Brief Report: Differences in Naturalistic Attention to Real-World Scenes in Adolescents with 16p.11.2 Deletion.

Sensory differences are nearly universal in autism, but their genetic origins are poorly understood. Here, we tested how individuals with an autism-linked genotype, 16p.11.2 deletion ("16p"), attend to visual information in immersive, real-world photospheres. We monitored participants' (N = 44) gaze while they actively explored 360° scenes via headmounted virtual reality. We modeled the visually salient and semantically meaningful information in scenes and quantified the relative bottom-up vs. top-down influences on attentional deployment. We found, when compared to typically developed control (TD) participants, 16p participants' attention was less dominantly predicted by semantically meaningful scene regions, relative to visually salient regions. These results suggest that a reduction in top-down relative to bottom-up attention characterizes how individuals with 16p.11.2 deletions engage with naturalistic visual environments.

Reduced social attention in autism is magnified by perceptual load in naturalistic environments.

Individuals with autism spectrum conditions (ASC) describe differences in both social cognition and sensory processing, but little is known about the causal relationship between these disparate functional domains. In the present study, we sought to understand how a core characteristic of autism-reduced social attention-is impacted by the complex multisensory signals present in real-world environments. We tested the hypothesis that reductions in social attention associated with autism would be magnified by increasing perceptual load (e.g., motion, multisensory cues). Adult participants (N = 40; 19 ASC) explored a diverse set of 360° real-world scenes in a naturalistic, active viewing paradigm (immersive virtual reality + eyetracking). Across three conditions, we systematically varied perceptual load while holding the social and semantic information present in each scene constant. We demonstrate that reduced social attention is not a static signature of the autistic phenotype. Rather, group differences in social attention emerged with increasing perceptual load in naturalistic environments, and the susceptibility of social attention to perceptual load predicted continuous measures of autistic traits across groups. Crucially, this pattern was specific to the social domain: we did not observe differential impacts of perceptual load on attention directed toward nonsocial semantic (i.e., object, place) information or low-level fixation behavior (i.e., overall fixation frequency or duration). This study provides a direct link between social and sensory processing in autism. Moreover, reduced social attention may be an inaccurate characterization of autism. Instead, our results suggest that social attention in autism is better explained by "social vulnerability," particularly to the perceptual load of real-world environments.

Reduced Sensory Habituation in Autism and Its Correlation with Behavioral Measures.

Autism is strongly associated with sensory processing difficulties. We investigate sensory habituation, given its relevance for understanding important phenotypic traits like hyper- and hypo-sensitivities. We collected electroencephalography data from 22 neuro-typical(NT) and 13 autistic(ASD) children during the presentation of visual and auditory sequences of repeated stimuli. Our data show that the ASD children have significantly reduced habituation relative to the NT children for both auditory and visual stimuli. These results point to impaired habituation as a modality-general phenomenon in ASD. Additionally, the rates of habituation are correlated with several clinical scores associated with competence along diverse phenotypic dimensions. These data suggest that the sensory difficulties in autism are likely to be associated with reduced habituation and are related to clinical symptomology.

Active vision in immersive, 360° real-world environments.

How do we construct a sense of place in a real-world environment? Real-world environments are actively explored via saccades, head turns, and body movements. Yet, little is known about how humans process real-world scene information during active viewing conditions. Here, we exploited recent developments in virtual reality (VR) and in-headset eye-tracking to test the impact of active vs. passive viewing conditions on gaze behavior while participants explored novel, real-world, 360° scenes. In one condition, participants actively explored 360° photospheres from a first-person perspective via self-directed motion (saccades and head turns). In another condition, photospheres were passively displayed to participants while they were head-restricted. We found that, relative to passive viewers, active viewers displayed increased attention to semantically meaningful scene regions, suggesting more exploratory, information-seeking gaze behavior. We also observed signatures of exploratory behavior in eye movements, such as quicker, more entropic fixations during active as compared with passive viewing conditions. These results show that active viewing influences every aspect of gaze behavior, from the way we move our eyes to what we choose to attend to. Moreover, these results offer key benchmark measurements of gaze behavior in 360°, naturalistic environments.

Reduced Language Lateralization in Autism and the Broader Autism Phenotype as Assessed with Robust Individual-Subjects Analyses.

One of the few replicated functional brain differences between individuals with autism spectrum disorders (ASD) and neurotypical (NT) controls is reduced language lateralization. However, most prior reports relied on comparisons of group-level activation maps or functional markers that had not been validated at the individual-subject level, and/or used tasks that do not isolate language processing from other cognitive processes, complicating interpretation. Furthermore, few prior studies have examined functional responses in other brain networks, as needed to determine the spatial selectivity of the effect. Using functional magnetic resonance imaging (fMRI), we compared language lateralization between 28 adult ASD participants and carefully pairwise-matched controls, with the language regions defined individually using a well-validated language "localizer" task. Across two language comprehension paradigms, ASD participants showed less lateralized responses due to stronger right hemisphere activity. Furthermore, this effect did not stem from a ubiquitous reduction in lateralization of function across the brain: ASD participants did not differ from controls in the lateralization of two other large-scale networks-the Theory of Mind network and the Multiple Demand network. Finally, in an exploratory study, we tested whether reduced language lateralization may also be present in NT individuals with high autism-like traits. Indeed, autistic trait load in a large set of NT participants (n = 189) was associated with less lateralized language responses. These results suggest that reduced language lateralization is robustly associated with autism and, to some extent, with autism-like traits in the general population, and this lateralization reduction appears to be restricted to the language system. LAY SUMMARY: How do brains of individuals with autism spectrum disorders (ASD) differ from those of neurotypical (NT) controls? One of the most consistently reported differences is the reduction of lateralization during language processing in individuals with ASD. However, most prior studies have used methods that made this finding difficult to interpret, and perhaps even artifactual. Using robust individual-level markers of lateralization, we found that indeed, ASD individuals show reduced lateralization for language due to stronger right-hemisphere activity. We further show that this reduction is not due to a general reduction of lateralization of function across the brain. Finally, we show that greater autistic trait load is associated with less lateralized language responses in the NT population. These results suggest that reduced language lateralization is robustly associated with autism and, to some extent, with autism-like traits in the general population. Autism Res 2020, 13: 1746-1761. © 2020 International Society for Autism Research and Wiley Periodicals LLC.

Slower Binocular Rivalry in the Autistic Brain.

Autism has traditionally been regarded as a disorder of the social brain. Recent reports of differences in visual perception have challenged this notion, but little evidence for altered visual processing in the autistic brain exists. We have previously observed slower behaviorally reported rates of a basic visual phenomenon, binocular rivalry, in autism [1, 2]. During rivalry, two images-one presented to each eye-vie for awareness, alternating back and forth in perception. This competition is modeled to rely, in part, on the balance of excitation and inhibition in visual cortex [3-8], which may be altered in autism [2, 9-14]. Yet direct neural evidence for this potential marker of excitation/inhibition (E/I) balance in autism is lacking. Here, we report a striking alteration in the neural dynamics of binocular rivalry in individuals with autism. Participants viewed true and simulated frequency-tagged binocular rivalry displays while steady-state visually evoked potentials (SSVEPs) were measured over occipital cortex using electroencephalography (EEG). First, we replicate our prior behavioral findings of slower rivalry and reduced perceptual suppression in individuals with autism compared with controls. Second, we provide direct neural evidence for slower rivalry in autism compared with controls, which strongly predicted individuals' behavioral switch rates. Finally, using neural data alone, we were able to predict autism symptom severity (ADOS) and correctly classify individuals' diagnostic status (autistic versus control; 87% accuracy). These findings clearly implicate atypical visual processing in the neurobiology of autism. Down the road, this paradigm may serve as a non-verbal marker of autism for developmental and cross-species research.

Cortical responses to dynamic emotional facial expressions generalize across stimuli, and are sensitive to task-relevance, in adults with and without Autism.

Individuals with Autism Spectrum Disorders (ASD) report difficulties extracting meaningful information from dynamic and complex social cues, like facial expressions. The nature and mechanisms of these difficulties remain unclear. Here we tested whether that difficulty can be traced to the pattern of activity in "social brain" regions, when viewing dynamic facial expressions. In two studies, adult participants (male and female) watched brief videos of a range of positive and negative facial expressions, while undergoing functional magnetic resonance imaging (Study 1: ASD n = 16, control n = 21; Study 2: ASD n = 22, control n = 30). Patterns of hemodynamic activity differentiated among facial emotional expressions in left and right superior temporal sulcus, fusiform gyrus, and parts of medial prefrontal cortex. In both control participants and high-functioning individuals with ASD, we observed (i) similar responses to emotional valence that generalized across facial expressions and animated social events; (ii) similar flexibility of responses to emotional valence, when manipulating the task-relevance of perceived emotions; and (iii) similar responses to a range of emotions within valence. Altogether, the data indicate that there was little or no group difference in cortical responses to isolated dynamic emotional facial expressions, as measured with fMRI. Difficulties with real-world social communication and social interaction in ASD may instead reflect differences in initiating and maintaining contingent interactions, or in integrating social information over time or context.