Doris I. Braun

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.

Transcranial magnetic stimulation of extrastriate cortex degrades human motion direction discrimination.

The human temporo-parieto-occipital junction is an extrastriate visual area that may mediate motion vision processing. We determined if transcranial magnetic stimulation (TMS) delivered over this extrastriate area would degrade motion discrimination, similar to the transient decrease in spatial acuity observed when TMS is delivered over striate cortex. TMS was delivered 50-250 msec after the onset of a brief, random dot, motion direction discrimination task or a spatial acuity task. TMS significantly reduced correct motion discrimination when delivered 100-150 msec after the random dot stimulus. During the same time window TMS did not significantly effect spatial acuity. TMS over the left extrastriate cortex reduced motion discrimination in both hemifields and its effect had a crude topographical organization. TMS safely perturbs extrastriate visual areas and may reveal the temporal sequence of higher perceptual processing.

Relationship between directed visual attention and saccadic reaction times.

SummarySaslow (1967) and Fischer and Ramsperger (1984) found that saccadic reaction time (SRT) depends on the interval between the fixation point offset and the target onset. Using a continuously visible fixation point, we asked whether a similar function would be obtained if subjects attended to a peripherally viewed point extinguished at variable intervals before or after the target onset. The interval was varied between -500ms (i.e., attention stimulus offset after saccade target onset = overlap trials) and 500ms (i.e., attention stimulus offset before saccade target onset = gap trials). The results show a constant mean SRT of about 240 ms for overlap trials, and a U-shaped function with a minimum of 140 ms, at a gap duration of 200 ms, for gap trials. These findings suggest that saccadic latencies do not depend on the cessation of fixation per se, but rather on the disengagement of attention from any location in the visual field. The time required for subjects to disengage their attention is approximately 100 ms. This disengaged state of attention — during which short latency (express) saccades can be made — can be sustained only for a gap duration of 300 ms. At longer gap durations mean SRTs increase again.

Effects of reappearance of fixated and attended stimuli upon saccadic reaction time

SummaryThe effects of visual attention and fixation upon the distribution of saccadic latencies: express (E-), fast regular (FR-), and slow regular (SR-) saccades were investigated. Extinguishing a fixation or an attention point 200–300 ms before target onset increases the incidence of E-saccades while concurrently decreasing the proportion of SR-saccades. Since this extinction forces a disengaging of attention, these changes in relative proportions of saccades reflect the elimination of one of the steps involved in programming saccades. It is shown that a previously attended stimulus has a favored status relative to other stimuli in the visual field. If, after being turned off, the previously attended fixation point or a peripheral attention stimulus is turned on near the time of the targets appearance, the occurrence of the E-saccades is greatly reduced. However, the appearance of any other stimulus in the visual field at or near the time of the target onset does not inhibit E-saccades. Contrary to the conclusions reached by Posner and Cohen (1984), a stimulus presented at the formerly attended location can attract attention more efficiently than a stimulus presented at another, new location.

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.

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.

Effects of contrast on smooth pursuit eye movements

It is well known that moving stimuli can appear to move more slowly when contrast is reduced (P. Thompson, 1982). Here we address the question whether changes in stimulus contrast also affect smooth pursuit eye movements. Subjects were asked to smoothly track a moving Gabor patch. Targets varied in velocity (1, 8, and 15 deg/s), spatial frequency (0.1, 1, 4, and 8 c/deg), and contrast, ranging from just below individual thresholds to maximum contrast. Results show that smooth pursuit eye velocity gain rose significantly with increasing contrast. Below a contrast level of two to three times threshold, pursuit gain, acceleration, latency, and positional accuracy were severely impaired. Therefore, the smooth pursuit motor response shows the same kind of slowing at low contrast that was demonstrated in previous studies on perception.

Selective Color Constancy Deficits after Circumscribed Unilateral Brain Lesions

The color of an object, when part of a complex scene, is determined not only by its spectral reflectance but also by the colors of all other objects in the scene (von Helmholtz, 1886; Ives, 1912; Land, 1959). By taking global color information into account, the visual system is able to maintain constancy of the color appearance of the object, despite large variations in the light incident on the retina arising from changes in the spectral content of the illuminating light (Hurlbert, 1998; Maloney, 1999). The neural basis of this color constancy is, however, poorly understood. Although there seems to be a prominent role for retinal, cone-specific adaptation mechanisms (von Kries, 1902; Pöppel, 1986; Foster and Nascimento, 1994), the contribution of cortical mechanisms to color constancy is still unclear (Land et al., 1983; D’Zmura and Lennie, 1986). We examined the color perception of 27 patients with defined unilateral lesions mainly located in the parieto-temporo-occipital and fronto-parieto-temporal cortex. With a battery of clinical and specially designed color vision tests we tried to detect and differentiate between possible deficits in central color processing. Our results show that color constancy can be selectively impaired after circumscribed unilateral lesions in parieto-temporal cortex of the left or right hemisphere. Five of 27 patients exhibited significant deficits in a color constancy task, but all of the 5 performed well in color discrimination or higher-level visual tasks, such as the association of colors with familiar objects. These results indicate that the computations underlying color constancy are mediated by specialized cortical circuitry, which is independent of the neural substrate for color discrimination and for assigning colors to objects.

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.