Martin Rolfs

Microsaccades: Small steps on a long way

Contrary to common wisdom, fixations are a dynamically rich behavior, composed of continual, miniature eye movements, of which microsaccades are the most salient component. Over the last few years, interest in these small movements has risen dramatically, driven by both neurophysiological and psychophysical results and by advances in techniques, analysis, and modeling of eye movements. The field has a long history but a significant portion of the earlier work has gone missing in the current literature, in part, as a result of the collapse of the field in the 1980s that followed a series of discouraging results. The present review compiles 60 years of work demonstrating the unique contribution of microsaccades to visual and oculomotor function. Specifically, the review covers the contribution of microsaccades to (1) the control of fixation position, (2) the reduction of perceptual fading and the continuity of perception, (3) the generation of synchronized visual transients, (4) visual acuity, (5) scanning of small spatial regions, (6) shifts of spatial attention, (7) resolving perceptual ambiguities in the face of multistable perception, as well as several other functions. The accumulated evidence demonstrates that microsaccades serve both perceptual and oculomotor goals and although in some cases their contribution is neither necessary nor unique, microsaccades are a malleable tool conveniently employed by the visual system.

Length, frequency, and predictability effects of words on eye movements in reading

We tested the effects of word length, frequency, and predictability on inspection durations (first fixation, single fixation, gaze duration, and reading time) and inspection probabilities during first‐pass reading (skipped, once, twice) for a corpus of 144 German sentences (1138 words) and a subset of 144 target words uncorrelated in length and frequency, read by 33 young and 32 older adults. For corpus words, length and frequency were reliably related to inspection durations and probabilities, predictability only to inspection probabilities. For first‐pass reading of target words all three effects were reliable for inspection durations and probabilities. Low predictability was strongly related to second‐pass reading. Older adults read slower than young adults and had a higher frequency of regressive movements. The data are to serve as a benchmark for computational models of eye movement control in reading.

Predictive remapping of attention across eye movements

Many cells in retinotopic brain areas increase their activity when saccades (rapid eye movements) are about to bring stimuli into their receptive fields. Although previous work has attempted to look at the functional correlates of such predictive remapping, no study has explicitly tested for better attentional performance at the future retinal locations of attended targets. We found that, briefly before the eyes start moving, attention drawn to the targets of upcoming saccades also shifted to those retinal locations that the targets would cover once the eyes had moved, facilitating future movements. This suggests that presaccadic visual attention shifts serve to both improve presaccadic perceptual processing at the target locations and speed subsequent eye movements to their new postsaccadic locations. Predictive remapping of attention provides a sparse, efficient mechanism for keeping track of relevant parts of the scene when frequent rapid eye movements provoke retinal smear and temporal masking.

Toward a model of microsaccade generation: the case of microsaccadic inhibition.

Microsaccades are one component of the small eye movements that constitute fixation. Their implementation in the oculomotor system is unknown. To better understand the physiological and mechanistic processes underlying microsaccade generation, we studied microsaccadic inhibition, a transient drop of microsaccade rate, in response to irrelevant visual and auditory stimuli. Quantitative descriptions of the time course and strength of inhibition revealed a strong dependence of microsaccadic inhibition on stimulus characteristics. In Experiment 1, microsaccadic inhibition occurred sooner after auditory than after visual stimuli and after luminance-contrast than after color-contrast visual stimuli. Moreover, microsaccade amplitude strongly decreased during microsaccadic inhibition. In Experiment 2, the latency of microsaccadic inhibition increased with decreasing luminance contrast. We develop a conceptual model of microsaccade generation in which microsaccades result from fixation-related activity in a motor map coding for both fixation and saccades. In this map, fixation is represented at the central site. Saccades are generated by activity in the periphery, their amplitude increasing with eccentricity. The activity at the central, fixation-related site of the map predicts the rate of microsaccades as well as their amplitude and direction distributions. This model represents a framework for understanding the dynamics of microsaccade behavior in a broad range of tasks.

Post-saccadic location judgments reveal remapping of saccade targets to non-foveal locations

The present study addresses the question of how objects are localized across saccades. In a task requiring participants to compare the location of a post-saccadic probe with the pre-saccadic target, we investigated the roles of saccade landing site and post-saccadic probe location. Saccade landing sites vary from trial to trial because of oculomotor error but can also be shifted by saccadic adaptation. Visual targets were extinguished during the saccade and reappeared after a short blank to counteract saccadic suppression of displacement. Performance in localizing targets after unadapted saccades was nearly veridical and independent of actual landing site, showing that trial-to-trial oculomotor error did not contribute to post-saccadic localization. This result suggests that much of the oculomotor error of saccades is included in the efference copy vector and this allows the recovery of a remapped target location that is often not foveal, but stable and accurate across trials. Displacement judgments relative to this remapped location will be independent of trial-to-trial variability in landing site. After adapted saccades, post-saccadic localization shifted in the direction opposite to adaptation but again, trial-by-trial landing site variability did not correlate with performance. This result suggests that the efference copy matches the planned upcoming saccade, be it adapted or not.

The reference frame of the motion aftereffect is retinotopic

Although eye-, head- and body-movements can produce large-scale translations of the visual input on the retina, perception is notable for its spatiotemporal continuity. The visual system might achieve this by the creation of a detailed map in world coordinates--a spatiotopic representation. We tested the coordinate system of the motion aftereffect by adapting observers to translational motion and then tested (1) at the same retinal and spatial location (full aftereffect condition), (2) at the same retinal location, but at a different spatial location (retinotopic condition), (3) at the same spatial, but at a different retinal location (spatiotopic condition), or (4) at a different spatial and retinal location (general transfer condition). We used large stimuli moving at high speed to maximize the likelihood of motion integration across space. In a second experiment, we added a contrast-decrement detection task to the motion stimulus to ensure attention was directed at the adapting location. Strong motion aftereffects were found when observers were tested in the full and retinotopic aftereffect conditions. We also found a smaller aftereffect at the spatiotopic location but it did not differ from that at the location that was neither spatiotopic nor retinotopic. This pattern of results did not change when attention was explicitly directed at the adapting stimulus. We conclude that motion adaptation took place at retinotopic levels of visual cortex and that no spatiotopic interaction of motion adaptation and test occurred across saccades.

Crossmodal coupling of oculomotor control and spatial attention in vision and audition

Fixational eye movements occur involuntarily during visual fixation of stationary scenes. The fastest components of these miniature eye movements are microsaccades, which can be observed about once per second. Recent studies demonstrated that microsaccades are linked to covert shifts of visual attention. Here, we generalized this finding in two ways. First, we used peripheral cues, rather than the centrally presented cues of earlier studies. Second, we spatially cued attention in vision and audition to visual and auditory targets. An analysis of microsaccade responses revealed an equivalent impact of visual and auditory cues on microsaccade-rate signature (i.e. an initial inhibition followed by an overshoot and a final return to the pre-cue baseline rate). With visual cues or visual targets, microsaccades were briefly aligned with cue direction and then opposite to cue direction during the overshoot epoch, probably as a result of an inhibition of an automatic saccade to the peripheral cue. With left auditory cues and auditory targets microsaccades oriented in cue direction. We argue that microsaccades can be used to study crossmodal integration of sensory information and to map the time course of saccade preparation during covert shifts of visual and auditory attention.

The reference frame of the tilt aftereffect.

Perceptual aftereffects provide a sensitive tool to investigate the influence of eye and head position on visual processing. There have been recent indications that the TAE is remapped around the time of a saccade to remain aligned to the adapting location in the world. Here, we investigate the spatial frame of reference of the TAE by independently manipulating retinal position, gaze orientation, and head orientation between adaptation and test. The results show that the critical factor in the TAE is the correspondence between the adaptation and test locations in a retinotopic frame of reference, whereas world- and head-centric frames of reference do not play a significant role. Our results confirm that adaptation to orientation takes place at retinotopic levels of visual processing. We suggest that the remapping process that plays a role in visual stability does not transfer feature gain information around the time of eye (or head) movements.

Event-Related Potentials Reveal Rapid Verification of Predicted Visual Input

Human information processing depends critically on continuous predictions about upcoming events, but the temporal convergence of expectancy-based top-down and input-driven bottom-up streams is poorly understood. We show that, during reading, event-related potentials differ between exposure to highly predictable and unpredictable words no later than 90 ms after visual input. This result suggests an extremely rapid comparison of expected and incoming visual information and gives an upper temporal bound for theories of top-down and bottom-up interactions in object recognition.

Microsaccade Orientation Supports Attentional Enhancement Opposite a Peripheral Cue: Commentary on Tse, Sheinberg, and Logothetis (2003)

Tse, Sheinberg, and Logothetis (2003) exploited a change-blindness paradigm to map the redistribution of spatial attention in response to a peripherally flashed cue. The probability of change detection at a given location was used as a measure of attention allocation. Using this measure, a ‘‘hot spot’’ of attention (i.e., close to perfect change detection) was found along the cue-fixation axis. This hot spot ex- tended in the hemifield opposite the cued location. Here we show that an analysis of fixational eye movements in a spatial-cuing paradigm supports this important finding. Psychological Science