Dynamic allocation of visual attention during the execution of sequences of saccades

Laboratory tasks used to study vision and attention usually require steady fixation, while natural visual processing occurs during the brief pauses between successive saccades. We studied vision and attentional allocation during intersaccadic pauses as subjects made repetitive sequences of saccades. Displays contained six outline squares located along the perimeter of an imaginary circle (diam 4 degrees). Saccades were made in sequence to every other square. The visual task was to identify the orientation (2AFC) of a Gabor test stimulus that appeared briefly (91 ms) along with superimposed noise in one of the squares during a randomly selected intersaccadic pause. Gabor location was cued in advance and noise frames were presented in all squares. Contrast thresholds during intersaccadic pauses were as much as 2-3 times higher than during steady fixation with comparable cueing. Thresholds improved over time during the intersaccadic pause, and the lowest extrafoveal thresholds (statistically indistinguishable from those at the same locations during steady fixation) were found for the location that was to be the target of the next saccade in the sequence. These results show that vision during intersaccadic pauses varies over space and time due to changes in the distribution of attention, as well as to visual suppression that may be related to the execution of the saccades themselves. Generation of sequences of accurate saccades encouraged a strategy of attentional allocation in which resources were dedicated primarily to the goal of the next saccade, leaving little attention for processing objects at other locations.     

Attention during active visual tasks: counting, pointing, or simply looking

Visual attention and saccades are typically studied in artificial situations, with stimuli presented to the steadily fixating eye, or saccades made along specified paths. By contrast, in real-world tasks saccadic patterns are constrained only by the demands of the motivating task. We studied attention during pauses between saccades made to perform three free-viewing tasks: counting dots, pointing to the same dots with a visible cursor, or simply looking at the dots using a freely-chosen path. Attention was assessed by the ability to identify the orientation of a briefly-presented Gabor probe. All primary tasks produced losses in identification performance, with counting producing the largest losses, followed by pointing and then looking-only. Looking-only resulted in a 37% increase in contrast thresholds in the orientation task. Counting produced more severe losses that were not overcome by increasing Gabor contrast. Detection or localization of the Gabor, unlike identification, were largely unaffected by any of the primary tasks. Taken together, these results show that attention is required to control saccades, even with freely-chosen paths, but the attentional demands of saccades are less than those attached to tasks such as counting, which have a significant cognitive load. Counting proved to be a highly demanding task that either exhausted momentary processing capacity (e.g., working memory or executive functions), or, alternatively, encouraged a strategy of filtering out all signals irrelevant to counting itself. The fact that the attentional demands of saccades (as well as those of detection/localization) are relatively modest makes it possible to continually adjust both the spatial and temporal pattern of saccades so as to re-allocate attentional resources as needed to handle the complex and multifaceted demands of real-world environments.     

The size and direction of saccadic curvatures during reading

Eye movements during the reading of multi-line pages of texts were analyzed to determine the trajectory of reading saccades. The results of two experiments showed that the trajectory of the majority of forward-directed saccades was negatively biased, i.e., the trajectory fell below the start and end location of the saccadic movement. This is attributed to a global top-to-bottom orienting of attention. The curvature size and the proportion of negative trajectories were diminished when linguistic processing demands were high and when the beginning lines of a page were read. Longer pre-saccadic fixations also yielded smaller saccadic curvatures, and they resulted in fewer negatively curved forward-directed saccades in Experiment 1 although not in Experiment 2. These findings indicate that the top-to-bottom pull of saccadic trajectories is modulated by processing demands and processing opportunities. The results are in general agreement with a time-locked attraction-inhibition hypothesis, according to which the horizontal movement component of a saccade is initially subject to an automatic top-to-bottom orienting of attention that is subsequently inhibited.     

Landmarks facilitate visual space constancy across saccades and during fixation

It has been demonstrated that visual objects that are present after saccadic eye movements act as landmarks for the localization of stimuli across saccades, facilitating space constancy (Deubel, 2004). We here study the temporal conditions under which landmark effects occur after saccadic eye movements, and during fixation. Two small objects were presented 6° in the periphery, one above the other. Observers saccaded to the space between them. One of the objects disappeared during the saccade and reappeared with a variable delay during or after the saccade. At the same time either that object or the continuously present one jumped by 1°. The observer’s task was to decide which object had moved. The results revealed a strong bias to assign movement to the object that was blanked, regardless of which actually moved. If both objects were blanked, the one that was blanked for a shorter time tended to be seen as stable. The effects were stronger as the onset asynchrony between the stimuli increased. Surprisingly, analogous though weaker effects occurred during visual fixation, suggesting that similar visual mechanisms relying on visual landmarks operate both across saccades and during fixation.     

Parametric integration of visual form across saccades

Through saccadic eye movements, the retinal projection of an extrafoveally glimpsed object can be brought into foveal vision quickly. We investigated what influence visual detail collected before the saccade exerts on the postsaccadic percept. Participants were instructed to saccade towards a peripheral stimulus, and to indicate on a continuum of ellipses with varying aspect ratios which exact shape they had perceived to be present after saccade landing. Compared to both an identical ellipse preview and a qualitatively different square preview, a quantitatively different ellipse preview was observed to shift the mean postsaccadic percept towards the presaccadic aspect ratio parameter value. This integration of subtly different form information was accompanied by an integration of the identity of both stimuli presented: In the great majority of these trials, subjects indicated that they had not noticed the occurrence of a change to the stimulus. When a blank screen preceded the postsaccadic stimulus onset the influence of presaccadic stimulus information on postsaccadic perception was weaker. An immediate postsaccadic mask on the other hand abolished the effect entirely. We conclude that integration of parametric visual form information occurs across saccades, but that it relies on a quickly decaying and maskable visual memory.     

Eye movements during multiple readings of the same text

People often read the same text more than once. Studying eye movements during multiple readings of the same texts provides a unique opportunity to observe the consistency of saccadic landing positions. Eye movements were recorded while 5 people read the same 4 texts more than 40 times, no more than 4 times/day, and never on consecutive trials. Other texts, read only once, were interspersed. Comprehension questions and a change-detection task helped maintain attention in the face of the repetition. There were two main findings: (1) repeated reading produced significant, but modest, changes in global saccadic patterns. The only change found in all readers was a reduction in the proportion of regressions. (2) Saccadic landing positions fell into clusters located at a variety of places with respect to word boundaries, and often across word boundaries. A mixed-strategy model of saccadic guidance (look to the center of words, while trying to maintain fairly uniform saccade lengths), could account for the overall strength of clustering, but not for the variability among cluster locations, suggesting that saccadic landing sites are selected in part on the basis of local text characteristics. The reliable clustering of saccadic landing positions found during multiple readings of the same text opens the way for cluster patterns to be used to study eye movement strategies during reading and overcome at least some of the variability associated with traditional global single-text measures.     

Speed and accuracy of saccades, vergence and combined eye movements in subjects with strabismus before and after eye surgery

The purpose of the study was to examine spatio-temporal characteristics of horizontal eye movements in the natural space (saccade, vergence and combined movements) in young subjects with early onset convergent or divergent strabismus. Nine young subjects (8-20 years old) were tested: three with divergent strabismus, six with convergent strabismus. A standard paradigm was used to elicit pure horizontal saccades at far and at close viewing distance, pure vergence along the median plane (convergence and divergence) and saccades combined with vergence movements. Horizontal eye movements from both eyes were recorded by a photoelectric device. Eye movements were recorded before surgery, and, for the majority of the subjects, two times after surgery. Before surgery the accuracy of convergence and divergence movements in their pure or combined form was poor with respect to normal values. The mean velocity of convergence was also abnormally slow. Strabismus surgery improved significantly the accuracy of these types of eye movements. The speed of pure convergence and of divergence combined movements increased significantly after surgery. We concluded that poor vergence eye movement’s performance, particularly those found for convergence in strabismic subjects could be due to impairment in the central structures related to sensory disparity inputs. Adaptive mechanisms promoted by the realignment of the eyes could be at the origin of the improvement in the vergence performances observed in our subjects after strabismus eye surgery.     

Fitts’s Law and speed/accuracy trade-offs during sequences of saccades: Implications for strategies of saccadic planning

Strategies of saccadic planning must take into account both the required level of accuracy of the saccades, and the time and resources needed to plan and execute the movements. To determine relationships between accuracy and time, we studied sequences of saccades made to scan a set of stationary targets located at the corners of an imaginary square. Target separation and size varied. The time taken to complete saccadic sequences increased with the required level of precision, in agreement with the classical Fitts’s Law (1954) relationship. This was mainly due to the use of error-correcting secondary saccades, whose frequency increased with target separation and decreased with target size. Increases in the time spent fixating near each target did not increase the accuracy of the next primary saccade in the sequence. Instead, secondary saccades were the principal means of correcting landing errors of primary saccades. The results are consistent with a scanning strategy that discourages careful planning of individual saccades in favor of increasing the rate of saccadic production (i.e., exploration), using secondary saccades as needed to correct saccadic landing errors.     

Stabilization of gaze: A relationship between ciliary muscle contraction and trapezius muscle activity

In an experimental study four levels of oculomotor load were induced binocularly. Trapezius muscle activity was measured with bipolar surface electromyography and normalized to a submaximal contraction. Twenty-eight subjects with a mean age of 29 (range 19-42, std 8) viewed a high-contrast fixation target for four 5-min periods through: (i) −3.5 dioptre (D) lenses; (ii) 0 D lenses; (iii) individually adjusted prism D lenses (1-2 D base out); and (iv) +3.5 D lenses. The target was placed close to the individual’s age-appropriate near point of accommodation in conditions (i-iii) and at 3 m in condition (iv). Each subject’s ability to compensate for the added blur was extracted via infrared photorefraction measurements. A bitwise linear regression model was fitted on group level with eye-lens refraction on the x-axis and normalized trapezius muscle EMG (%RVE) on the y-axis. The model had a constant level of trapezius muscle activity - where subjects had not compensated for the incurred defocus by a change in eye-lens accommodation - and a slope, where the subjects had compensated. The slope coefficient was significantly positive in the −D (i) and the +D blur conditions (iv). During no blur (ii) and prism blur (iii) there were no signs of relationships. Nor was there any sign of relationship between the convergence response and trapezius muscle EMG in any of the experimental conditions. The results appear directly attributable to an engagement of the eye-lens accommodative system and most likely reflect sensorimotor processing along its reflex arc for the purpose of achieving stabilization of gaze.     

Spatial deployment of attention influences both saccadic and pursuit tracking

We examined the effects of changing spatial aspects of attention during oculomotor tracking. Human subjects were instructed to make a discrimination on either the small (0.8 degrees ) central or the large (8 degrees ) peripheral part of a compound stimulus (two counter-rotating concentric rings) while the stimulus either translated across the screen or was stationary. During this period, a transient perturbation with either step or ramp movement profile occurred. For perturbations leading to a change in position larger than the small ring, saccades occurred more frequently and had much shorter latencies (by 135 ms) when attention was directed to the small ring than when attention was directed to the large ring. These latency differences were sufficiently great that from a single saccade one can identify the attentional instruction with 94% accuracy. However, with target steps as small as the small ring, saccade latencies differed less. For pursuit, ramp perturbations caused larger changes in eye velocity with little change in latency when attention was directed to the small ring. Finally, when only the motion of the non-attended ring was perturbed, most subjects showed stronger saccadic responses to perturbations of the small than the large ring, and stronger pursuit responses to perturbations of the large than the small ring. By fitting the saccade latency distributions with the Reddi and Carpenter LATER model, we found that our subjects apparently employed at least two distinct strategies for changing latency when attending large vs. small. We propose that the timing of the saccade decision process depends on both the size of the attended object and the magnitude of the perturbation.     

Asymmetries in the direction of saccades during perception of scenes and fractals: Effects of image type and image features

The direction in which people tend to move their eyes when inspecting images can reveal the different influences on eye guidance in scene perception, and their time course. We investigated biases in saccade direction during a memory-encoding task with natural scenes and computer-generated fractals. Images were rotated to disentangle egocentric and image-based guidance. Saccades in fractals were more likely to be horizontal, regardless of orientation. In scenes, the first saccade often moved down and subsequent eye movements were predominantly vertical, relative to the scene. These biases were modulated by the distribution of visual features (saliency and clutter) in the scene. The results suggest that image orientation, visual features and the scene frame-of-reference have a rapid effect on eye guidance.     

The influence of bright background flicker during different saccade periods on saccadic performance

We investigated saccades from central fixation to targets at 5 degrees to the left or right. These targets were red laser points of light with an intensity unmodulated in time (referred to as steady), while a bright background (76 cd/m(2)) was illuminated by a special fluorescent lamp, the output of which were series of light pulses (at frequencies of 50 or 100 Hz) that were presented only during certain periods, in synchrony with the saccade: e.g. during fixation of the central target, or during the latency (i.e. the period from target onset to saccade onset), or during the execution of the saccade; otherwise, the background luminance was steady. We observed a mean increase in latency of about 23 ms when 50 Hz flicker pulses occurred during the latency alone. This result is interpreted in terms of saccadic inhibition [Reingold & Stampe, (2000) In: Kennedy, Radach, Heller, & Pynte (Eds.) Reading as a perceptual process. Elsevier, Amsterdam]: our bright background flicker during the latency may have produced longer latencies, similar to the remote distractors in the model of Findlay and Walker [Behav. Brain Sci. 22 (1999) 661].     

Transient torsion during and after saccades

In five normal subjects, we analyzed uncalled for torsion (blips) during and after horizontal and vertical saccades. Torsion was defined as movement out of Listing's plane. During horizontal saccades in downward gaze the abducting eye extorted and the adducting eye intorted. The direction of the blips reversed in upward gaze. Peak torsional amplitudes (up to 1–2 deg) were always reached during saccades; drifts back to Listing's plane outlasted the saccades. Torsion of the extorting eye was larger than that of the intorting eye, producing a transient positive cyclovergence. Torsion and cyclovergence evoked by vertical saccades were also stereotyped in each eye, but showed idiosyncratic differences among subjects. We conclude that Listing's law is violated during saccades. Transient saccade-evoked torsion might reflect properties of the three-dimensional velocity-to-position integrator and/or the ocular plant.     

The time course of vertical, horizontal and oblique saccade trajectories: Evidence for greater distractor interference during vertical saccades

The present study aimed to characterize the effect of a nearby distractor on vertical, horizontal, and oblique saccade curvature under normal saccade preparation times. Consistent with previous findings, longer-latency vertical saccades showed greater curvature away from a distractor than did oblique or horizontal saccades. At short latencies, vertical saccades also showed greater curvature towards the distractor. A neural explanation for why vertical saccades show greater interference from a distractor is theorized.     

Dynamic interaction between "Go" and "Stop" signals in the saccadic eye movement system: New evidence against the functional independence of the underlying neural mechanisms

We investigated human oculomotor behaviour in a Go-NoGo saccadic task in which the saccadic response to a peripheral visual target was to be inhibited in a minority of trials (NoGo trials). Different from classical experimental paradigms on the inhibitory control of intended actions, in our task the inhibitory cue was identical to the saccadic target (used in Go trials) in timing, location and shape—the only difference being its colour. By analysing the latency and the metrics of saccades erroneously executed after a NoGo instruction (NoGo-escapes), we observed a characteristic pattern of performance: first, we observed a decrease in the amplitude of NoGo-escapes with increasing latency; second, we revealed a consistent population of long-latency small saccades opposite in direction to the NoGo cue; finally, we found a strong side-specific inhibitory effect in terms of saccadic reaction times, on trials immediately following a NoGo trial. In addition, we manipulated the readiness to initiate a saccade towards the visual target, by introducing a probability bias in the random sequence of target locations. We found that the capacity to inhibit the impending saccade was improved for the most likely target location, i.e. the condition corresponding to the increased readiness for movement execution. Overall, our results challenge the notion of a central inhibitory mechanism independent from movement preparation. More precisely, they indicate that the two mechanisms (action preparation and action inhibition) interact dynamically, possibly sharing spatially-specific mechanisms, and are similarly affected by particular contextual manipulations.     

Effects of luminance contrast and its modifications on fixation behavior during free viewing of images from different categories

During viewing of natural scenes, do low-level features guide attention, and if so, does this depend on higher-level features? To answer these questions, we studied the image category dependence of low-level feature modification effects. Subjects fixated contrast-modified regions often in natural scene images, while smaller but significant effects were observed for urban scenes and faces. Surprisingly, modifications in fractal images did not influence fixations. Further analysis revealed an inverse relationship between modification effects and higher-level, phase-dependent image features. We suggest that high- and mid-level features - such as edges, symmetries, and recursive patterns - guide attention if present. However, if the scene lacks such diagnostic properties, low-level features prevail. We posit a hierarchical framework, which combines aspects of bottom-up and top-down theories and is compatible with our data.     

Saccade trajectory deviations and inhibition-of-return: Measuring the amount of attentional processing

This study used a classic exogenous cueing task in which an abrupt onset cue indicated the target location at chance level. When there was a delay between the cue and the target, observers responded slower and less accurate to the target presented at cued than at uncued locations, signifying the occurrence of inhibition-of-return (IOR). On some trials, instead of a manual response, participants had to move their eyes to a location in space. Our findings show no saccade deviation away from the location that was inhibited due to IOR unless participants had to process the target letter presented at the inhibited location. Our findings are consistent with the notion that inhibition resulting in IOR does not occur at the saccade map level but IOR seems to reduce the input of signals going into the saccade map. We show that the strength of saccade deviation is an important measure which can reveal the amount of attentional processing taking place at any particular location in time.     

Differential detection of global luminance and contrast changes across saccades and flickers during active scene perception

How sensitive are viewers to changes in global image properties across saccades during active real-world scene perception? This question was investigated by globally increasing and/or decreasing luminance or contrast in photographs of real-world scenes across saccadic eye movements or during matched brief interruptions in a flicker paradigm. The results from two experiments demonstrated very poor sensitivity to global image changes in both the saccade-contingent and flicker paradigms, suggesting that the specific values of basic sensory properties do not contribute to the perception of stability across saccades during complex scene perception. In addition, overall sensitivity was significantly worse in the saccade-contingent change paradigm than the flicker paradigm, suggesting that the flicker paradigm is an imperfect simulation of transsaccadic vision.     

The relationship between spatial pooling and attention in saccadic and perceptual tasks

Saccades aimed at spatially extended targets land reliably at central locations determined by pooling information across the target shape [Melcher, D., & Kowler, E. (1999). Shape, surfaces and saccades. Vision Research, 39, 2929-2946; Vishwanath, D., & Kowler, E. (2003). Localization of shapes: Eye movements and perception compared. Vision Research, 43, 1637-1653]. Previous findings of saccadic errors when attempting to look at a target in the midst of distractors encouraged suggestions that pooling occurs indiscriminately, with little or no influence of a selective filter to eliminate the influence of nearby distractors. To determine the effectiveness of filtering, saccadic localization was studied for saccades made to a set of target elements (discs) interleaved with an equivalent set of distractors of a different color. With such interleaved elements, selection and spatial pooling are constrained to occur over the same spatial region. The results showed that filtering was effective and saccadic landing position was determined mainly by the target elements. Concurrent perceptual judgments made about the same stimuli (estimating the mean size of either target or distractor discs) showed better performance for the target discs than distractors, confirming that perceptual attention was allocated to the set of target elements. These results: (1) support the role of attention in setting the input to the spatial pooling process that guides saccades to spatially extended targets, and (2) show that perceptual judgments of mean value, often thought to impose modest attentional demands, are not immune to the constraints of this pre-saccadic filter.