Alexander C. Schütz

Eye movements and perception: A selective review

Eye movements are an integral and essential part of our human foveated vision system. Here, we review recent work on voluntary eye movements, with an emphasis on the last decade. More selectively, we address two of the most important questions about saccadic and smooth pursuit eye movements in natural vision. First, why do we saccade to where we do? We argue that, like for many other aspects of vision, several different circuits related to salience, object recognition, actions, and value ultimately interact to determine gaze behavior. Second, how are pursuit eye movements and perceptual experience of visual motion related? We show that motion perception and pursuit have a lot in common, but they also have separate noise sources that can lead to dissociations between them. We emphasize the point that pursuit actively modulates visual perception and that it can provide valuable information for motion perception.

Improved visual sensitivity during smooth pursuit eye movements

When we view the world around us, we constantly move our eyes. This brings objects of interest into the fovea and keeps them there, but visual sensitivity has been shown to deteriorate while the eyes are moving. Here we show that human sensitivity for some visual stimuli is improved during smooth pursuit eye movements. Detection thresholds for briefly flashed, colored stimuli were 16% lower during pursuit than during fixation. Similarly, detection thresholds for luminance-defined stimuli of high spatial frequency were lowered. These findings suggest that the pursuit-induced sensitivity increase may have its neuronal origin in the parvocellular retino-thalamic system. This implies that the visual system not only uses feedback connections to improve processing for locations and objects being attended to, but that a whole processing subsystem can be boosted. During pursuit, facilitation of the parvocellular system may reduce motion blur for stationary objects and increase sensitivity to speed changes of the tracked object.

What is the best fixation target? The effect of target shape on stability of fixational eye movements.

People can direct their gaze at a visual target for extended periods of time. Yet, even during fixation the eyes make small, involuntary movements (e.g. tremor, drift, and microsaccades). This can be a problem during experiments that require stable fixation. The shape of a fixation target can be easily manipulated in the context of many experimental paradigms. Thus, from a purely methodological point of view, it would be good to know if there was a particular shape of a fixation target that minimizes involuntary eye movements during fixation, because this shape could then be used in experiments that require stable fixation. Based on this methodological motivation, the current experiments tested if the shape of a fixation target can be used to reduce eye movements during fixation. In two separate experiments subjects directed their gaze at a fixation target for 17s on each trial. The shape of the fixation target varied from trial to trial and was drawn from a set of seven shapes, the use of which has been frequently reported in the literature. To determine stability of fixation we computed spatial dispersion and microsaccade rate. We found that only a target shape which looks like a combination of bulls eye and cross hair resulted in combined low dispersion and microsaccade rate. We recommend the combination of bulls eye and cross hair as fixation target shape for experiments that require stable fixation.

Dynamic integration of information about salience and value for saccadic eye movements

Humans shift their gaze to a new location several times per second. It is still unclear what determines where they look next. Fixation behavior is influenced by the low-level salience of the visual stimulus, such as luminance, contrast, and color, but also by high-level task demands and prior knowledge. Under natural conditions, different sources of information might conflict with each other and have to be combined. In our paradigm, we trade off visual salience against expected value. We show that both salience and value information influence the saccadic end point within an object, but with different time courses. The relative weights of salience and value are not constant but vary from eye movement to eye movement, depending critically on the availability of the value information at the time when the saccade is programmed. Short-latency saccades are determined mainly by salience, but value information is taken into account for long-latency saccades. We present a model that describes these data by dynamically weighting and integrating detailed topographic maps of visual salience and value. These results support the notion of independent neural pathways for the processing of visual information and value.

Temporal contrast sensitivity during smooth pursuit eye movements

During smooth pursuit eye movements, stimuli other than the pursuit target move across the retina, and this might affect their detectability. We measured detection thresholds for vertically oriented Gabor stimuli with different temporal frequencies (1, 4, 8, 12, 16, 20, and 24 Hz) of the sinusoids. Observers kept fixation on a small target spot that was either stationary or moved horizontally at a speed of 8 deg/s. The sinusoid of the Gabor stimuli moved either in the same or in the opposite direction as the pursuit target. Observers had to indicate whether the Gabor stimuli were displayed 4 degrees above or below the target spot. Results show that contrast sensitivity was mainly determined by retinal-image motion but was slightly reduced during smooth pursuit eye movements. Moreover, sensitivity for motion opposite to pursuit direction was reduced in comparison to motion in pursuit direction. The loss in sensitivity for peripheral targets during pursuit can be interpreted in terms of space-based attention to the pursuit target. The loss of sensitivity for motion opposite to pursuit direction can be interpreted as feature-based attention to the pursuit direction.

Trans-saccadic integration of peripheral and foveal feature information is close to optimal

Due to the inhomogenous visual representation across the visual field, humans use peripheral vision to select objects of interest and foveate them by saccadic eye movements for further scrutiny. Thus, there is usually peripheral information available before and foveal information after a saccade. In this study we investigated the integration of information across saccades. We measured reliabilities--i.e., the inverse of variance-separately in a presaccadic peripheral and a postsaccadic foveal orientation--discrimination task. From this, we predicted trans-saccadic performance and compared it to observed values. We show that the integration of incongruent peripheral and foveal information is biased according to their relative reliabilities and that the reliability of the trans-saccadic information equals the sum of the peripheral and foveal reliabilities. Both results are consistent with and indistinguishable from statistically optimal integration according to the maximum-likelihood principle. Additionally, we tracked the gathering of information around the time of the saccade with high temporal precision by using a reverse correlation method. Information gathering starts to decline between 100 and 50 ms before saccade onset and recovers immediately after saccade offset. Altogether, these findings show that the human visual system can effectively use peripheral and foveal information about object features and that visual perception does not simply correspond to disconnected snapshots during each fixation.

Smooth Pursuit Eye Movements to Isoluminant Targets

At slow speeds, chromatic isoluminant stimuli are perceived to move much slower than comparable luminance stimuli. We investigated whether smooth pursuit eye movements to isoluminant stimuli show an analogous slowing. Beside pursuit speed and latency, we studied speed judgments to the same stimuli during fixation and pursuit. Stimuli were either large sine wave gratings or small Gaussians blobs moving horizontally at speeds between 1 and 11 degrees /s. Targets were defined by luminance contrast or color. Confirming prior studies, we found that speed judgments of isoluminant stimuli during fixation showed a substantial slowing when compared with luminance stimuli. A similarly strong and significant effect of isoluminance was found for pursuit initiation: compared with luminance targets of matched contrasts, latencies of pursuit initiation were delayed by 50 ms at all speeds and eye accelerations were reduced for isoluminant targets. A small difference was found between steady-state eye velocities of luminance and isoluminant targets. For comparison, we measured latencies of saccades to luminance and isoluminant stimuli under similar conditions, but the effect of isoluminance was only found for pursuit. Parallel psychophysical experiments revealed that different from speed judgments of moving isoluminant stimuli made during fixation, judgments during pursuit are veridical for the same stimuli at all speeds. Therefore information about target speed seems to be available for pursuit eye movements and speed judgments during pursuit but is degraded for perceptual speed judgments during fixation and for pursuit initiation.

Contrast sensitivity during the initiation of smooth pursuit eye movements.

Eye movements challenge the perception of a stable world by inducing retinal image displacement. During saccadic eye movements visual stability is accompanied by a remapping of visual receptive fields, a compression of visual space and perceptual suppression. Here we explore whether a similar suppression changes the perception of briefly presented low contrast targets during the initiation of smooth pursuit eye movements. In a 2AFC design we investigated the contrast sensitivity for threshold-level stimuli during the initiation of smooth pursuit and during saccades. Pursuit was elicited by horizontal step-ramp and ramp stimuli. At any time from 200 ms before to 500 ms after pursuit stimulus onset, a blurred 0.3 deg wide horizontal line with low contrast just above detection threshold appeared for 10 ms either 2 deg above or below the pursuit trajectory. Observers had to pursue the moving stimulus and to indicate whether the target line appeared above or below the pursuit trajectory. In contrast to perceptual suppression effects during saccades, no pronounced suppression was found at pursuit onset for step-ramp motion. When pursuit was elicited by a ramp stimulus, pursuit initiation was accompanied by catch-up saccades, which caused saccadic suppression. Additionally, contrast sensitivity was attenuated at the time of pursuit or saccade stimulus onset. This attenuation might be due to an attentional deficit, because the stimulus required the focus of attention during the programming of the following eye movement.

Object recognition during foveating eye movements

We studied how saccadic and smooth pursuit eye movements affect the recognition of briefly presented letters appearing within the eye movement target. First we compared the recognition performance during steady-state pursuit and during fixation. Single letters were presented for seven different durations ranging from 10 to 400 ms and four contrast levels ranging from 5% to 40%. For both types of eye movements the recognition rates increased with duration and contrast, but they were on average 11% lower during pursuit. In daily life humans use a combination of saccadic and smooth pursuit eye movements to foveate a peripheral moving object. To investigate this more natural situation, we presented a peripheral target that was either stationary or moving horizontally, above or below the fixation spot. Participants were asked to saccade to the target and to keep it foveated. The letters were presented at different times relative to the first target directed saccade. As would be expected from retinal masking and motion blur during saccades, the discrimination performance increased with increasing post-saccadic delay. If the target moved and the saccade was followed by pursuit, letter recognition performance was on average 16% lower than if the target was stationary and the saccade was followed by fixation.

Does the noise matter? Effects of different kinematogram types on smooth pursuit eye movements and perception

We investigated how the human visual system and the pursuit system react to visual motion noise. We presented three different types of random-dot kinematograms at five different coherence levels. For transparent motion, the signal and noise labels on each dot were preserved throughout each trial, and noise dots moved with the same speed as the signal dots but in fixed random directions. For white noise motion, every 20 ms the signal and noise labels were randomly assigned to each dot and noise dots appeared at random positions. For Brownian motion, signal and noise labels were also randomly assigned, but the noise dots moved at the signal speed in a direction that varied randomly from moment to moment. Neither pursuit latency nor early eye acceleration differed among the different types of kinematograms. Late acceleration, pursuit gain, and perceived speed all depended on kinematogram type, with good agreement between pursuit gain and perceived speed. For transparent motion, pursuit gain and perceived speed were independent of coherence level. For white and Brownian motions, pursuit gain and perceived speed increased with coherence but were higher for white than for Brownian motion. This suggests that under our conditions, the pursuit system integrates across all directions of motion but not across all speeds.