Suppression without inhibition: how retinal computation contributes to saccadic suppression.
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ABSTRACT:
SUBMITTER: Idrees S
PROVIDER: S-EPMC9276698 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description: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.
| S-EPMC8018005 | biostudies-literature
Project description:We make fast, ballistic eye movements called saccades more often than our heart beats. Although every saccade causes a large movement of the image of the environment on our retina, we never perceive this motion. This aspect of perceptual stability is often referred to as saccadic suppression: a reduction of visual sensitivity around the time of saccades. Here, we investigated the neural basis of this perceptual phenomenon with extracellular recordings from awake, behaving monkeys in the middle temporal, medial superior temporal, ventral intraparietal, and lateral intraparietal areas. We found that, in each of these areas, the neural response to a visual stimulus changes around an eye movement. The perisaccadic response changes are qualitatively different in each of these areas, suggesting that they do not arise from a change in a common input area. Importantly, our data show that the suppression in the dorsal stream starts well before the eye movement. This clearly shows that the suppression is not just a consequence of the changes in visual input during the eye movement but rather must involve a process that actively modulates neural activity just before a saccade.
| S-EPMC2787621 | biostudies-other
Project description:Visual sensitivity, probed through perceptual detectability of very brief visual stimuli, is strongly impaired around the time of rapid eye movements. This robust perceptual phenomenon, called saccadic suppression, is frequently attributed to active suppressive signals that are directly derived from eye movement commands. Here we show instead that visual-only mechanisms, activated by saccade-induced image shifts, can account for all perceptual properties of saccadic suppression that we have investigated. Such mechanisms start at, but are not necessarily exclusive to, the very first stage of visual processing in the brain, the retina. Critically, neural suppression originating in the retina outlasts perceptual suppression around the time of saccades, suggesting that extra-retinal movement-related signals, rather than causing suppression, may instead act to shorten it. Our results demonstrate a far-reaching contribution of visual processing mechanisms to perceptual saccadic suppression, starting in the retina, without the need to invoke explicit motor-based suppression commands.
| S-EPMC7181657 | biostudies-literature
Project description:Introspection makes it clear that we do not see the visual motion generated by our saccadic eye movements. We refer to the lack of awareness of the motion across the retina that is generated by a saccade as saccadic omission [1]: the visual stimulus generated by the saccade is omitted from our subjective awareness. In the laboratory, saccadic omission is often studied by investigating saccadic suppression, the reduction in visual sensitivity before and during a saccade (see Ross et al. [2] and Wurtz [3] for reviews). We investigated whether perceptual stability requires that a mechanism like saccadic suppression removes perisaccadic stimuli from visual processing to prevent their presumed harmful effect on perceptual stability [4, 5]. Our results show that a stimulus that undergoes saccadic omission can nevertheless generate a shape contrast illusion. This illusion can be generated when the inducer and test stimulus are separated in space and is therefore thought to be generated at a later stage of visual processing [6]. This shows that perceptual stability is attained without removing stimuli from processing and suggests a conceptually new view of perceptual stability in which perisaccadic stimuli are processed by the early visual system, but these signals are prevented from reaching awareness at a later stage of processing.
| S-EPMC3254668 | biostudies-literature
Project description:Processing of visual information in the central (foveal) and peripheral visual field is vastly different. To achieve a homogeneous representation of the visual world across eye movements, the visual system needs to compensate for these differences. By introducing subtle changes between peripheral and foveal inputs across saccades, one can test this compensation. We morphed shapes between a triangle and a circle and presented two different change directions (circularity decrease or increase) at varying magnitudes across a saccade. In a change-discrimination task, observers disproportionally often reported percepts of circularity increase. To test the relationship with visual-field differences, we measured perception when shapes were exclusively presented either in the periphery (before a saccade), or in the fovea (after a saccade). We found that overall shapes were perceived as more circular before than after a saccade and the more pronounced this difference was for a participant, the smaller was their circularity-increase bias in the change-discrimination task. We propose that visual-field differences have a direct and an indirect influence on transsaccadic perception of shape change. The direct influence is based on the distinct appearance of shape in the central and peripheral visual field in a trial, causing an increase of the perceptual magnitude of circularity-decrease changes. The indirect influence is based on long-term build-up of transsaccadic expectations; if a change is opposite (circularity increase) to the expectation (circularity decrease), it should elicit a strong error signal facilitating change detection. We discuss the concept of transsaccadic expectations and theoretical implications for transsaccadic perception of other feature changes.
| S-EPMC7611036 | biostudies-literature
Project description:Saccadic eye movements are known to cause saccadic suppression, a temporary reduction in visual sensitivity and visual cortical firing rates. While saccadic suppression has been well characterized at the level of perception and single neurons, relatively little is known about the visual cortical networks governing this phenomenon. Here we examine the effects of saccadic suppression on distinct neural subpopulations within visual area V4. We find subpopulation-specific differences in the magnitude and timing of peri-saccadic modulation. Input-layer neurons show changes in firing rate and inter-neuronal correlations prior to saccade onset, and putative inhibitory interneurons in the input layer elevate their firing rate during saccades. A computational model of this circuit recapitulates our empirical observations and demonstrates that an input-layer-targeting pathway can initiate saccadic suppression by enhancing local inhibitory activity. Collectively, our results provide a mechanistic understanding of how eye movement signaling interacts with cortical circuitry to enforce visual stability.
| S-EPMC10528056 | biostudies-literature
Project description:Saccadic eye movements modulate visual perception: they initiate and terminate high acuity vision at a certain location in space, but before and during their execution visual contrast sensitivity is strongly attenuated for 100 to 200 ms. Transient perisaccadic perceptual distortions are assumed to be an important mechanism to maintain visual stability. Little is known about age effects on saccadic suppression, even though for healthy adults other major age-related changes are well documented, like a decrease of visual contrast sensitivity for intermediate and high spatial frequencies or an increase of saccade latencies. Here, we tested saccadic suppression of luminance and isoluminant chromatic flashes in 100 participants from eight to 78 years. To estimate the effect of saccadic suppression on contrast sensitivity, we used a two-alternative forced choice (2AFC) design and an adaptive staircase procedure to modulate the luminance or chromatic contrast of a flashed detection target during fixation and 15 ms after saccade onset. The target was a single horizontal luminance or chromatic line flashed 2° above or below the fixation or saccade target. Compared to fixation, average perisaccadic contrast sensitivity decreased significantly by 66% for luminance and by 36% for color. A significant correlation was found for the strength of saccadic suppression of luminance and color. However, a small age effect was found only for the strength of saccadic suppression of luminance, which increased from 64% to 70% from young to old age. We conclude that saccadic suppression for luminance and color is present in most participants independent of their age and that mechanisms of suppression stay relatively stable during healthy aging.
| S-EPMC8237129 | biostudies-literature
Project description:Humans do not notice small displacements to objects that occur during saccades, termed saccadic suppression of displacement (SSD), and this effect is reduced when a blank is introduced between the pre- and postsaccadic stimulus (Bridgeman, Hendry, & Stark, 1975; Deubel, Schneider, & Bridgeman, 1996). While these effects have been studied extensively in adults, it is unclear how these phenomena are characterized in children. A potentially related mechanism, saccadic suppression of contrast sensitivity-a prerequisite to achieve a stable percept-is stronger for children (Bruno, Brambati, Perani, & Morrone, 2006). However, the evidence for how transsaccadic stimulus displacements may be suppressed or integrated is mixed. While they can integrate basic visual feature information from an early age, they cannot integrate multisensory information (Gori, Viva, Sandini, & Burr, 2008; Nardini, Jones, Bedford, & Braddick, 2008), suggesting a failure in the ability to integrate more complex sensory information. We tested children 7 to 12 years old and adults 19 to 23 years old on their ability to perceive intrasaccadic stimulus displacements, with and without a postsaccadic blank. Results showed that children had stronger SSD than adults and a larger blanking effect. Children also had larger undershoots and more variability in their initial saccade endpoints, indicating greater intrinsic uncertainty, and they were faster in executing corrective saccades to account for these errors. Together, these results suggest that children may have a greater internal expectation or prediction of saccade error than adults; thus, the stronger SSD in children may be due to higher intrinsic uncertainty in target localization or saccade execution.
| S-EPMC7571331 | biostudies-literature
Project description:By repeating saccades unconsciously, humans explore the surrounding world every day. Saccades inevitably move external visual images across the retina at high velocity; nonetheless, healthy humans don't perceive transient blurring of the visual scene during saccades. This perceptual stability is referred to as saccadic suppression. Functional suppression is believed to take place transiently in the visual systems, but it remains unknown how commonly or differentially the human occipital lobe activities are suppressed at the large-scale cortical network level. We determined the spatial-temporal dynamics of intracranially-recorded gamma activity at 80-150 Hz around spontaneous saccades under no-task conditions during wakefulness and those in darkness during REM sleep. Regardless of wakefulness or REM sleep, a small degree of attenuation of gamma activity was noted in the occipital regions during saccades, most extensively in the polar and least in the medial portions. Longer saccades were associated with more intense gamma-attenuation. Gamma-attenuation was subsequently followed by gamma-augmentation most extensively involving the medial and least involving the polar occipital region. Such gamma-augmentation was more intense during wakefulness and temporally locked to the offset of saccades. The polarities of initial peaks of perisaccadic event-related potentials (ERPs) were frequently positive in the medial and negative in the polar occipital regions. The present study, for the first time, provided the electrophysiological evidence that human occipital cortices differentially exert perisaccadic modulation. Transiently suppressed sensitivity of the primary visual cortex in the polar region may be an important neural basis for saccadic suppression. Presence of occipital gamma-attenuation even during REM sleep suggests that saccadic suppression might be exerted even without external visual inputs. The primary visual cortex in the medial region, compared to the polar region, may be more sensitive to an upcoming visual scene provided at the offset of each saccade.
| S-EPMC3815968 | biostudies-literature
Project description:During covert and pre-saccadic attentional shifts, it is unclear how facilitation and suppression processes interact for target selection. A recent countermanding task pointed to greater suppression at unattended locations during trials with saccades compared to trials without saccades (i.e., fixation and successful stop trials), whereas target facilitation did not differ. It is unknown whether this finding is restricted to countermanding paradigms that involve inhibitory processes. To test this, we adapted Gaspelin and colleagues (2015)'s attention capture task where, within the same block, one location was primed with frequent line discrimination trials, and all locations were occasionally probed using letters report trials. Participants also performed a baseline condition without priming. We tested 15 participants and examined how performance at non-primed locations was affected by covert versus pre-saccadic attention in blocks of four or six items, as well as by position from the primed location and timing from saccade onset. For both attention conditions, letter report at non-primed locations was worse compared to baseline, demonstrating suppression, and letter report at primed location was better, demonstrating facilitation. In saccades trials, letter report was better at primed locations and worse at non-primed locations compared to fixation trials. The timing of this additional pre-saccadic suppression differed from saccadic suppression. In both attention conditions, suppression was greater when primed and non-primed locations were within the same hemifield or in diagonal opposite quadrants. These results confirmed that attention preceding saccade execution suppressed non-primed locations to a larger extent than covert attention, with the same spatial quadrant effect.
| S-EPMC9819743 | biostudies-literature