Bottom-up effects modulate saccadic latencies in well-known eye movement paradigm

A well-known eye movement paradigm combines saccades (fast eye movements) with a perceptual discrimination task. At a variable time after the onset of a central arrow cue indicating the target direction [the stimulus onset asynchrony (SOA)], discrimination symbols appear briefly at saccade target and non-target locations. A previous study revealed an unexpected effect of SOA on saccadic latencies: latencies were longer in trials with longer SOAs. It was suggested that this effect reflects a top-down process as observers may wait for the discrimination symbol to appear before executing saccades. However, symbol onsets may also modulate saccade latencies from the bottom-up. To clarify the origin of the SOA effect on latencies in this paradigm, we used a simplified version of the original task plus two new symbol onset conditions for comparison. The results indicate that the modulation of saccadic latencies was not due to a top-down strategy, but to a combination of two opposing bottom-up effects: the symbol onsets at the target location shortened saccade latencies, while symbol onsets at non-target locations lengthened saccade latencies.     

Strategic control over saccadic eye movements: studies of the fixation offset effect

We studied the strategic (presumably cortical) control of ocular fixation in experiments that measured the fixation offset effect (FOE) while manipulating readiness to make reflexive or voluntary eye movements. The visual grasp reflex, which generates reflexive saccades to peripheral visual signals, reflects an opponent process in the superior colliculus (SC) between fixation cells at the rostral pole, whose activity helps maintain ocular position and increases when a stimulus is present at fixation, and movement cells, which generate saccades and are inhibited by rostral fixation neurons. Voluntary eye movements are controlled by movement and fixation cells in the frontal eye field (FEF). The FOE--a decrease in saccade latency when the fixation stimulus is extinguished--has been shown to reflect activity in the collicular eye movement circuitry and also to have an activity correlate in the FEF. Our manipulation of preparatory set to make reflexive or voluntary eye movements showed that when reflexive saccades were frequent and voluntary saccades were infrequent, the FOE was attenuated only for reflexive saccades. When voluntary saccades were frequent and reflexive saccades were infrequent, the FOE was attenuated only for voluntary saccades. We conclude that cortical processes related to task strategy are able to decrease fixation neuron activity even in the presence of a fixation stimulus, resulting in a smaller FOE. The dissociation in the effects of a fixation stimulus on reflexive and voluntary saccade latencies under the same strategic set suggests that the FOEs for these two types of eye movements may reflect a change in cellular activity in different neural structures, perhaps in the SC for reflexive saccades and in the FEF for voluntary saccades.     

Control of reflexive and voluntary saccades in the gap effect

In two experiments, we examined whether voluntary and reflexive saccades shared a common fixation disengagement mechanism, Participants were required to perform a variety of tasks, each requiring a different level of information processing of the display prior to execution of the saccade. In Experiment 1, participants executed either a prosaccade or an antisaccade upon detecting a stimulus array. In Experiment 2, participants executed a prosaccade to a stimulus array only if the array contained a target item. The target could be a line (easy search) or a digit (difficult search). The critical manipulation in both experiments was the relative timing between the removal of the fixation stimulus and the onset of the stimulus array. In both experiments, it was found that saccadic latencies were shortest when the fixation stimulus was removed before the onset of the stimulus array—a gap effect. It was concluded that reflexive and voluntary saccades share a common fixation disengagement mechanism that is largely independent of higher level cognitive processes.     

Control' of reflexive and voluntary saccades in the gap effect.

In two experiments, we examined whether voluntary and reflexive saccades shared a common fixation disengagement mechanism. Participants were required to perform a variety of tasks, each requiring a different level of information processing of the display prior to execution of the saccade. In Experiment 1, participants executed either a prosaccade or an antisaccade upon detecting a stimulus array. In Experiment 2, participants executed a prosaccade to a stimulus array only if the array contained a target item. The target could be a line (easy search) or a digit (difficult search). The critical manipulation in both experiments was the relative timing between the removal of the fixation stimulus and the onset of the stimulus array. In both experiments, it was found that saccadic latencies were shortest when the fixation stimulus was removed before the onset of the stimulus array--a gap effect. It was concluded that reflexive and voluntary saccades share a common fixation disengagement mechanism that is largely independent of higher level cognitive processes.     

Neurophysiology and neuroanatomy of reflexive and volitional saccades: evidence from studies of humans

This review provides a summary of the contributions made by human functional neuroimaging studies to the understanding of neural correlates of saccadic control. The generation of simple visually guided saccades (redirections of gaze to a visual stimulus or pro-saccades) and more complex volitional saccades require similar basic neural circuitry with additional neural regions supporting requisite higher level processes. The saccadic system has been studied extensively in non-human (e.g., single-unit recordings) and human (e.g., lesions and neuroimaging) primates. Considerable knowledge of this system’s functional neuroanatomy makes it useful for investigating models of cognitive control. The network involved in pro-saccade generation (by definition largely exogenously-driven) includes subcortical (striatum, thalamus, superior colliculus, and cerebellar vermis) and cortical (primary visual, extrastriate, and parietal cortices, and frontal and supplementary eye fields) structures. Activation in these regions is also observed during endogenously-driven voluntary saccades (e.g., anti-saccades, ocular motor delayed response or memory saccades, predictive tracking tasks and anticipatory saccades, and saccade sequencing), all of which require complex cognitive processes like inhibition and working memory. These additional requirements are supported by changes in neural activity in basic saccade circuitry and by recruitment of additional neural regions (such as prefrontal and anterior cingulate cortices). Activity in visual cortex is modulated as a function of task demands and may predict the type of saccade to be generated, perhaps via top-down control mechanisms. Neuroimaging studies suggest two foci of activation within FEF - medial and lateral - which may correspond to volitional and reflexive demands, respectively. Future research on saccade control could usefully (i) delineate important anatomical subdivisions that underlie functional differences, (ii) evaluate functional connectivity of anatomical regions supporting saccade generation using methods such as ICA and structural equation modeling, (iii) investigate how context affects behavior and brain activity, and (iv) use multi-modal neuroimaging to maximize spatial and temporal resolution.     

Inhibitory inefficiency and failures of intention activation: age-related decline in the control of saccadic eye movements

Young and older adults' control of saccadic eye movements was compared using an antisaccade task, which requires the inhibition of a reflexive saccade toward a peripheral onset cue followed by an intentional saccade in the opposite direction. In 2 experiments, an age-related decline was found in the suppression of reflexive eye movements, as indicated by an increased proportion of saccades toward the cue, and a longer time needed to initiate correct antisaccades. The results from Experiment 2 suggested that older adults' slower antisaccades may be explained partly in terms of increased failures to maintain the cue-action representation at a sufficient activation level. The results suggest that the notion of selective preservation with age of the ability to inhibit spatial responses does not apply to the active inhibition of prepotent spatial responses.     

Neurophysiology and neuroanatomy of reflexive and volitional saccades: Evidence from studies of humans

This review provides a summary of the contributions made by human functional neuroimaging studies to the understanding of neural correlates of saccadic control. The generation of simple visually guided saccades (redirections of gaze to a visual stimulus or pro-saccades) and more complex volitional saccades require similar basic neural circuitry with additional neural regions supporting requisite higher level processes. The saccadic system has been studied extensively in non-human (e.g., single-unit recordings) and human (e.g., lesions and neuroimaging) primates. Considerable knowledge of this system’s functional neuroanatomy makes it useful for investigating models of cognitive control. The network involved in pro-saccade generation (by definition largely exogenously-driven) includes subcortical (striatum, thalamus, superior colliculus, and cerebellar vermis) and cortical (primary visual, extrastriate, and parietal cortices, and frontal and supplementary eye fields) structures. Activation in these regions is also observed during endogenously-driven voluntary saccades (e.g., anti-saccades, ocular motor delayed response or memory saccades, predictive tracking tasks and anticipatory saccades, and saccade sequencing), all of which require complex cognitive processes like inhibition and working memory. These additional requirements are supported by changes in neural activity in basic saccade circuitry and by recruitment of additional neural regions (such as prefrontal and anterior cingulate cortices). Activity in visual cortex is modulated as a function of task demands and may predict the type of saccade to be generated, perhaps via top-down control mechanisms. Neuroimaging studies suggest two foci of activation within FEF - medial and lateral - which may correspond to volitional and reflexive demands, respectively. Future research on saccade control could usefully (i) delineate important anatomical subdivisions that underlie functional differences, (ii) evaluate functional connectivity of anatomical regions supporting saccade generation using methods such as ICA and structural equation modeling, (iii) investigate how context affects behavior and brain activity, and (iv) use multi-modal neuroimaging to maximize spatial and temporal resolution.     

Saccade landing point selection and the competition account of pro- and antisaccade generation: the involvement of visual attention--a review

This paper presents a review and summary of experimental findings on the role of attention in the preparation of saccadic eye movements. The focus is on experiments where performance of prosaccades (saccades towards a suddenly appearing item) and antisaccades (saccades of equal amplitude in the direction opposite to where the target moved) is compared. Evidence suggests that these two opposite responses to the same stimulus event entail competition between neural pathways that generate reflexive movements to the target and neural mechanisms involved in inhibiting the reflex and generating a voluntary gaze shift in the opposite direction to the target appearance. Evidence for such a competition account is discussed in light of a large amount of experimental findings and the overall picture clearly indicates that this competition account has great explanatory power when data on saccadic reaction times and error rates are compared for the two types of saccade. The role of attention is also discussed in particular in light of the finding that the withdrawal of attention by a secondary task 200 to 500 ms before the saccade target appears, leads to speeded antisaccades (without a similar increase in error rates), showing that the results do not simply reflect a speed-accuracy trade-off. This result indicates that the tendency for "reflexive" prosaccades is diminished when attention is engaged in a different task. Furthermore, experiments are discussed that show that as the tendency for a reflexive prosaccade is weakened, antisaccades are speeded up, further supporting the competition account of pro- and antisaccade generation. In the light of evidence from neurophysiology of monkeys and humans, a tentative model of pro- and antisaccade generation is proposed.     

Effects of informative peripheral cues on eye movements: Revisiting William James’ “derived attention”

Two experiments examined effects of peripheral information on the latency of saccadic eye movements. In Experiment 1, simple target stimuli were presented to the left or right visual field. Prior to each target, a pair of cue letters was presented for 40msec bilaterally. The relative location of the letters (W-S or S-W) was related to target location, but participants were not informed of this contingency. After a brief practice period, saccadic latencies were faster for targets at the likely location, as indicated by the letter pair. This derived peripheral cueing effect was related to participants' awareness of the relation between cue type and target location. Experiments 2A and 2B employed monocular viewing in order to compare performance across the nasal and temporal visual fields. The effect observed in Experiment 1 was confined to the nasal visual field. In a reflexive orienting condition, the effect of a unilateral letter cue was larger in the temporal visual field. It is concluded that the neurocognitive processes responsible for derived peripheral cueing are distinct from those involved in either reflexive or voluntary orienting.     

Saccadic Eye Movements in Parkinson's Disease: I. Delayed Saccades

The saccadic eye movements of nine patients with Parkinson's disease were compared to those of nine age-matched controls in two paradigms generating volitional saccades. In both paradigms, subjects had to make delayed saccades to peripheral LED targets: a peripheral target appeared 700 msec before a buzzer sounded, the buzzer being the signal to make a saccade to the target. In the first paradigm (“centre-off”), the fixation target was extinguished simultaneously with buzzer onset. In the second (“centre-remain”) it was not extinguished until 1000 msec later. The results showed that for outward saccades in both paradigms, there was no difference between Parkinsonian patients and controls, but saccadic latencies were significantly shorter in the “centre-remain” paradigm. The initial outward saccades were indistinguishable from the normal, reflex saccades of the same subjects. However, saccades returning to the centre (a type of remembered target saccade) were hypometric and showed multistepping. Both effects were more pronounced in patients with Parkinson's disease. The significance of these findings in terms of current hypotheses about the nature of the Parkinsonian saccadic deficit is discussed.     

The Role of Emotional Content and Perceptual Saliency During the Programming of Saccades Toward Faces

Previous studies have shown that the human visual system can detect a face and elicit a saccadic eye movement toward it very efficiently compared to other categories of visual stimuli. In the first experiment, we tested the influence of facial expressions on fast face detection using a saccadic choice task. Face-vehicle pairs were simultaneously presented and participants were asked to saccade toward the target (the face or the vehicle). We observed that saccades toward faces were initiated faster, and more often in the correct direction, than saccades toward vehicles, regardless of the facial expressions (happy, fearful, or neutral). We also observed that saccade endpoints on face images were lower when the face was happy and higher when it was neutral. In the second experiment, we explicitly tested the detection of facial expressions. We used a saccadic choice task with emotional-neutral pairs of faces and participants were asked to saccade toward the emotional (happy or fearful) or the neutral face. Participants were faster when they were asked to saccade toward the emotional face. They also made fewer errors, especially when the emotional face was happy. Using computational modeling, we showed that this happy face advantage can, at least partly, be explained by perceptual factors. Also, saccade endpoints were lower when the target was happy than when it was fearful. Overall, we suggest that there is no automatic prioritization of emotional faces, at least for saccades with short latencies, but that salient local face features can automatically attract attention.     

反向眼跳的实验范式、机制及影响因素

反向眼跳任务是研究内源性眼跳的主要方法。1978年,Hallett在研究中首次使用了反向眼跳的实验任务。实验中要求被试抑制对外围目标的注视,并注视它的相反位置。反向眼跳任务是研究行为控制以及注意功能的有效范式。目前认为反向眼跳任务中的朝向眼跳和反向眼跳计划是同时加工并相互竞争的,并且反向眼跳的产生与额顶叶皮层下组织有关。反向眼跳会受到多种因素的影响,例如,空白效应、工作记忆、认知老化、目标离心率等。     

Age-group differences in inhibiting an oculomotor response

Age-group differences were examined in the delayed oculomotor response task, which requires that observers delay the execution of a saccade (eye movement) toward an abrupt-onset visual cue. This task differs from antisaccade and attentional capture in that inhibition causes saccades to be postponed, not redirected. Older adults executed more premature saccades than young adults, but there were no age-group differences in latency or accuracy of saccades executed at the proper time. The results suggest that older adults are less capable of inhibiting a prepotent saccadic response, but that other aspects of visual working memory related to the task are preserved.     

Age-group Differences in Inhibiting an Oculomotor Response

ABSTRACT

Age-group differences were examined in the delayed oculomotor response task, which requires that observers delay the execution of a saccade (eye movement) toward an abrupt-onset visual cue. This task differs from antisaccade and attentional capture in that inhibition causes saccades to be postponed, not redirected. Older adults executed more premature saccades than young adults, but there were no age-group differences in latency or accuracy of saccades executed at the proper time. The results suggest that older adults are less capable of inhibiting a prepotent saccadic response, but that other aspects of visual working memory related to the task are preserved.     

Averaging saccades are repelled by prior uninformative cues at both short and long intervals

When two spatially proximal stimuli are presented simultaneously, a first saccade is often directed to an intermediate location between the stimuli (averaging saccade). In an earlier study, Watanabe (2001) showed that, at a long cue–target onset asynchrony (CTOA; 600 ms), uninformative cues not only slowed saccadic response times (SRTs) to targets presented at the cued location in single target trials (inhibition of return, IOR), but also biased averaging saccades away from the cue in double target trials. The present study replicated Watanabe's experimental task with a short CTOA (50 ms), as well as with mixed short (50 ms) and long (600 ms) CTOAs. In all conditions on double target trials, uninformative cues robustly biased averaging saccades away from cued locations. Although SRTs on single target trials were delayed at previously cued locations at both CTOAs when they were mixed, this delay was not observed in the blocked, short CTOA condition. We suggest that top-down factors, such as expectation and attentional control settings, may have asymmetric effects on the temporal and spatial dynamics of oculomotor processing.     

Saccadic eye movements as indicators of cognitive function in older adults

Older adults appear to have greater difficulty ignoring distractions during day-to-day activities than younger adults. To assess these effects of age, the ability of adults aged between 50 and 80 years to ignore distracting stimuli was measured using the antisaccade and oculomotor capture tasks. In the antisaccade task, observers are instructed to look away from a visual cue, whereas in the oculomotor capture task, observers are instructed to look toward a colored singleton in the presence of a concurrent onset distractor. Index scores of the Repeatable Battery for the Assessment of Neuropsychological Status (RBANS) were compared with capture errors, and with prosaccade errors on the antisaccade task. A higher percentage of capture errors were made on the oculomotor capture tasks by the older members of the cohort compared to the younger members. There was a weak relationship between the attention index and capture errors, but the visuospatial/constructional index was the strongest predictor of prosaccade error rate in the antisaccade task. The saccade reaction times (SRTs) of correct initial saccades in the oculomotor capture task were poorly correlated with age, and with the neurospsychological tests, but prosaccade SRTs in both tasks moderately correlated with antisaccade error rate. These results were interpreted in terms of a competitive integration (or race) model. Any variable that reduces the strength of the top-down neural signal to produce a voluntary saccade, or that increases saccade speed, will enhance the likelihood that a reflexive saccade to a stimulus with an abrupt onset will occur.     

Enhanced saccadic control in young people with Tourette syndrome despite slowed pro‐saccades

Tourette syndrome (TS) is a neurodevelopmental disorder characterized by motor and vocal tics. Tics are repetitive and uncontrolled behaviours that have been associated with basal ganglia dysfunction. We investigated saccadic eye movements in a group of young people with TS but without co‐morbid ADHD. Participants performed two tasks. One required them to perform only pro‐saccade responses (pure pro‐saccade task). The other involved shifting, unpredictably, between executing pro‐ and anti‐saccades (mixed saccade task). We show that in the mixing saccade task, the TS group makes significantly fewer errors than an age‐matched control group, while responding equally fast. By contrast, on the pure pro‐saccade task, the TS group were shown to be significantly slower to initiate and to complete the saccades (longer movement duration and decreased peak velocity) than controls, while movement amplitude and direction accuracy were not different. These findings demonstrate enhanced shifting ability despite slower reflexive responding in TS and are discussed with respect to a disorder‐related adaptation for increased cognitive regulation of behaviour.     

Quantifying the performance limits of human saccadic targeting during visual search.

In previous studies of saccadic targeting, the issue how visually guided saccades to unambiguous targets are programmed and executed has been examined. These studies have found different degrees of guidance for saccades depending on the task and task difficulty. In this study, we use ideal-observer analysis to estimate the visual information used for the first saccade during a search for a target disk in noise. We quantitatively compare the performance of the first saccadic decision to that of the ideal observer (ie absolute efficiency of the first saccade) and to that of the associated final perceptual decision at the end of the search (ie relative efficiency of the first saccade). Our results show, first, that at all levels of salience tested, the first saccade is based on visual information from the stimulus display, and its highest absolute efficiency is approximately 20%. Second, the efficiency of the first saccade is lower than that of the final perceptual decision after active search (with eye movements) and has a minimum relative efficiency of 19% at the lowest level of saliency investigated. Third, we found that requiring observers to maintain central fixation (no saccades allowed) decreased the absolute efficiency of their perceptual decision by up to a factor of two, but that the magnitude of this effect depended on target salience. Our results demonstrate that ideal-observer analysis can be extended to measure the visual information mediating saccadic target-selection decisions during visual search, which enables direct comparison of saccadic and perceptual efficiencies.     

Delayed oculomotor inhibition in patients with lesions to the human frontal oculomotor cortex: Evidence from a study on saccade averaging

The frontal oculomotor cortex is known to play an important role in oculomotor selection. The aim of the current study was to examine whether previously observed findings concerning the role of the frontal oculomotor cortex in the speed of saccade initiation and oculomotor inhibition might be related to a common underlying role of these areas in oculomotor selection. To this end, six patients with lesions to the frontal oculomotor cortex performed a double stimulus paradigm in which two elements were presented simultaneously in close proximity. Patients performed a block in which no specific task instruction was given and a block in which an instruction was provided about which of the two elements was the target. The rationale behind this manipulation was that the introduction of a specific task instruction would require a stronger involvement of top-down factors. In contrast to the block without a specific task instruction, saccade latencies to the contralesional visual field were longer than the ipsilesional visual field when a task instruction was given. This effect was strongest for saccades that landed away from the target and the distractor, reflecting trials in which strong oculomotor inhibition was applied. The observed deficits can be explained in terms of a slowing of the inhibitory signals associated with the rejection of a distractor. Given the known role of the Frontal Eye Fields and the location of the lesions, we attribute these findings to the Frontal Eye Fields, revealing their important role in the voluntary control of eye movements.     

Programming saccadic eye movements

This article addresses questions about the preparatory processes that immediately precede saccadic eye movements. Saccade latencies were measured in a task in which subjects were provided partial advance information about the spatial location of a target fixation. In one experiment, subjects were faster in initiating saccades when they knew either the direction or amplitude of the required movement in advance compared to a condition with equal uncertainty about the number of potential saccade targets but without knowledge of the parameters required to execute the movement. These results suggest that the direction and amplitude for an upcoming saccade were calculated separately, and not in a fixed serial order. In another experiment, subjects appear to have programmed the saccades more holistically--with computations of direction and amplitude parameters occurring simultaneously. The implications of these results for models of eye movement preparation are discussed.