Learning to silence saccadic suppression

Perceptual stability is facilitated by a decrease in visual sensitivity during rapid eye movements, called saccadic suppression. While a large body of evidence demonstrates that saccadic programming is plastic, little is known about whether the perceptual consequences of saccades can be modified. Here, we demonstrate that saccadic suppression is attenuated during learning on a standard visual detection-in-noise task, to the point that it is effectively silenced. Across a period of 7 days, 44 participants were trained to detect brief, low-contrast stimuli embedded within dynamic noise, while eye position was tracked. Although instructed to fixate, participants regularly made small fixational saccades. Data were accumulated over a large number of trials, allowing us to assess changes in performance as a function of the temporal proximity of stimuli and saccades. This analysis revealed that improvements in sensitivity over the training period were accompanied by a systematic change in the impact of saccades on performance—robust saccadic suppression on day 1 declined gradually over subsequent days until its magnitude became indistinguishable from zero. This silencing of suppression was not explained by learning-related changes in saccade characteristics and generalized to an untrained retinal location and stimulus orientation. Suppression was restored when learned stimulus timing was perturbed, consistent with the operation of a mechanism that temporarily reduces or eliminates saccadic suppression, but only when it is behaviorally advantageous to do so. Our results indicate that learning can circumvent saccadic suppression to improve performance, without compromising its functional benefits in other viewing contexts.

Humans continuously sample the external world using frequent and rapid gaze shifts called saccades, which cause the image of the visual scene to sweep across the retina. The fact that we remain unaware of these frequent disruptions to visual input and maintain a stable perception of the world has intrigued generations of vision scientists (1–9). While early researchers attributed the lack of awareness of intrasaccadic stimulation to a form of central anesthesia (6), it is most commonly associated with the phenomenon of saccadic suppression—a reduction in the visibility of brief flashes presented around the time of a saccade. A large number of studies spanning more than a century have reported changes in the threshold for, or probability of detecting, brief perisaccadic stimuli. These effects have been demonstrated for different classes of saccadic eye movements and under a range of experimental conditions; for example, with large reactive saccades initiated under instruction, smaller spontaneous saccades during attempted fixation (10–12), targets presented on clear (11, 13) and textured (10, 14, 15) backgrounds, and in both the central (16, 17) and peripheral (11, 14, 18, 19) visual field. Despite widespread agreement that saccadic suppression is a robust phenomenon, consensus regarding its underlying mechanisms has proved elusive. During natural viewing, it is likely that the postsaccadic visual scene acts to mask the intrasaccadic image, which has been blurred by its rapid translation across the retina (4, 20–24). However, some researchers have argued for an active form of suppression, triggered by an extraretinal signal or corollary discharge of the saccadic eye movement (refs. 8 and 25–28; for counter arguments, see refs. 3, 4, and 23).Saccades were classically considered to be highly stereotyped movements, reflecting the fact that they have relatively stable kinematic properties that are resistant to voluntary control and modification by training (29, 30). However, it is becoming increasingly clear that most characteristics of saccades can be modified. Evidence for saccadic plasticity comes from a variety of sources. Rather than being fixed, the “main sequence” relationship between saccade velocity and amplitude can be manipulated by visual stimulation (31) or reward (32, 33). When saccadic targets are consistently displaced by an experimenter during flight, individuals quickly adapt the amplitude (34–36) or direction (37) of future saccades to minimize landing errors. Repeated training on oculomotor tasks has been shown to decrease saccadic reaction times and increase the frequency of a variety of saccade types (38–41). In addition, close examination of eye movements has revealed that saccade production adjusts to meet current behavioral goals. During the threading of a needle, for example, small spontaneous saccades move the eye regularly between the tip of the thread and the eye of the needle in order to estimate relative alignment between the two (42). In addition, saccade rate and amplitude distributions are influenced by a variety of factors such as task complexity (43, 44), whether an individual is performing free-viewing or visual search (45), the size of the visual scene (46), and how informative an image region is (47).In contrast to the growing literature documenting different forms of oculomotor plasticity, far less is known about the extent to which the perceptual consequences of saccades can be modified. This is partly due to ongoing debate over the relative contribution of active (extraretinal) and passive (masking) mechanisms to saccadic suppression, which has dominated much of the work in this area. Given its hypothesized functional role in maintaining visual stability across eye movements, it is tempting to assume that saccadic suppression must be a stable, perhaps even hard-wired effect that is impervious to training. Empirical validation of this assumption is lacking, however, as most studies aggregate perisaccadic visual judgements (often in a small number of well-trained observers) across multiple testing sessions. Two recent studies have reported learned improvements in visual task performance following training with stimuli consistently presented before (48) or during (49) saccades. While these findings demonstrate that perceptual learning is possible around the time of saccades, the role of suppression in this process remains unclear. Is saccadic suppression impervious to learning, placing an upper limit on the amount of improvement that is achievable with training? Or can learning modify saccadic suppression in a manner that actively contributes to improvements in sensory performance?To address these questions, we measured visual sensitivity to a brief peripheral target stimulus embedded in luminance noise. This task consistently shows large improvements in performance with practice, and variants have been used extensively to investigate the characteristics and mechanisms of perceptual learning. Rather than direct subjects to make large saccades around the time of stimulus presentation, we instead exploited spontaneously occurring saccades during attempted fixation. This approach had several advantages. From a practical perspective, it enabled us to make use of a standard perceptual learning paradigm, with the only addition being noninvasive monitoring of eye position. Moreover, it avoided the conflict of having to instruct subjects to perform the task as accurately as possible, while also making eye movements that would likely impair their ability to do so. While the majority of suppression studies focus on a small number of highly trained individuals, we were able to instead use a larger group of completely naive subjects without the need for any eye movement training. Although saccadic suppression has generally been investigated using large voluntary saccades, a body of evidence suggests that the visual consequences of fixational and voluntary saccades are comparable (12, 25, 26, 50–53), consistent with a view that fixational saccades are part of a saccadic continuum that is simply delineated by the magnitude of the eye movement (28, 51, 54–57).