The execution of saccadic eye movements suppresses visual processing of both color and luminance in the early visual cortex of humans.

Our eyes execute rapid, directional movements known as saccades, occurring several times per second, to focus on objects of interest in our environment. During these movements, visual sensitivity is temporarily reduced. Despite numerous studies on this topic, the underlying mechanism remains elusive, including a lingering debate on whether saccadic suppression affects the parvocellular visual pathway. To address this issue, we conducted a study employing steady-state visual evoked potentials (SSVEPs) elicited by chromatic and luminance stimuli while observers performed saccadic eye movements. We also employed an innovative analysis pipeline to enhance the signal-to-noise ratio, yielding superior results compared to the previous method. Our findings revealed a clear suppression effect on SSVEP signals during saccades compared to fixation periods. Notably, this suppression effect was comparable for both chromatic and luminance stimuli. We went further to measure the suppression effect across various contrast levels, which enabled us to model SSVEP responses with contrast response functions. The results suggest that saccades primarily reduce response gain without significantly affecting contrast gain and that this reduction applies uniformly to both chromatic and luminance pathways. In summary, our study provides robust evidence that saccades similarly suppress visual processing in both the parvocellular and magnocellular pathways within the human early visual cortex, as indicated by SSVEP responses. The observation that saccadic eye movements impact response gain rather than contrast gain implies that they influence visual processing through a multiplicative mechanism.NEW & NOTEWORTHY The present study demonstrates that saccadic eye movements reduce the processing of both luminance and chromatic stimuli in the early visual cortex of humans. By modeling the contrast response function, the study further shows that saccades affect visual processing by reducing the response gain rather than altering the contrast gain, suggesting that a multiplicative mechanism of visual attenuation affects both parvocellular and magnocellular pathways.

Laplacian reference is optimal for steady-state visual-evoked potentials.

Steady-state visual-evoked potentials (SSVEPs) are widely used in human neuroscience studies and applications such as brain-computer interfaces (BCIs). Surprisingly, no previous study has systematically evaluated different reference methods for SSVEP analysis, despite that signal reference is crucial for the proper assessment of neural activities. In the present study, using four datasets from our previous SSVEP studies (Chen J, Valsecchi M, Gegenfurtner KR. J Neurophysiol 118: 749-754, 2017; Chen J, Valsecchi M, Gegenfurtner KR. Neuropsychologia 102: 206-216, 2017; Chen J, McManus M, Valsecchi M, Harris LR, Gegenfurtner KR. J Vis 19: 8, 2019) and three public datasets from other studies (Baker DH, Vilidaite G, Wade AR. PLoS Comput Biol 17: e1009507, 2021; Lygo FA, Richard B, Wade AR, Morland AB, Baker DH. NeuroImage 230: 117780, 2021; Vilidaite G, Norcia AM, West RJH, Elliott CJH, Pei F, Wade AR, Baker DH. Proc R Soc B 285: 20182255, 2018), we compared four reference methods: monopolar reference, common average reference, averaged-mastoids reference, and Laplacian reference. The quality of the resulting SSVEP signals was compared in terms of both signal-to-noise ratios (SNRs) and reliability. The results showed that Laplacian reference, which uses signals at the maximally activated electrode after subtracting the average of the nearby electrodes to reduce common noise, gave rise to the highest SNRs. Furthermore, the Laplacian reference resulted in SSVEP signals that were highly reliable across recording sessions or trials. These results suggest that Laplacian reference is optimal for SSVEP studies and applications. Laplacian reference is especially advantageous for SSVEP experiments where short preparation time is preferred as it requires only data from the maximally activated electrode and a few surrounding electrodes.NEW & NOTEWORTHY The present study provides a comprehensive evaluation of the use of different reference methods for steady-state visual-evoked potentials (SSVEPs) and has found that Laplacian reference increases signal-to-noise ratios (SNRs) and enhances reliabilities of SSVEP signals. Thus, the results suggest that Laplacian reference is optimal for SSVEP analysis.

The time course of chromatic adaptation in human early visual cortex revealed by SSVEPs.

Previous studies have identified at least two components of chromatic adaptation: a rapid component with a time scale between tens of milliseconds to a few seconds, and a slow component with a half-life of about 10 to 30 seconds. The basis of the rapid adaptation probably lies in receptor adaptation at the retina. The neural substrate for the slow adaptation remains unclear, although previous psychophysical results hint at the early visual cortex. A promising approach to investigate adaptation effects in the visual cortex is to analyze steady-state visual evoked potentials (SSVEPs) elicited by chromatic stimuli, which typically use long durations of stimulation. Here, we re-analyzed the data from two previous pattern-reversal SSVEP studies. In these experiments (N = 49 observers in total), SSVEPs were elicited by counter-phase flickering color- or luminance-defined grating stimuli for 150 seconds in each trial. By analyzing SSVEPs with short time windows, we found that chromatic SSVEP responses decreased with increasing stimulation duration and reached a lower asymptote within a minute of stimulation. The luminance SSVEPs did not show any systematic adaptation. The time course of chromatic SSVEPs can be well described by an exponential decay function with a half-life of about 20 seconds, which is very close to previous psychophysical reports. Despite the difference in stimuli between the current and previous studies, the coherent time course may indicate a more general adaptation mechanism in the early visual cortex. In addition, the current result also provides a guide for future color SSVEP studies in terms of either avoiding or exploiting this adaptation effect.

Screen size matches of familiar images are biased by canonical size, rather than showing a memory size effect.

Being confronted with the depiction of a familiar object activates a number of properties of the object that are stored in memory. Memory properties such as color and size have been shown to interfere with the processing of the color and of the size of the depiction, so that that reaction times are longer when the color or size of the depiction are incongruent with the stored knowledge about the object. In the case of color, it is known that the memorized information also affects the appearance of the depiction, for example when a gray banana appears slightly yellow, a phenomenon known as memory color effect. Here, I tested whether a memory size effect also occurs. To this aim, I conducted one experiment where observers matched either the screen size or the real-world size of pairs of animals or vehicles. The results indicate that the screen matches are biased in the same direction as the real-world size matches, opposite of what would be predicted by a memory color effect. This result was replicated in a second experiment using a different and larger set of animal images. Overall, I confirm that observers cannot ignore the real-world size information when they attempt to match the screen size of two items, although this results in a bias towards the canonical size of the items, rather than in a memory size effect.

Underconfidence in peripheral vision.

Our visual experience appears uniform across the visual field, despite the poor resolution of peripheral vision. This may be because we do not notice that we are missing details in the periphery of our visual field and believe that peripheral vision is just as rich as central vision. In other words, the uniformity of the visual scene could be explained by a metacognitive bias. We deployed a confidence forced-choice method to measure metacognitive performance in peripheral as compared to central vision. Participants judged the orientation of gratings presented in central and peripheral vision, and reported whether they thought they were more likely to be correct in the perceptual decision for the central or for the peripheral stimulus. Observers were underconfident in the periphery: higher sensory evidence in the periphery was needed to equate confidence choices between central and peripheral perceptual decisions. When performance on the central and peripheral tasks was matched, observers were still more confident in their ability to report the orientation of the central gratings over the one of the peripheral gratings. In a second experiment, we measured metacognitive sensitivity, as the difference in perceptual sensitivity between perceptual decisions that are chosen with high confidence and decisions that are chosen with low confidence. Results showed that metacognitive sensitivity is lower when participants compare central to peripheral perceptual decisions compared to when they compare peripheral to peripheral or central to central perceptual decisions. In a third experiment, we showed that peripheral underconfidence does not arise because observers based confidence judgments on stimulus size or contrast range rather than on perceptual performance. Taken together, results indicate that humans are impaired in comparing central with peripheral perceptual performance, but metacognitive biases cannot explain our impression of uniformity, as this would require peripheral overconfidence.

Softness and weight from shape: Material properties inferred from local shape features.

Object shape is an important cue to material identity and for the estimation of material properties. Shape features can affect material perception at different levels: at a microscale (surface roughness), mesoscale (textures and local object shape), or megascale (global object shape) level. Examples for local shape features include ripples in drapery, clots in viscous liquids, or spiraling creases in twisted objects. Here, we set out to test the role of such shape features on judgments of material properties softness and weight. For this, we created a large number of novel stimuli with varying surface shape features. We show that those features have distinct effects on softness and weight ratings depending on their type, as well as amplitude and frequency, for example, increasing numbers and pointedness of spikes makes objects appear harder and heavier. By also asking participants to name familiar objects, materials, and transformations they associate with our stimuli, we can show that softness and weight judgments do not merely follow from semantic associations between particular stimuli and real-world object shapes. Rather, softness and weight are estimated from surface shape, presumably based on learned heuristics about the relationship between a particular expression of surface features and material properties. In line with this, we show that correlations between perceived softness or weight and surface curvature vary depending on the type of surface feature. We conclude that local shape features have to be considered when testing the effects of shape on the perception of material properties such as softness and weight.

A comparison of the temporal and spatial properties of trans-saccadic perceptual recalibration and saccadic adaptation.

Repeated exposure to a consistent trans-saccadic step in the position of the saccadic target reliably produces a change of saccadic gain, a well-established trans-saccadic motor learning phenomenon known as saccadic adaptation. Trans-saccadic changes can also produce perceptual effects. Specifically, a systematic increase or decrease in the size of the object that is being foveated changes the perceptually equivalent size between fovea and periphery. Previous studies have shown that this recalibration of perceived size can be established within a few dozen trials, persists overnight, and generalizes across hemifields. In the current study, we use a novel adjustment paradigm to characterize both temporally and spatially the learning process that subtends this form of recalibration, and directly compare its properties to those of saccadic adaptation. We observed that sinusoidal oscillations in the amplitude of the trans-saccadic change produce sinusoidal oscillations in the reported peripheral size, with a lag of under 10 trials. This is qualitatively similar to what has been observed in the case of saccadic adaptation. We also tested whether learning is generalized to the mirror location on the opposite hemifield for both size recalibration and saccade adaptation. Here the results were markedly different, showing almost complete generalization for recalibration and no generalization for saccadic adaptation. We conclude that perceptual and visuomotor consequences of trans-saccadic changes rely on learning mechanisms that are distinct but develop on similar time scales.

A review of interactions between peripheral and foveal vision.

Visual processing varies dramatically across the visual field. These differences start in the retina and continue all the way to the visual cortex. Despite these differences in processing, the perceptual experience of humans is remarkably stable and continuous across the visual field. Research in the last decade has shown that processing in peripheral and foveal vision is not independent, but is more directly connected than previously thought. We address three core questions on how peripheral and foveal vision interact, and review recent findings on potentially related phenomena that could provide answers to these questions. First, how is the processing of peripheral and foveal signals related during fixation? Peripheral signals seem to be processed in foveal retinotopic areas to facilitate peripheral object recognition, and foveal information seems to be extrapolated toward the periphery to generate a homogeneous representation of the environment. Second, how are peripheral and foveal signals re-calibrated? Transsaccadic changes in object features lead to a reduction in the discrepancy between peripheral and foveal appearance. Third, how is peripheral and foveal information stitched together across saccades? Peripheral and foveal signals are integrated across saccadic eye movements to average percepts and to reduce uncertainty. Together, these findings illustrate that peripheral and foveal processing are closely connected, mastering the compromise between a large peripheral visual field and high resolution at the fovea.

Saccadic suppression measured by steady-state visual evoked potentials.

Visual sensitivity is severely impaired during the execution of saccadic eye movements. This phenomenon has been extensively characterized in human psychophysics and nonhuman primate single-neuron studies, but a physiological characterization in humans is less established. Here, we used a method based on steady-state visually evoked potential (SSVEP), an oscillatory brain response to periodic visual stimulation, to examine how saccades affect visual sensitivity. Observers made horizontal saccades back and forth, while horizontal black-and-white gratings flickered at 5-30 Hz in the background. We analyzed EEG epochs with a length of 0.3 s either centered at saccade onset (saccade epochs) or centered at fixations half a second before the saccade (fixation epochs). Compared with fixation epochs, saccade epochs showed a broadband power increase, which most likely resulted from saccade-related EEG activity. The execution of saccades, however, led to an average reduction of 57% in the SSVEP amplitude at the stimulation frequency. This result provides additional evidence for an active saccadic suppression in the early visual cortex in humans. Compared with previous functional MRI and EEG studies, an advantage of this approach lies in its capability to trace the temporal dynamics of neural activity throughout the time course of a saccade. In contrast to previous electrophysiological studies in nonhuman primates, we did not find any evidence for postsaccadic enhancement, even though simulation results show that our method would have been able to detect it. We conclude that SSVEP is a useful technique to investigate the neural correlates of visual perception during saccadic eye movements in humans. NEW & NOTEWORTHY We make fast ballistic saccadic eye movements a few times every second. At the time of saccades, visual sensitivity is severely impaired. The present study uses steady-state visually evoked potentials to reveal a neural correlate of the fine temporal dynamics of these modulations at the time of saccades in humans. We observed a strong reduction (57%) of visually driven neural activity associated with saccades but did not find any evidence for postsaccadic enhancement.

Steady-state visually evoked potentials reveal partial size constancy in early visual cortex.

Our visual system maintains a stable representation of object size when viewing distance, and thus retinal size, changes. Previous studies have revealed that the extent of an object's representation in V1 shows systematic deviations from strict retinotopy when the object is perceived to be at different distances. It remains unknown, however, to what degree V1 activity accounts for perceptual size constancy. We investigated the neural correlates of size-constancy using steady-state visually evoked potentials (SSVEP) known to originate in early visual cortex. Flickering stimuli of various sizes were placed at a viewing distance of 40 cm and stimuli twice as large were shown at 80 cm. Thus both sets of stimuli had identical retinal sizes. At a constant viewing distance, SSVEP amplitude increased as a function of increasing retinal size. Crucially, SSVEP was larger when stimuli of a given retinal size were presented at 80 cm compared with at 40 cm independent of flicker frequency. Experiments were repeated and extended in virtual reality. Our results agree with previous findings showing that V1 activity plays a role in size constancy. Furthermore, we estimated the degree of the neural correction for the SSVEP as being close to 50% of the perceptual size constancy. This was the case in all experiments, independent of the effectiveness of perceptual size constancy. We conclude that retinotopy in V1 does get quite massively adjusted by perceived size, but not to the same extent as perceptual judgments.

Repulsive Serial Effects in Visual Numerosity Judgments.

We investigated how the approximate perceived numerosity of ensembles of visual elements is modulated by the numerosity of previously viewed ensembles depending on whether the first ensemble is held in visual working memory or not. We show that the numerosity of the previously seen ensemble has a repulsive effect, that is, a stimulus with high numerosity induces an underestimation of the following one and vice versa. This repulsive effect is present regardless of whether the first stimulus is memorized or not. While subtle changes of the experimental paradigm can have major consequences for the nature of interstimulus dependencies in perception, generally speaking the fact that we found such effects in a visual numerosity estimation task confirms that the process by which human observers produce estimates of the number of elements bears analogies to the processes that lead to the perception of visual dimensions such as orientation.

Prediction shapes peripheral appearance.

Peripheral perception is limited in terms of visual acuity, contrast sensitivity, and positional uncertainty. In the present study we used an image-manipulation algorithm (the Eidolon Factory) based on a formal description of the visual field as a tool to investigate how peripheral stimuli appear in the presence of such limitations. Observers were asked to match central and peripheral stimuli, both configurations of superimposed geometric shapes and patches of natural images, in terms of the parameters controlling the amplitude of the perturbation (reach) and the cross-scale similarity of the perturbation (coherence). We found that observers systematically tended to report the peripheral stimuli as having shorter reach and higher coherence. This means that their matches both were less distorted and had sharper edges relative to the actual stimulus. Overall, the results indicate that the way we see objects in our peripheral visual field is complemented by our assumptions about the way the same objects would appear if they were viewed foveally.

Enhanced brain responses to color during smooth-pursuit eye movements.

Eye movements alter visual perceptions in a number of ways. During smooth-pursuit eye movements, previous studies reported decreased detection threshold for colored stimuli and for high-spatial-frequency luminance stimuli, suggesting a boost in the parvocellular system. The present study investigated the underlying neural mechanism using EEG in human participants. Participants followed a moving target with smooth-pursuit eye movements while steady-state visually evoked potentials (SSVEPs) were elicited by equiluminant red-green flickering gratings in the background. SSVEP responses to colored gratings were 18.9% higher during smooth pursuit than during fixation. There was no enhancement of SSVEPs by smooth pursuit when the flickering grating was defined by luminance instead of color. This result provides physiological evidence that the chromatic response in the visual system is boosted by the execution of smooth-pursuit eye movements in humans. Because the response improvement is thought to be the result of an improved response in the parvocellular system, SSVEPs to equiluminant stimuli could provide a direct test of parvocellular signaling, especially in populations where collecting an explicit behavioral response from the participant is not feasible.NEW & NOTEWORTHY We constantly move our eyes when we explore the world. Eye movements alter visual perception in various ways. The smooth-pursuit eye movements have been shown to boost color sensitivity. We recorded steady-state visually evoked potentials to equiluminant chromatic flickering stimuli and observed increased steady-state visually evoked potentials when participants smoothly pursued a moving target compared with when they maintained fixation. This work provides direct neurophysiological evidence for the parvocellular boost by smooth-pursuit eye movements in humans.

Foveal to peripheral extrapolation of brightness within objects.

Peripheral viewing is characterized by poor resolution and distortions as compared to central viewing; nevertheless, when we move our gaze around, the visual scene does not appear to change. One possible mechanism leading to perceptual uniformity would be that peripheral appearance is extrapolated based on foveal information. Here we investigate foveal-to-peripheral extrapolation in the case of the perceived brightness of an object's surface. While fixating a spot on the rendered object, observers were asked to adjust the brightness of a disc to match a peripherally viewed target area on the surface of the same object. Being forced to fixate a better illuminated point led to brighter matches as compared to fixating points in the shadow, indicating that foveal brightness information was extrapolated. When observers fixated additional points outside of the object on the scene's background, fixated brightness had no effect on the brightness match. Results indicate that our visual system uses the brightness of the foveally viewed surface area to estimate the brightness of areas in the periphery. However, this mechanism is selectively applied within an object's boundary.

Eidolons: Novel stimuli for vision research.

Meanings and qualities are fundamental attributes of visual awareness. We propose "eidolons" as a tool for establishing equivalence classes of appearance along meaningful dimensions. The "eidolon factory" is an algorithm that generates stimuli in such a meaningful and transparent way. The algorithm allows us to focus on location, scale, and size of perceptually salient structures, proto-objects, and perhaps even semantics rather than global overall parameters, such as contrast and spatial frequency. The eidolon factory is based on models of the psychogenesis of visual awareness. It affects the image in terms of the disruption of image structure across space and spatial scales. This is a very general method with many potential applications. We illustrate a few instances. We present results for the example of tarachopic amblyopia, showing that scrambled vision is indeed an apt interpretation.

Role of motor execution in the ocular tracking of self-generated movements.

When human observers track the movements of their own hand with their gaze, the eyes can start moving before the finger (i.e., anticipatory smooth pursuit). The signals driving anticipation could come from motor commands during finger motor execution or from motor intention and decision processes associated with self-initiated movements. For the present study, we built a mechanical device that could move a visual target either in the same direction as the participant's hand or in the opposite direction. Gaze pursuit of the target showed stronger anticipation if it moved in the same direction as the hand compared with the opposite direction, as evidenced by decreased pursuit latency, increased positional lead of the eye relative to target, increased pursuit gain, decreased saccade rate, and decreased delay at the movement reversal. Some degree of anticipation occurred for incongruent pursuit, indicating that there is a role for higher-level movement prediction in pursuit anticipation. The fact that anticipation was larger when target and finger moved in the same direction provides evidence for a direct coupling between finger and eye motor commands.

LRP predicts smooth pursuit eye movement onset during the ocular tracking of self-generated movements.

Several studies have indicated that human observers are very efficient at tracking self-generated hand movements with their gaze, yet it is not clear whether this is simply a by-product of the predictability of self-generated actions or if it results from a deeper coupling of the somatomotor and oculomotor systems. In a first behavioral experiment we compared pursuit performance as observers either followed their own finger or tracked a dot whose motion was externally generated but mimicked their finger motion. We found that even when the dot motion was completely predictable in terms of both onset time and kinematics, pursuit was not identical to that produced as the observers tracked their finger, as evidenced by increased rate of catch-up saccades and by the fact that in the initial phase of the movement gaze was lagging behind the dot, whereas it was ahead of the finger. In a second experiment we recorded EEG in the attempt to find a direct link between the finger motor preparation, indexed by the lateralized readiness potential (LRP) and the latency of smooth pursuit. After taking into account finger movement onset variability, we observed larger LRP amplitudes associated with earlier smooth pursuit onset across trials. The same held across subjects, where average LRP onset correlated with average eye latency. The evidence from both experiments concurs to indicate that a strong coupling exists between the motor systems leading to eye and finger movements and that simple top-down predictive signals are unlikely to support optimal coordination.

Optimal sampling of visual information for lightness judgments.

The variable resolution and limited processing capacity of the human visual system requires us to sample the world with eye movements and attentive processes. Here we show that where observers look can strongly modulate their reports of simple surface attributes, such as lightness. When observers matched the color of natural objects they based their judgments on the brightest parts of the objects; at the same time, they tended to fixate points with above-average luminance. When we forced participants to fixate a specific point on the object using a gaze-contingent display setup, the matched lightness was higher when observers fixated bright regions. This finding indicates a causal link between the luminance of the fixated region and the lightness match for the whole object. Simulations with rendered physical lighting show that higher values in an object's luminance distribution are particularly informative about reflectance. This sampling strategy is an efficient and simple heuristic for the visual system to achieve accurate and invariant judgments of lightness.

Variations in daylight as a contextual cue for estimating season, time of day, and weather conditions.

Experience and experiments on human color constancy (i.e., Arend & Reeves, 1986; Craven & Foster, 1992) tell us that we are capable of judging the illumination. However, when asked to make a match of the illuminant's color and brightness, human observers seem to be quite poor (Granzier, Brenner, & Smeets, 2009a). Here we investigate whether human observers use (rather than match) daylight for estimating ecologically important dimensions: time of year, time of day, and outdoor temperature. In the first three experiments we had our observers evaluate calibrated color images of an outdoor urban scene acquired throughout a year. Although some observers could estimate the month and the temperature, overall they were quite poor at judging the time of day. In particular, observers were not able to discriminate between morning and afternoon pictures even when they were allowed to compare multiple images captured on the same day (Experiment 3). However, observers could distinguish between midday and sunset and sunrise daylight. Classification analysis showed that, given a perfect knowledge of its variation, an ideal observer could have performed the task over chance only considering the average chromatic variation in the picture. Instead, our observers reported using shadows to detect the position of the sun in order to estimate the time of day. However, this information is highly unreliable without knowledge of the orientation of the scene. In Experiment 4 we used an LED chamber in order to present our observers with lights whose chromaticity and illuminance varied along the daylight locus, thus isolating the light cues from the sun position cue. We conclude that discriminating the slight variations in chromaticity and brightness, which potentially distinguish morning and afternoon illuminations, lies beyond the ability of human observers.

Differential effects of visual attention and working memory on binocular rivalry.

The investigation of cognitive influence on binocular rivalry has a long history. However, the effects of visual WM on rivalry have never been studied so far. We examined top-down modulation of rivalry perception in four experiments to compare the effects of visual WM and sustained selective attention: In the first three experiments we failed to observe any sustained effect of the WM content; only the color of the memory probe was found to prime the initially dominant percept. In Experiment 4 we found a clear effect of sustained attention on rivalry both in terms of the first dominant percept and of the overall dominance when participants were involved in a tracking task. Our results provide an example of dissociation between visual WM and selective attention, two phenomena which otherwise functionally overlap to a large extent. Furthermore, our study highlights the importance of the task employed to engage cognitive resources: The observed perceptual epiphenomena of binocular rivalry are indicative of visual competition at an early stage, which is not affected by WM but is still susceptible to attention influence as long as the observer's attention is constrained to one of the two rival images via a specific concomitant task.