Svenja Gremmler

Saccadic adaptation shapes visual space in macaques.

Saccadic eye movements are an integral part of many visually guided behaviors. Recent research in humans has shown that processes which control saccades are also involved in establishing perceptual space: A shift in object localization during fixation occurred after saccade amplitudes had been shortened or lengthened by saccadic adaptation. We tested whether similar effects can be established in nonhuman primates. Two trained macaque monkeys localized briefly presented stimuli on a touch screen by indicating the memorized target position with the hand on the screen. The monkeys performed this localization task before and after saccade amplitudes were modified through saccadic adaptation. During localization trials they had to maintain fixation. Successful saccadic adaptation led to a concurrent shift of the touched position on the screen. This mislocalization occurred for both adaptive shortening and lengthening of saccade amplitude. We conclude that saccadic adaptation has the potential to influence localization performance in monkeys, similar to the results found in humans.

The reward of seeing: Different types of visual reward and their ability to modify oculomotor learning

Saccadic adaptation is an oculomotor learning process that maintains the accuracy of eye movements to ensure effective perception of the environment. Although saccadic adaptation is commonly considered an automatic and low-level motor calibration in the cerebellum, we recently found that strength of adaptation is influenced by the visual content of the target: pictures of humans produced stronger adaptation than noise stimuli. This suggests that meaningful images may be considered rewarding or valuable in oculomotor learning. Here we report three experiments that establish the boundaries of this effect. In the first, we tested whether stimuli that were associated with high and low value following long term self-administered reinforcement learning produce stronger adaptation. Twenty-eight expert gamers participated in two sessions of adaptation to game-related high- and low-reward stimuli, but revealed no difference in saccadic adaptation (Bayes Factor01 = 5.49). In the second experiment, we tested whether cognitive (literate) meaning could induce stronger adaptation by comparing targets consisting of words and nonwords. The results of twenty subjects revealed no difference in adaptation strength (Bayes Factor01 = 3.21). The third experiment compared images of human figures to noise patterns for reactive saccades. Twenty-two subjects adapted significantly more toward images of human figures in comparison to noise (p < 0.001). We conclude that only primary (human vs. noise), but not secondary, reinforcement affects saccadic adaptation (words vs. nonwords, high- vs. low-value video game images).

New is always better: Novelty modulates oculomotor learning

Saccadic adaptation aims at keeping saccades accurate to enable precise foveation of objects. It has been believed to be a rather low-level adjustment, responding chiefly to direction and magnitude of postsaccadic position error. However, recent studies have shown that image content can modify saccadic adaptation. Adaptation is more complete for saccades toward socially relevant human figures in comparison to noise when time constraints exist. In the present experiment, we show that saccadic adaptation is also susceptible to the novelty of a stimulus. In a scanning adaptation paradigm, 20 subjects participated in two sessions of forward adaptation to one position at which the same human picture was always displayed versus a position at which a new human figure was presented in every trial. Saccadic adaptation was more complete to the novel-target position. This suggests that novelty can increase oculomotor learning and corroborates the claim that saccadic adaptation includes influences that reflect the targets visual properties.

Saccadic suppression during voluntary versus reactive saccadesGremmler & Lappe

Saccades are fast eye movements that reorient gaze. They can be performed voluntarily-for example, when viewing a scene-but they can also be triggered in reaction to suddenly appearing targets. The generation of these voluntary and reactive saccades have been shown to involve partially different cortical pathways. However, saccades of either type confront the visual system with a major challenge from massive image motion on the retina. Despite the fact that the whole scene is swept across the retina, a saccade usually does not elicit a percept of motion. This saccadic omission has been linked to a transient decrease of visual sensitivity during the eye movement, a phenomenon called saccadic suppression. A passive origin of saccadic suppression based on temporal masking has been proposed as well as an active central process that inhibits visual processing during the saccade. The latter one would need to include an extraretinal signal, which is generated already during saccade preparation. Since saccade generation differs for voluntary and reactive saccades, timing and nature of this extraretinal signal as well as its impact on visual sensitivity might also differ. We measured detection thresholds for luminance stimuli that were flashed during voluntary and reactive saccades and during fixation. Detection thresholds were higher during voluntary than during reactive saccades such that suppression appeared stronger during voluntary saccades. Stronger suppression in voluntary saccades could arise from a stronger extraretinal signal that activates suppression or could indicate that a suppression underlying process itself partially differs between voluntary and reactive saccades.

The influence of image content on oculomotor plasticity.

When we observe a scene, we shift our gaze to different points of interest via saccadic eye movements. Saccades provide high resolution views of objects and are essential for vision. The successful view of an interesting target might constitute a rewarding experience to the oculomotor system. We measured the influence of image content on learning efficiency in saccade control. We compared meaningful pictures to luminance and spatial frequency-matched random noise images in a saccadic adaptation paradigm. In this paradigm a shift of the target during the saccades results in a gradual increase of saccade amplitude. Stimuli were masked at different times after saccade onset. For immediate masking of the stimuli, as well as for their permanent visibility, saccadic adaptation was similar for both types of targets. However, when stimuli were masked 200 ms after saccade onset, adaptation of saccades directed toward the meaningful target stimuli was significantly greater than that of saccades directed toward noise targets. Thus, the percept of a meaningful image at the saccade landing position facilitates learning of the appropriate parameters for saccadic motor control when time constraints exist. We conclude that oculomotor learning, which is traditionally considered a low-level and highly automatized process, is modulated by the visual content of the image.

Saccadic Adaptation Is Associated with Starting Eye Position

Saccadic adaptation is the motor learning process that keeps saccade amplitudes on target. This process is eye position specific: amplitude adaptation that is induced for a saccade at one particular location in the visual field transfers incompletely to saccades at other locations. In our current study, we investigated wether this eye position signal corresponds to the initial or to the final eye position of the saccade. Each case would have different implications on the mechanisms of adaptation. The initial eye position is not directly available, when the adaptation driving post saccadic error signal is received. On the other hand the final eye position signal is not available, when the motor command for the saccade is calculated. In six human subjects we adapted a saccade of 15 degree amplitude that started at a constant position. We then measured the transfer of adaptation to test saccades of 10 and 20 degree amplitude. In each case we compared test saccades that matched the start position of the adapted saccade to those that matched the target of the adapted saccade. We found significantly more transfer of adaptation to test saccades with the same start position than to test saccades with the same target position. The results indicate that saccadic adaptation is specific to the initial eye position. This is consistent with a previously proposed effect of gain field modulated input from areas like the frontal eye field, the lateral intraparietal area and the superior colliculus into the cerebellar adaptation circuitry.

Meaningful images produce stronger saccadic adaptation

Saccades are made to scan interesting objects in the environment with foveal vision. In the lab, however, they are usually studied with meaningless point targets. Recent experiments showed that vision of a meaningful target affects saccade kinematics, accuracy, and latency. We investigated whether saccadic adaptation, a gradual change of amplitude when the target is shifted during the saccade, is affected by the content of the target. We expected that the motivation to land accurately on a target may be stronger if the target was not a point but a meaningful picture. Thirty-four subjects (27 female) participated in a scanning outward adaptation experiment in which 4 targets (1.8°x2.8°) in rectangular arrangement had to be viewed successively. One of the targets was a small image of a human figure. A control target contained random noise matched for luminance and spatial frequency. The stimulus set shifted in saccade direction during each horizontal saccade by 33% of the initial target distance (12°). In different conditions, stimuli either remained visible throughout the experiment, or were masked after saccade onset, or 200 ms later. Adaptation was quantified by computing the Gain Change (GC) ((amplitudelate-amplitudepre)/initial target distance) for each subject, which was then averaged according to experimental condition. The results showed that saccadic adaptation was greater for saccades directed towards meaningful pictures than towards noise (GChuman 14.14 %, GCnoise 10.83 %). This was also true when the images were masked 200ms after saccade onset such that only a brief glimpse could be obtained (GChuman 13.13%, GCnoise 09.68 %). When images were masked at saccade onset, no significant difference in adaptation was observed (GChuman 10.48%, GCnoise 10.76 %). We conclude that the post-saccadic view of a meaningful image at the saccade landing position facilitates saccadic adaptation. Meeting abstract presented at VSS 2015.