Oculomotor evidence for top-down control following the initial saccade

The goal of the current study was to investigate how salience-driven and goal-driven processes unfold during visual search over multiple eye movements. Eye movements were recorded while observers searched for a target, which was located on (Experiment 1) or defined as (Experiment 2) a specific orientation singleton. This singleton could either be the most, medium, or least salient element in the display. Results were analyzed as a function of response time separately for initial and second eye movements. Irrespective of the search task, initial saccades elicited shortly after the onset of the search display were primarily salience-driven whereas initial saccades elicited after approximately 250 ms were completely unaffected by salience. Initial saccades were increasingly guided in line with task requirements with increasing response times. Second saccades were completely unaffected by salience and were consistently goal-driven, irrespective of response time. These results suggest that stimulus-salience affects the visual system only briefly after a visual image enters the brain and has no effect thereafter.     

Error Correcting Mechanisms during Antisaccades: Contribution of Online Control during Primary Saccades and Offline Control via Secondary Saccades

Errors in eye movements can be corrected during the ongoing saccade through in-flight modifications (i.e., online control), or by programming a secondary eye movement (i.e., offline control). In a reflexive saccade task, the oculomotor system can use extraretinal information (i.e., efference copy) online to correct errors in the primary saccade, and offline retinal information to generate a secondary corrective saccade. The purpose of this study was to examine the error correction mechanisms in the antisaccade task. The roles of extraretinal and retinal feedback in maintaining eye movement accuracy were investigated by presenting visual feedback at the spatial goal of the antisaccade. We found that online control for antisaccade is not affected by the presence of visual feedback; that is whether visual feedback is present or not, the duration of the deceleration interval was extended and significantly correlated with reduced antisaccade endpoint error. We postulate that the extended duration of deceleration is a feature of online control during volitional saccades to improve their endpoint accuracy. We found that secondary saccades were generated more frequently in the antisaccade task compared to the reflexive saccade task. Furthermore, we found evidence for a greater contribution from extraretinal sources of feedback in programming the secondary “corrective” saccades in the antisaccade task. Nonetheless, secondary saccades were more corrective for the remaining antisaccade amplitude error in the presence of visual feedback of the target. Taken together, our results reveal a distinctive online error control strategy through an extension of the deceleration interval in the antisaccade task. Target feedback does not improve online control, rather it improves the accuracy of secondary saccades in the antisaccade task.     

Reading and Visual Search: A Developmental Study in Normal Children

Studies dealing with developmental aspects of binocular eye movement behaviour during reading are scarce. In this study we have explored binocular strategies during reading and during visual search tasks in a large population of normal young readers. Binocular eye movements were recorded using an infrared video-oculography system in sixty-nine children (aged 6 to 15) and in a group of 10 adults (aged 24 to 39). The main findings are (i) in both tasks the number of progressive saccades (to the right) and regressive saccades (to the left) decreases with age; (ii) the amplitude of progressive saccades increases with age in the reading task only; (iii) in both tasks, the duration of fixations as well as the total duration of the task decreases with age; (iv) in both tasks, the amplitude of disconjugacy recorded during and after the saccades decreases with age; (v) children are significantly more accurate in reading than in visual search after 10 years of age. Data reported here confirms and expands previous studies on children''s reading. The new finding is that younger children show poorer coordination than adults, both while reading and while performing a visual search task. Both reading skills and binocular saccades coordination improve with age and children reach a similar level to adults after the age of 10. This finding is most likely related to the fact that learning mechanisms responsible for saccade yoking develop during childhood until adolescence.     

Very Slow Search and Reach: Failure to Maximize Expected Gain in an Eye-Hand Coordination Task

We examined an eye-hand coordination task where optimal visual search and hand movement strategies were inter-related. Observers were asked to find and touch a target among five distractors on a touch screen. Their reward for touching the target was reduced by an amount proportional to how long they took to locate and reach to it. Coordinating the eye and the hand appropriately would markedly reduce the search-reach time. Using statistical decision theory we derived the sequence of interrelated eye and hand movements that would maximize expected gain and we predicted how hand movements should change as the eye gathered further information about target location. We recorded human observers'' eye movements and hand movements and compared them with the optimal strategy that would have maximized expected gain. We found that most observers failed to adopt the optimal search-reach strategy. We analyze and describe the strategies they did adopt.     

Saccadic eye movements minimize the consequences of motor noise

The durations and trajectories of our saccadic eye movements are remarkably stereotyped. We have no voluntary control over these properties but they are determined by the movement amplitude and, to a smaller extent, also by the movement direction and initial eye orientation. Here we show that the stereotyped durations and trajectories are optimal for minimizing the variability in saccade endpoints that is caused by motor noise. The optimal duration can be understood from the nature of the motor noise, which is a combination of signal-dependent noise favoring long durations, and constant noise, which prefers short durations. The different durations of horizontal vs. vertical and of centripetal vs. centrifugal saccades, and the somewhat surprising properties of saccades in oblique directions are also accurately predicted by the principle of minimizing movement variability. The simple and sensible principle of minimizing the consequences of motor noise thus explains the full stereotypy of saccadic eye movements. This suggests that saccades are so stereotyped because that is the best strategy to minimize movement errors for an open-loop motor system.     

Immaturity of the oculomotor saccade and vergence interaction in dyslexic children: evidence from a reading and visual search study

Studies comparing binocular eye movements during reading and visual search in dyslexic children are, at our knowledge, inexistent. In the present study we examined ocular motor characteristics in dyslexic children versus two groups of non dyslexic children with chronological/reading age-matched. Binocular eye movements were recorded by an infrared system (mobileEBT®, e(ye)BRAIN) in twelve dyslexic children (mean age 11 years old) and a group of chronological age-matched (N = 9) and reading age-matched (N = 10) non dyslexic children. Two visual tasks were used: text reading and visual search. Independently of the task, the ocular motor behavior in dyslexic children is similar to those reported in reading age-matched non dyslexic children: many and longer fixations as well as poor quality of binocular coordination during and after the saccades. In contrast, chronological age-matched non dyslexic children showed a small number of fixations and short duration of fixations in reading task with respect to visual search task; furthermore their saccades were well yoked in both tasks. The atypical eye movement''s patterns observed in dyslexic children suggest a deficiency in the visual attentional processing as well as an immaturity of the ocular motor saccade and vergence systems interaction.     

Eye-Head Coordination for Visual Cognitive Processing

We investigated coordinated movements between the eyes and head (“eye-head coordination”) in relation to vision for action. Several studies have measured eye and head movements during a single gaze shift, focusing on the mechanisms of motor control during eye-head coordination. However, in everyday life, gaze shifts occur sequentially and are accompanied by movements of the head and body. Under such conditions, visual cognitive processing influences eye movements and might also influence eye-head coordination because sequential gaze shifts include cycles of visual processing (fixation) and data acquisition (gaze shifts). In the present study, we examined how the eyes and head move in coordination during visual search in a large visual field. Subjects moved their eyes, head, and body without restriction inside a 360° visual display system. We found patterns of eye-head coordination that differed those observed in single gaze-shift studies. First, we frequently observed multiple saccades during one continuous head movement, and the contribution of head movement to gaze shifts increased as the number of saccades increased. This relationship between head movements and sequential gaze shifts suggests eye-head coordination over several saccade-fixation sequences; this could be related to cognitive processing because saccade-fixation cycles are the result of visual cognitive processing. Second, distribution bias of eye position during gaze fixation was highly correlated with head orientation. The distribution peak of eye position was biased in the same direction as head orientation. This influence of head orientation suggests that eye-head coordination is involved in gaze fixation, when the visual system processes retinal information. This further supports the role of eye-head coordination in visual cognitive processing.     

Stimulus-driven and voluntary saccades are coded in different coordinate systems

We make fast, "saccadic" eye movements to view our surroundings, "voluntary" saccades when saccade targets are deliberately selected, and "stimulus-driven" saccades when a target suddenly appears. Saccades of patients with spatial neglect have been studied to identify the coordinate systems guiding such behavior. However, previous reports disagree on whether neglect involves an eye-centered deficit of (delayed and hypometric) saccades specifically when performed in the direction opposite the brain lesion or not. We show that this inconsistency is due to independent mechanisms underlying voluntary and stimulus-driven saccades. We used a new experimental procedure comparing identical saccades performed either during an exploratory search task or a stimulus-driven task, both of which required similar cognitive functions (Figure 1). Only the patients' stimulus-driven saccades showed the eye-centered deficit. The same saccades were intact when voluntarily performed. However, here the patients showed a head-centered deficit; their saccades ignored the left part of space. In none of our control subjects with or without brain lesions did the neglect patients' pattern of deficits occur. The results argue that the brain flexibly uses a system of distinct but interrelated neural circuits for visual orienting to optimally encode its sensorimotor functions in multiple behavioral situations.     

Goal-related activity in V4 during free viewing visual search. Evidence for a ventral stream visual salience map

Natural exploration of complex visual scenes depends on saccadic eye movements toward important locations. Saccade targeting is thought to be mediated by a retinotopic map that represents the locations of salient features. In this report, we demonstrate that extrastriate ventral area V4 contains a retinotopic salience map that guides exploratory eye movements during a naturalistic free viewing visual search task. In more than half of recorded cells, visually driven activity is enhanced prior to saccades that move the fovea toward the location previously occupied by a neuron's spatial receptive field. This correlation suggests that bottom-up processing in V4 influences the oculomotor planning process. Half of the neurons also exhibit top-down modulation of visual responses that depends on search target identity but not visual stimulation. Convergence of bottom-up and top-down processing streams in area V4 results in an adaptive, dynamic map of salience that guides oculomotor planning during natural vision.     

Saccadic target selection as a function of time

Recent evidence indicates that stimulus-driven and goal-directed control of visual selection operate independently and in different time windows (van Zoest et al., 2004). The present study further investigates how eye movements are affected by stimulus-driven and goal-directed control. Observers were presented with search displays consisting of one target, multiple non-targets and one distractor element. The task of observers was to make a fast eye movement to a target immediately following the offset of a central fixation point, an event that either co-occurred with or soon followed the presentation of the search display. Distractor saliency and target-distractor similarity were independently manipulated. The results demonstrated that the effect of distractor saliency was transient and only present for the fastest eye movements, whereas the effect of target-distractor similarity was sustained and present in all but the fastest eye movements. The results support an independent timing account of visual selection.     

Causal Inference for Spatial Constancy across Saccades

Our ability to interact with the environment hinges on creating a stable visual world despite the continuous changes in retinal input. To achieve visual stability, the brain must distinguish the retinal image shifts caused by eye movements and shifts due to movements of the visual scene. This process appears not to be flawless: during saccades, we often fail to detect whether visual objects remain stable or move, which is called saccadic suppression of displacement (SSD). How does the brain evaluate the memorized information of the presaccadic scene and the actual visual feedback of the postsaccadic visual scene in the computations for visual stability? Using a SSD task, we test how participants localize the presaccadic position of the fixation target, the saccade target or a peripheral non-foveated target that was displaced parallel or orthogonal during a horizontal saccade, and subsequently viewed for three different durations. Results showed different localization errors of the three targets, depending on the viewing time of the postsaccadic stimulus and its spatial separation from the presaccadic location. We modeled the data through a Bayesian causal inference mechanism, in which at the trial level an optimal mixing of two possible strategies, integration vs. separation of the presaccadic memory and the postsaccadic sensory signals, is applied. Fits of this model generally outperformed other plausible decision strategies for producing SSD. Our findings suggest that humans exploit a Bayesian inference process with two causal structures to mediate visual stability.     

Fixational eye movements predict visual sensitivity

During steady fixation, observers make small fixational saccades at a rate of around 1–2 per second. Presentation of a visual stimulus triggers a biphasic modulation in fixational saccade rate—an initial inhibition followed by a period of elevated rate and a subsequent return to baseline. Here we show that, during passive viewing, this rate signature is highly sensitive to small changes in stimulus contrast. By training a linear support vector machine to classify trials in which a stimulus is either present or absent, we directly compared the contrast sensitivity of fixational eye movements with individuals'' psychophysical judgements. Classification accuracy closely matched psychophysical performance, and predicted individuals'' threshold estimates with less bias and overall error than those obtained using specific features of the signature. Performance of the classifier was robust to changes in the training set (novel subjects and/or contrasts) and good prediction accuracy was obtained with a practicable number of trials. Our results indicate a tight coupling between the sensitivity of visual perceptual judgements and fixational eye control mechanisms. This raises the possibility that fixational saccades could provide a novel and objective means of estimating visual contrast sensitivity without the need for observers to make any explicit judgement.     

Feature-based attention in the frontal eye field and area V4 during visual search

When we search for a target in a crowded visual scene, we often use the distinguishing features of the target, such as color or shape, to guide our attention and eye movements. To investigate the neural mechanisms of feature-based attention, we simultaneously recorded neural responses in the frontal eye field (FEF) and area V4 while monkeys performed a visual search task. The responses of cells in both areas were modulated by feature attention, independent of spatial attention, and the magnitude of response enhancement was inversely correlated with the number of saccades needed to find the target. However, an analysis of the latency of sensory and attentional influences on responses suggested that V4 provides bottom-up sensory information about stimulus features, whereas the FEF provides a top-down attentional bias toward target features that modulates sensory processing in V4 and that could be used to guide the eyes to a searched-for target.     

Memory and prediction in natural gaze control

In addition to stimulus properties and task factors, memory is an important determinant of the allocation of attention and gaze in the natural world. One way that the role of memory is revealed is by predictive eye movements. Both smooth pursuit and saccadic eye movements demonstrate predictive effects based on previous experience. We have previously shown that unskilled subjects make highly accurate predictive saccades to the anticipated location of a ball prior to a bounce in a virtual racquetball setting. In this experiment, we examined this predictive behaviour. We asked whether the period after the bounce provides subjects with visual information about the ball trajectory that is used to programme the pursuit movement initiated when the ball passes through the fixation point. We occluded a 100 ms period of the ball''s trajectory immediately after the bounce, and found very little effect on the subsequent pursuit movement. Subjects did not appear to modify their strategy to prolong the fixation. Neither were we able to find an effect on interception performance. Thus, it is possible that the occluded trajectory information is not critical for subsequent pursuit, and subjects may use an estimate of the ball''s trajectory to programme pursuit. These results provide further support for the role of memory in eye movements.     

Modelling eye movements in a categorical search task

We introduce a model of eye movements during categorical search, the task of finding and recognizing categorically defined targets. It extends a previous model of eye movements during search (target acquisition model, TAM) by using distances from an support vector machine classification boundary to create probability maps indicating pixel-by-pixel evidence for the target category in search images. Other additions include functionality enabling target-absent searches, and a fixation-based blurring of the search images now based on a mapping between visual and collicular space. We tested this model on images from a previously conducted variable set-size (6/13/20) present/absent search experiment where participants searched for categorically defined teddy bear targets among random category distractors. The model not only captured target-present/absent set-size effects, but also accurately predicted for all conditions the numbers of fixations made prior to search judgements. It also predicted the percentages of first eye movements during search landing on targets, a conservative measure of search guidance. Effects of set size on false negative and false positive errors were also captured, but error rates in general were overestimated. We conclude that visual features discriminating a target category from non-targets can be learned and used to guide eye movements during categorical search.     

Different programming modes of human saccadic eye movements as a function of stimulus eccentricity: Indications of a functional subdivision of the visual field

1. Voluntary saccadic eye movements were made toward flashes of light on the horizontal meridian, whose duration and distance from the point of fixation were varied; eye movements were measured using d.c.-electrooculography.—2. Targets within 10°–15° eccentricity are usually reached by one saccadic eye movement. When the eyes turn toward targets of more than 10°–15° eccentricity, the first saccadic eye movement falls short of the target by an angle usually not exceeding 10°. The presence of the image of the target off the fovea (visual error signal) subsequent to such an undershoot elicits, after a short interval, corrective saccades (usually one) which place the image of the target on the fovea. In the absence of a visual error signal, the probability of occurrence of corrective saccades is low, but it increases with greater target eccentricities. These observations suggest that there are different, eccentricity-dependent modes of programming saccadic eye movements.—3. Saccadic eye movements appear to be programmed in retinal coordinates. This conclusion is based on the observations that, irrespective of the initial position of the eyes in the orbit, a) there are different programming modes for eye movements to targets within and beyond 10°–15° from the fixation point, and b_ the maximum velocity of saccadic eye movements is always reached at 25° to 30° target eccentricity. —4. Distributions of latency and intersaccadic interval (ISI) are frequently multimodal, with a separation between modes of 30 to 40 msec. These observations suggest that saccadic eye movements are produced by mechanisms which, at a frequency of 30 Hz, process visual information. —5. Corrective saccades may occur after extremely short intervals (30 to 60 msec) regardless of whether or not a visual error signal is present; the eyes may not even come to a complete stop during these very short intersaccadic intervals. It is suggested that these corrective saccades are triggered by errors in the programming of the initial saccadic eye movements, and not by a visual error signal. —6. The exitence of different, eccentricity-dependent programming modes of saccadic eye movements, is further supported by anatomical, physiological, psychophysical, and neuropathological observations that suggest a dissociation of visual functions dependent on retinal eccentricity. Saccadic eye movements to targets more eccentric than 10°–15° appear to be executed by a mechanism involving the superior colliculus (perhaps independent of the visual cortex), whereas saccadic eye movements to less eccentric targets appear to depend on a mechanism involving the geniculo-cortical pathway (perhaps in collaboration with the superior colliculus).     

Eye Movements,Visual Search and Scene Memory,in an Immersive Virtual Environment

Visual memory has been demonstrated to play a role in both visual search and attentional prioritization in natural scenes. However, it has been studied predominantly in experimental paradigms using multiple two-dimensional images. Natural experience, however, entails prolonged immersion in a limited number of three-dimensional environments. The goal of the present experiment was to recreate circumstances comparable to natural visual experience in order to evaluate the role of scene memory in guiding eye movements in a natural environment. Subjects performed a continuous visual-search task within an immersive virtual-reality environment over three days. We found that, similar to two-dimensional contexts, viewers rapidly learn the location of objects in the environment over time, and use spatial memory to guide search. Incidental fixations did not provide obvious benefit to subsequent search, suggesting that semantic contextual cues may often be just as efficient, or that many incidentally fixated items are not held in memory in the absence of a specific task. On the third day of the experience in the environment, previous search items changed in color. These items were fixated upon with increased probability relative to control objects, suggesting that memory-guided prioritization (or Surprise) may be a robust mechanisms for attracting gaze to novel features of natural environments, in addition to task factors and simple spatial saliency.     

The effect of the visual stimulation of the leading and nonleading eye on the value of the saccadic latency period and on the peak latency of rapid presaccadic potentials]

Visual targets were presented monocularly to the leading and nonleading eyes. The complex of rapid positive and negative potentials was studied using the reverse summation from the onset of saccades. The latencies of saccades and peak latencies of the averaged presaccadic potentials were measured. The dependence of the saccade latencies and peak latencies of the complex of potentials on stimulation of the leading or nonleading eye and saccade direction was not simple and was largely determined by the individual profile of asymmetry. It is suggested that during stimulation of the leading eye the processes of attention fixation and switching as well as of the space visual processing are faster than during stimulation of the nonleading eye. Thus, the leading role of the right eye is reflected not only in fixation processes but also in movement anticipation.     

Attention governs action in the primate frontal eye field

While the motor and attentional roles of the frontal eye field (FEF) are well documented, the relationship between them is unknown. We exploited the known influence of visual motion on the apparent positions of targets, and measured how this illusion affects saccadic eye movements during FEF microstimulation. Without microstimulation, saccades to a moving grating are biased in the direction of motion, consistent with the apparent position illusion. Here we show that microstimulation of spatially aligned FEF representations increases the influence of this illusion on saccades. Rather than simply impose a fixed-vector signal, subthreshold stimulation directed saccades away from the FEF movement field, and instead more strongly in the direction of visual motion. These results demonstrate that the attentional effects of FEF stimulation govern visually guided saccades, and suggest that the two roles of the FEF work together to select both the features of a target and the appropriate movement to foveate it.     

Looking for Discriminating Is Different from Looking for Looking’s Sake

Recent studies provide evidence for task-specific influences on saccadic eye movements. For instance, saccades exhibit higher peak velocity when the task requires coordinating eye and hand movements. The current study shows that the need to process task-relevant visual information at the saccade endpoint can be, in itself, sufficient to cause such effects. In this study, participants performed a visual discrimination task which required a saccade for successful completion. We compared the characteristics of these task-related saccades to those of classical target-elicited saccades, which required participants to fixate a visual target without performing a discrimination task. The results show that task-related saccades are faster and initiated earlier than target-elicited saccades. Differences between both saccade types are also noted in their saccade reaction time distributions and their main sequences, i.e., the relationship between saccade velocity, duration, and amplitude.