechanism to increase or decrease the amplitude gain of subsequent saccades, if a saccade is not on target. Recent research has shown that the mechanism of gain increasing, or outward adaptation, and the mechanism of gain decreasing, or inward adaptation, rely on partly different processes. We investigate how outward and inward adaptation of reactive saccades transfer to other types of saccades, namely scanning, overlap, memory-guided, and gap saccades. Previous research has shown that inward adaptation of reactive saccades transfers only partially to these other saccade types, suggesting differences in the control mechanisms between these saccade categories. We show that outward adaptation transfers stronger to scanning and overlap saccades than inward adaptation, and that the strength of transfer depends on the duration for which the saccade target is visible before saccade onset. Furthermore, we show that this transfer is mainly driven by an increase in saccade duration, which is apparent for all saccade categories. Inward adaptation, in contrast, is accompanied by a decrease in duration and in peak velocity, but only the peak velocity decrease transfers from reactive saccades to other saccade categories, i.e., saccadic duration remains constant or even increases for test saccades of the other categories. Our results, therefore, show that duration and peak velocity are independent parameters of saccadic adaptation and that they are differently involved in the transfer of adaptation between saccade categories. Furthermore, our results add evidence that inward and outward adaptation are different processes.     

The gap effect and express saccades in the auditory modality

Latencies of eye movements to peripheral targets are reduced when there is a short delay (typically 200 ms) between the offset of a central visual fixation point and the target onset. This has been termed the gap effect. In addition, some subjects, usually with practice, exhibit a separate population of very short latency saccades, called express saccades. Both these phenomena have been attributed to disengagement of visual attention when the fixation point is extinguished. A competing theory of the gap effect attributes it to disengagement of oculomotor fixation during the temporal gap. It is known that auditory targets are effective in eliciting saccadic eye movements, and also that covert attention operates in the auditory modality. If the gap effect and express saccades are due to disengagement of spatial attention, both should persist in the auditory modality. However, fixation of gaze is largely under visual control. If the gap effect results from disengagement of fixation, then at least a reduced effect should be seen in the auditory modality. Human subjects performed the gap task and a control task in the dark, using auditory fixation points and saccadic targets, on five successive days. Despite this practice, express saccades were not observed. There was a reliable gap effect, but the reduction in saccadic latency was only 17 ms, compared with 32 ms for the same subjects in the visual modality. This suggests that about half the gap effect is due to disengagement of visual fixation. The remainder was not due to non-specific warning effects and could be attributed to offset of the auditory fixation stimulus. Received: 1 March 1996 / Accepted: 11 July 1997