Oculomotor randomness is higher in autistic children and increases with the severity of symptoms.

A variety of studies have suggested that at least some children with autism spectrum disorder (ASD) view the world differently. Differences in gaze patterns as measured by eye tracking have been demonstrated during visual exploration of images and natural viewing of movies with social content. Here we analyzed the temporal randomness of saccades and blinks during natural viewing of movies, inspired by a recent measure of "randomness" applied to micro-movements of the hand and head in ASD (Torres et al., 2013; Torres & Denisova, 2016). We analyzed a large eye-tracking dataset of 189 ASD and 41 typically developing (TD) children (1-11 years old) who watched three movie clips with social content, each repeated twice. We found that oculomotor measures of randomness, obtained from gamma parameters of inter-saccade intervals (ISI) and blink duration distributions, were significantly higher in the ASD group compared with the TD group and were correlated with the ADOS comparison score, reflecting increased "randomness" in more severe cases. Moreover, these measures of randomness decreased with age, as well as with higher cognitive scores in both groups and were consistent across repeated viewing of each movie clip. Highly "random" eye movements in ASD children could be associated with high "neural variability" or noise, poor sensory-motor control, or weak engagement with the movies. These findings could contribute to the future development of oculomotor biomarkers as part of an integrative diagnostic tool for ASD.

Oculomotor inhibition markers of working memory load.

Involuntary eye movements occur constantly even during fixation and were shown to convey information about cognitive processes. They are inhibited momentarily in response to external stimuli (oculomotor inhibition, OMI), with a time and magnitude that depend on stimulus saliency, attention, and expectations. It was recently shown that the working memory load for numbers modulates the microsaccade rate; however, the generality of the effect and its temporal properties remain unclear. Our goal was to investigate the relationship between OMI and the working memory load for simple colored shapes. Participants (N = 26) maintained their fixation while their eyes were tracked; they viewed briefly flashed colored shapes accompanied by small arrows indicating the shapes to be memorized (1/2/3). After a retention period, a probe shape appeared for matching. The microsaccade rate modulation and temporal properties were analyzed for the memory encoding, maintenance, and retrieval phases. Microsaccade inhibition was stronger when more shapes were memorized, and performance improved when microsaccades were suppressed during maintenance and retrieval. This occurred even though the physical stimuli were identical in number under all conditions. Thus, oculomotor inhibition may play a role in silencing the visual input while processing current stimuli and is generally related to processing time and load.

Fixation-related visual mismatch negativity.

Vision under natural conditions could be studied by combining electroencephalogram (EEG) and eye tracking as well as using saccades as triggers for the onset of the fixation-related potentials (FRPs) and for the oculomotor inhibition (OMI) that follows every saccade. The result of this analysis is thought to be equivalent to the event-related response following a peripheral preview. Previous studies that measured responses to visual deviants in a sequence of flashed stimuli found an increased negativity in the occipital N1 component (visual mismatch negativity [vMMN]), and prolonged saccadic inhibition for unexpected events. The aim of the current study was to develop an oddball paradigm in constrained natural-viewing and determine whether a similar mismatched FRP and prolonged OMI for deviance could be found. To this end, we developed a visual oddball paradigm on a static display to generate expectancy and surprise across successive saccades. Observers (n = 26) inspected, one after the other, seven small patterns of E and an inverted E arranged on the screen along a horizontal path, with one frequent (standard) and one rare (deviant), looking for a superimposed tiny dot target in each 5-second trial. Our results show a significantly larger FRP-N1 negativity for the deviant, compared with the standard and prolonged OMI of the following saccade, as previously found for transient oddballs. Our results show, for the first time, prolonged OMI and stronger fixation-related N1 to a task-irrelevant visual mismatch (vMMN) in natural, but task-guided viewing. These two signals combined could serve as markers of prediction error in free viewing.

Involuntary oculomotor inhibition markers of saliency and deviance in response to auditory sequences.

Our eyes move constantly but are often inhibited momentarily in response to external stimuli (oculomotor inhibition [OMI]), depending on the stimulus saliency, anticipation, and attention. Previous studies have shown prolonged OMI for auditory oddballs; however, they required counting the oddballs, possibly reflecting voluntary attention. Here, we investigated whether the "passive" OMI response to auditory deviants can provide a quantitative measure of deviance strength (pitch difference) and studied its dependence on the inter-trial interval (ITI). Participants fixated centrally and passively listened to repeated short sequences of pure tones that contained a deviant tone either regularly or with 20% probability (oddballs). In an "active" control experiment, participants counted the deviant or the standard. As in previous studies, the results showed prolonged microsaccade inhibition and increased pupil dilation following the rare deviant tone. Earlier inhibition onset was found in proportion to the pitch deviance (the saliency effect), and a later release was found for oddballs, but only for ITI <2.5 seconds. The active control experiment showed similar results when counting the deviant but longer OMI for the standard when counting it. Taken together, these results suggest that OMI provides involuntary markers of saliency and deviance, which can be obtained without the participant's response.

Fixation-related saccadic inhibition in free viewing in response to stimulus saliency.

Microsaccades that occur during fixation were studied extensively in response to transient stimuli, showing a typical inhibition (Oculomotor Inhibition, OMI), and a later release with a latency that depends on stimulus saliency, attention, and expectations. Here, we investigated the hypothesis that in free viewing every saccade provides a new transient stimulation that should result in a stimulus-dependent OMI like a flashed presentation during fixation. Participants (N = 16) freely inspected static displays of randomly oriented Gabor texture images, with varied contrast and spatial frequency (SF) for periods of 10 s each. Eye tracking recordings were divided into epochs triggered by saccade landing (> 1 dva), and microsaccade latency relative to fixation onset was computed (msRT). We found that the msRT in free viewing was shorter for more salient stimuli (higher contrast or lower SF), as previously found for flashed stimuli. It increased with saccade size and decreased across successive saccades, but only for higher contrast, suggesting contrast-dependent repetition enhancement in free viewing. Our results indicate that visual stimulus-dependent inhibition of microsaccades also applies to free viewing. These findings are in agreement with the similarity found between event-related and fixation-related potentials and open the way for studies combining both approaches to study natural vision.

Visual Detection and Decoding Skills of Aerial Photography by Adults with Autism Spectrum Disorder (ASD).

Despite challenges in social communication skills people with ASD often display strengths in visual processing. Aerial photography analysis is an occupation reliant on strong visual processing skills that matches this unique profile. We investigated basic-vision and "real-life" visual tasks in 20 cognitively-able young adults with ASD and 20 typically-developed (TD) "gamers". Basic-vision tests included Visual-Search, Embedded-Figures, and Vigilance; "real-life" tests included aerial-photograph detection and identification. Groups performed equally well, and did not differ significantly on any tasks. The study demonstrates strong visual skills in people with ASD in basic and "real-life" settings, and supports the idea that they may be well suited for employment in occupations that demand high visual perception skills such as aerial photography analysis.

What Makes an Image Interesting and How Can We Explain It.

Here, we explore the question: What makes a photograph interesting? Answering this question deepens our understanding of human visual cognition and knowledge gained can be leveraged to reliably and widely disseminate information. Observers viewed images belonging to different categories, which covered a wide, representative spectrum of real-world scenes, in a self-paced manner and, at trial's end, rated each image's interestingness. Our studies revealed the following: landscapes were the most interesting of all categories tested, followed by scenes with people and cityscapes, followed still by aerial scenes, with indoor scenes of homes and offices being least interesting. Judgments of relative interestingness of pairs of images, setting a fixed viewing duration, or changing viewing history - all of the above manipulations failed to alter the hierarchy of image category interestingness, indicating that interestingness is an intrinsic property of an image unaffected by external manipulation or agent. Contrary to popular belief, low-level accounts based on computational image complexity, color, or viewing time failed to explain image interestingness: more interesting images were not viewed for longer and were not more complex or colorful. On the other hand, a single higher-order variable, namely image uprightness, significantly improved models of average interest. Observers' eye movements partially predicted overall average interest: a regression model with number of fixations, mean fixation duration, and a custom measure of novel fixations explained >40% of variance. Our research revealed a clear category-based hierarchy of image interestingness, which appears to be a different dimension altogether from memorability or awe and is as yet unexplained by the dual appraisal hypothesis.

Oculomotor inhibition during smooth pursuit and its dependence on contrast sensitivity.

Our eyes are never still, but tend to "freeze" in response to stimulus onset. This effect is termed "oculomotor inhibition" (OMI); its magnitude and time course depend on the stimulus parameters, attention, and expectation. We previously showed that the time course and duration of microsaccade and spontaneous eye-blink inhibition provide an involuntary measure of low-level visual properties such as contrast sensitivity during fixation. We investigated whether this stimulus-dependent inhibition also occurs during smooth pursuit, for both the catch-up saccades and the pursuit itself. Observers followed a target with continuous back-and-forth horizontal motion while a Gabor patch was briefly flashed centrally with varied spatial frequency and contrast. Catch-up saccades of the size of microsaccades had a similar pattern of inhibition as microsaccades during fixation, with stronger inhibition onset and faster inhibition release for more salient stimuli. Moreover, a similar stimulus dependency of inhibition was shown for pursuit latencies and peak velocity. Additionally, microsaccade latencies at inhibition release, peak pursuit velocities, and latencies at minimum pursuit velocity were correlated with contrast sensitivity. We demonstrated the generality of OMI to smooth pursuit for both microsaccades and the pursuit itself and its close relation to the low-level processes that define saliency, such as contrast sensitivity.

Concealed information revealed by involuntary eye movements on the fringe of awareness in a mock terror experiment.

Involuntary eye movements during fixation are typically inhibited following stimulus onset (Oculomotor Inhibition, OMI), depending on the stimulus saliency and attention, with an earlier and longer OMI for barely visible familiar faces. However, it is still unclear whether OMI regarding familiarities and perceptual saliencies differ enough to allow a reliable OMI-based concealed information test (CIT). In a "mock terror" experiment with 25 volunteers, 13 made a concealed choice of a "terror-target" (one of eight), associated with 3 probes (face, name, and residence), which they learned watching text and videos, whereas 12 "innocents" pre-learned nothing. All participants then watched ~ 25 min of repeated brief presentations of barely visible (masked) stimuli that included the 8 potential probes, as well as a universally familiar face as a reference, while their eye movements were monitored. We found prolonged and deviant OMI regarding the probes. Incorporated with the individual pattern of responses to the reference, our analysis correctly identified 100% of the terror targets, and was 95% correct in discriminating "terrorists" from "innocents". Our results provide a "proof of concept" for a novel approach to CIT, based on involuntary oculomotor responses to barely visible stimuli, individually tailored, and with high accuracy and theoretical resistance to countermeasures.

Investigating face and house discrimination at foveal to parafoveal locations reveals category-specific characteristics.

Since perceptual and neural face sensitivity is associated with a foveal bias, and neural place sensitivity is associated with a peripheral bias (integration over space), we hypothesized that face perception ability will decline more with eccentricity than place perception ability. We also wanted to examine whether face perception ability would show a left visual field (LeVF) bias due to earlier reports suggesting right hemisphere dominance for faces, or would show an upper or lower visual field bias. Participants performed foveal and parafoveal face and house discrimination tasks for upright or inverted stimuli (≤4°) while their eye movements were monitored. Low-level visual tasks were also measured. The eccentricity-related accuracy reductions were evident for all categories. Through detailed analyses we found (i) a robust face inversion effect across the parafovea, while for houses an opposite effect was found, (ii) higher eccentricity-related sensitivity for face performance than for house performance (via inverted vs. upright within-category eccentricity-driven reductions), (iii) within-category but not across-category performance associations across eccentricities, and (iv) no hemifield biases. Our central to parafoveal investigations suggest that high-level vision processing may be reflected in behavioural performance.

Sequence Learning in Minimally Verbal Children With ASD and the Beneficial Effect of Vestibular Stimulation.

People with autism spectrum disorder (ASD) and especially the minimally verbal, often fail to learn basic perceptual and motor skills. This deficit has been demonstrated in several studies, but the findings could have been due to the nonoptimal adaptation of the paradigms. In the current study, we sought to characterize the skill learning deficit in young minimally verbal children with ASD and explore ways for improvement. For this purpose, we used vestibular stimulation (VS) whose beneficial effects have been demonstrated in the typical population, but the data regarding ASD are limited. We trained 36 children ages 6-13 years, ASD (N = 18, 15 of them minimally verbal) and typical development (TD, N = 18), on a touch version of the visual-motor Serial-Reaction-Time sequence-learning task, in 10 short (few minutes) weekly practice sessions. A subgroup of children received VS prior to each training block. All the participants but two ASD children showed gradual median reaction time improvement with significant speed gains across the training period. The ASD children were overall slower (by ~250 msec). Importantly, those who received VS (n = 10) showed speed gains comparable to TD, which were larger (by ~100%) than the ASD controls, and partially sequence-specific. VS had no effect on the TD group. These results suggest that VS has a positive effect on learning in minimally verbal ASD children, which may have important therapeutic implications. Furthermore, contrary to some previous findings, minimally verbal children with ASD can acquire, in optimal conditions, procedural skills with few short training sessions, spread over weeks, and with a similar time course as non-ASD controls. Autism Res 2020, 13: 320-337. © 2019 International Society for Autism Research, Wiley Periodicals, Inc. LAY SUMMARY: Minimally verbal children with ASD who received specially adjusted learning conditions showed significant learning of a visual-motor sequence across 10 practice days. This learning was considerably improved with vestibular stimulation before each short learning session. This may have important practical implications in the education and treatment of ASD children.

Familiarity revealed by involuntary eye movements on the fringe of awareness.

Involuntary eye movements during fixation of gaze are typically transiently inhibited following stimulus onset. This oculomotor inhibition (OMI), which includes microsaccades and spontaneous eye blinks, is modulated by stimulus saliency and anticipation, but it is currently unknown whether it is sensitive to familiarity. To investigate this, we measured the OMI while observers passively viewed a slideshow of one familiar and 7 unfamiliar facial images presented briefly at 1 Hz in random order. Since the initial experiments indicated that OMI was occasionally insensitive to familiarity when the facial images were highly visible, and to prevent top-down strategies and potential biases, we limited visibility by backward masking making the faces barely visible or at the fringe of awareness. Under these conditions, we found prolonged inhibition of both microsaccades and eye-blinks, as well as earlier onset of microsaccade inhibition with familiarity. These findings demonstrate, for the first time, the sensitivity of OMI to familiarity. Because this is based on involuntary eye movements and can be measured on the fringe of awareness and in passive viewing, our results provide direct evidence that OMI can be used as a novel physiological measure for studying hidden memories with potential implications for health, legal, and security purposes.

Comparing set summary statistics and outlier pop out in vision.

Visual scenes are too complex to perceive immediately in all their details. Two strategies (among others) have been suggested as providing shortcuts for evaluating scene gist before its details: (a) Scene summary statistics provide average values that often suffice for judging sets of objects and acting in their environment. Set summary perception spans simple/complex dimensions (circle size, face emotion), various statistics (mean, variance, range), and separate statistics for discernible sets. (b) Related to set summary perception is detecting outliers from sets, called "pop out," which allows rapid perception of presence and properties of unusual, and thus, possibly salient items in the scene. To understand better visual system mechanisms underlying these two set-related perceptual phenomena, we now study their properties and the relationship between them. We present observers with two clouds of bars with distributed orientations and ask them to discriminate their mean orientations, reporting which cloud is oriented more clockwise, on average. In the second experiment, the two clouds had the same mean orientation, but one had a bar with an outlier orientation, which observers detected. We find that cloud mean orientation discrimination depends mainly on the difference in means, whereas outlier detection depends mainly on the distance of the outlier orientation from the edge of the cloud orientation range. Neither percept depends largely on the range of the set itself. A unified model of a population-code mechanism underlying these two phenomena is discussed.

Microsaccades are sensitive to word structure: A novel approach to study language processing.

Microsaccades are miniature eye movements that occur involuntarily during fixation. They are typically inhibited following stimulus onset and are released from inhibition about 300 ms post-stimulus. Microsaccade-inhibition is modulated by low level features of visual stimuli, but it is currently unknown whether they are sensitive to higher level, abstract linguistic properties. To address this question, we measured the timing of microsaccades while subjects were presented with written Hebrew words and pronounceable nonwords (pseudowords). We manipulated the underlying structure of pseudowords such that half of them contained real roots while the other half contained invented roots. Importantly, orthographic similarity to real words was equated between the two conditions. Microsaccade onset was significantly slower following real-root compared to invented-root stimuli. Similar results were obtained when considering post-stimulus delay of eye blinks. Moreover, microsaccade-delay was positively and significantly correlated with measures of real-word similarity. These findings demonstrate, for the first time, sensitivity of microsaccades to linguistic structure. Because microsaccades are involuntary and can be measured in the absence of overt response, our results provide initial evidence that they can be used as a novel physiological measure in the study of language processes in healthy and clinical populations.

Asymmetric visual interactions across the boundary of awareness.

A salient visual object can disappear from conscious perception when surrounded by a moving texture, a phenomenon known as MIB, Motion-Induced Blindness (Bonneh, Cooperman, & Sagi, 2001). Here we tested the information available in the brain from such stimuli that do not access awareness by examining interactions across the boundary of awareness between stimuli that reach awareness and those that do not. Observers performed the MIB task in which a "Cue" was presented next to the "Target" after observers reported the perceptual disappearance of the target (Kawabe, Yamada, & Miura, 2007). Oriented Gabor patches were used as targets and cues; observers reported the target's reappearance. The results indicated an interaction between the target and the cue, depending on the orientation difference (∼30° bandwidth) and distance (∼1° range), indicating preserved properties of features in the absence of awareness. Object-based representation (binding) of unseen stimuli was tested by examining the interaction between a compound stimulus and its composing features. Here we used vertical and horizontal Gabor patches and their combinations (plaids) as targets and cues. Results indicated asymmetric relations between aware and unaware object representations; a plaid cue was not effective with a component target, but a plaid target efficiently reappeared by its component cues. This result suggests that the unseen, but not the seen plaid, is decomposed into its features. Plaid targets also reappeared with plaid cues, supporting binding without awareness. Our findings suggest preconscious representations of objects and their features, with conscious perception confined to object representations.

Contrast sensitivity revealed by spontaneous eyeblinks: Evidence for a common mechanism of oculomotor inhibition.

Spontaneous eyeblinks are known to serve important physiological functions, and recent evidence shows that they are also linked to cognitive processes. It is yet unclear whether this link reflects a crude rate modulation or, alternatively, an automatic and precise process, tightly linked to the low-level properties of sensory stimuli. We have recently reported (Y. S. Bonneh, Adini, & Polat, 2015) that, for microsaccades, the onset and release from inhibition in response to transient stimuli depend systematically on the low-level stimulus parameters. Here we reanalyzed our previous data for both microsaccades and eyeblinks for observers with sufficient blinking (>10% of trials, 18 of 23 observers tested) who watched and silently counted sequences of Gabor patches at 1 Hz with varied contrast and spatial frequency. We found that spontaneous eyeblinks, although less frequent, were similar to microsaccades in their modulation pattern in response to transient stimuli, demonstrating inhibition and rebound, which were dependent on the contrast and spatial frequency of the stimuli. The average blink response time, measured as the latency of the first blink following its release from inhibition, was longer for lower contrast and higher spatial frequency. Importantly, it was highly correlated with a similar measure for microsaccades as well as with psychophysical measures of contrast sensitivity. These results suggest that both eyeblinks and microsaccades are linked to the same inhibitory mechanism that presumably turns off oculomotor events while processing previous events and generates a rebound effect upon its release. The onset of both eyeblinks and microsaccades may thus reflect the time course of this mechanism and the associated cognitive process.

The time course and characteristics of procedural learning in schizophrenia patients and healthy individuals.

Patients with schizophrenia have deficits in some types of procedural learning. Several mechanisms contribute to this learning in healthy individuals, including statistical and sequence-learning. To find preserved and impaired learning mechanisms in schizophrenia, we studied the time course and characteristics of implicitly introduced sequence-learning (SRT task) in 15 schizophrenia patients (seven mild and eight severe) and nine healthy controls, in short sessions over multiple days (5-22). The data show speed gains of similar magnitude for all groups, but the groups differed in overall speed and in the characteristics of the learning. By analyzing the data according to its spatial-position and temporal-order components, we provide evidence for two types of learning that could differentiate the groups: while the learning of the slower, severe group was dominated by statistical learning, the control group moved from a fast learning phase of statistical-related performance to subsequence learning (chunking). Our findings oppose the naïve assumption that a similar gain of speed reflects a similar learning process; they indicate that the slower performance reflects the activation of a different motor plan than does the faster performance; and demonstrate that statistical learning and subsequence learning are two successive stages in implicit sequence learning, with chunks inferred from prior statistical computations. Our results indicate that statistical learning is intact in patients with schizophrenia, but is slower to develop in the severe patients. We suggest that this slow learning rate and the associated slow performance contribute to their deficit in developing sequence-specific learning by setting a temporal constraint on developing higher order associations.