Visual attention and inhibitory control in children, teenagers and adults with autism without intellectual disability: results of oculomotor tasks from a 2-year longitudinal follow-up study (InFoR).

BACKGROUND: Inhibitory control and attention processing atypicalities are implicated in various diseases, including autism spectrum disorders (ASD). These cognitive functions can be tested by using visually guided saccade-based paradigms in children, adolescents and adults to determine the time course of such disorders. METHODS: In this study, using Gap, Step, Overlap and Antisaccade tasks, we analyzed the oculomotor behavior of 82 children, teenagers and adults with high functioning ASD and their peer typically developing (TD) controls in a two-year follow-up study under the auspices of the InFoR-Autism project. Analysis of correlations between oculomotors task measurements and diagnostic assessment of attentional (ADHD-RS and ADHD comorbidity indices) and executive functioning (BRIEF scales) were conducted in order to evaluate their relationship with the oculomotor performance of participants with ASD. RESULTS: As indicated by the presence of a Gap and Overlap effects in all age groups, the oculomotor performances of ASD participants showed a preserved capability in overt attention switching. In contrast, the difference in performances of ASD participants in the Antisaccade task, compared to their TD peers, indicated an atypical development of inhibition and executive functions. From correlation analysis between our oculomotor data and ADHD comorbidity index, and scores of attention and executive function difficulties, our findings support the hypothesis that a specific dysfunction of inhibition skills occurs in ASD participants that is independent of the presence of ADHD comorbidity. LIMITATIONS: These include the relatively small sample size of the ASD group over the study's two-year period, the absence of an ADHD-only control group and the evaluation of a TD control group solely at the study's inception. CONCLUSIONS: Children and teenagers with ASD have greater difficulty in attention switching and inhibiting prepotent stimuli. Adults with ASD can overcome these difficulties, but, similar to teenagers and children with ASD, they make more erroneous and anticipatory saccades and display a greater trial-to-trial variability in all oculomotor tasks compared to their peers. Our results are indicative of a developmental delay in the maturation of executive and attentional functioning in ASD and of a specific impairment in inhibitory control.

Temporal preparation in adults with autistic spectrum disorder: The variable foreperiod effect.

Research suggested the possibility that temporal cognition may be different in autistic spectrum disorder (ASD). Although there are some empirical studies examining timing ability in these individuals, to our knowledge, no one directly assessed the ability to predict when an event will occur. Here, we report a study on implicit temporal preparation in individuals with ASD as indexed by the variable foreperiod (FP) effect. We compared a group of adult ASD participants to a group of typically-developed (TD) controls, for their respective abilities to utilize implicit temporal information in a simple detection task with three different preparatory intervals (FP, short, middle and long). Participants were given a warning tone to signal an imminent stimulus, and asked to press a key as quickly as they could upon detection of the stimulus. Both groups were able to use implicit temporal information, as revealed by both the variable-FP effect (i.e., faster response for targets appearing after a long FP) and asymmetric sequential effects (i.e., slower response in short-FP trials following a previous long-FP trial). The TD group exhibited a faster response in a long-FP trial that was preceded by short-FP one, whereas the ASD group did not, as reflected in their higher percentage of response omissions for a target that appeared later than in the previous trial. The reduced ability of ASD participants to modulate their responses under these conditions might reflect a difficulty in time-based monitoring of stimulus occurrence. LAY SUMMARY: Time-processing may be different in autistic spectrum disorder (ASD). This study addressed the ability to anticipate a relevant stimulus's onset according to predictable interstimulus intervals comparing adults with ASD and typically developed controls. We found that ASD participants did not benefit from temporal preparation when stimulus appeared later than previously attended. This suggests a reduced ability in detecting implicit temporal regularities between events.

Emotional face recognition in autism and in cerebral visual impairments: In search for specificity.

Autism spectrum disorder (ASD) is characterized by difficulties in the social domain, but also by hyper- and hypo-reactivity. Atypical visual behaviours and processing have often been observed. Nevertheless, several similar signs are also identified in other clinical conditions including cerebral visual impairments (CVI). In the present study, we investigated emotional face categorization in groups of children with ASD and CVI by comparing each group to typically developing individuals (TD) in two tasks. Stimuli were either non-filtered or filtered by low- and high-spatial frequencies (LSF and HSF). All participants completed the autism spectrum quotient score (AQ) and a complete neurovisual evaluation. The results show that while both clinical groups presented difficulties in the emotional face recognition tasks and atypical processing of filtered stimuli, they did not differ from one another. Additionally, autistic traits were observed in the CVI group and symmetrically, some visual disturbances were present in the ASD group as measured via the AQ score and a neurovisual evaluation, respectively. The present study suggests the relevance of comparing ASD to CVI by showing that emotional face categorization difficulties should not be solely considered as autism-specific but merit investigation for potential dysfunction of the visual processing neural network. These results are of interest in both clinical and research perspectives, indicating that systematic visual examination is warranted for individuals with ASD.

Trustworthiness and Dominance Personality Traits' Judgments in Adults with Autism Spectrum Disorder.

Autism Spectrum Disorder (ASD) is characterized by impairments in social functioning, communication, and by the presence of repetitive behaviours and restricted interests. Abnormal processing of faces has also been described as a neuropsychological feature of ASD. We investigated the ability to judge two personality traits in adults with ASD in comparison to typically developed adults (TD). We used an eye tracking device to investigate the exploration of faces when participants judged the degree of trustworthiness and dominance of synthetic faces. In sum, we found that adults with ASD were as capable as TD adults to judge personality traits of face trustworthiness and dominance, which relied on similar exploration of the synthetic faces in the two populations.

Phenomenal, bodily and brain correlates of fictional reappraisal as an implicit emotion regulation strategy.

The ability to modulate our emotional experience, depending on our current goal and context, is of critical importance for adaptive behavior. This ability encompasses various emotion regulation strategies, such as fictional reappraisal, at stake whenever one engages in fictional works (e.g., movies, books, video games, virtual environments). Neuroscientific studies investigating the distinction between the processing of real and fictional entities have reported the involvement of brain structures related to self-relevance and emotion regulation, suggesting a threefold interaction between the appraisal of reality, aspects of the Self, and emotions. The main aim of this study is to investigate the effect of implicit fictional reappraisal on different components of emotion, as well as on the modulatory role of autobiographical and conceptual self-relevance. While recording electrodermal, cardiac, and brain activity (EEG), we presented negative and neutral pictures to 33 participants, describing them as either real or fictional. After each stimulus, the participants reported their subjective emotional experience, self-relevance of the stimuli, as well as their agreement with their description. Using the Bayesian mixed-modeling framework, we showed that stimuli presented as fictional, compared with real, were subjectively appraised as less intense and less negative, and elicited lower skin conductance response, stronger heart-rate deceleration, and lower late positive potential amplitudes. Finally, these phenomenal and physiological changes did, to a moderate extent, rely on variations of specific aspects of self-relevance. Implications for the neuroscientific study of implicit emotion regulation are discussed.

Prior Knowledge, Episodic Control and Theory of Mind in Autism: Toward an Integrative Account of Social Cognition.

Over the last 30 years, research has explored theory of mind (ToM), the ability to attribute mental states to oneself and to others. Work on ToM in typical and atypical populations has shed light on the neurocognitive mechanisms underlying social understanding and interaction. The ToM hypothesis has long been regarded as one comprehensive explanation of the severe cognitive and behavioral impairments encountered by individuals with autism. However, high-functioning individuals can often pass both first-order and second-order false belief tasks using cognitive compensation strategies. To provide more sensitive measures of mental state attribution abilities, researchers have introduced more difficult, "advanced" theory of mind tasks. In this article, we argue that in attempting to bypass compensation strategies, these new advanced ToM tasks, such as the Faux Pas and the Strange Stories tasks, impose cognitive demands beyond those specific to the domain of ToM. We then provide an integrative account of social deficits in autism that takes into account several distinct components of mental state understanding, including both general cognitive capacities and processes specific to ToM. We argue that a number of related cognitive abilities, including episodic cognitive control and inferencing from prior knowledge, are necessary to understand how both people with autism and typical development navigate challenging, real-life social situations.

Saccadic eye movements in adults with high-functioning autism spectrum disorder.

In this study, we examined the accuracy and dynamics of visually guided saccades in 20 adults with autism spectrum disorder, as compared to 20 typically developed adults using the Step/Overlap/Gap paradigms. Performances in participants with autistic spectrum disorder were characterized by preserved Gap/Overlap effect, but reduced gain and peak velocity, as well as a greater trial-to-trial variability in task performance, as compared to the control group. While visual orienting and attentional engagement were relatively preserved in individuals with autistic spectrum disorder, overall these findings provide evidence that abnormal oculomotor behavior in autistic spectrum disorder reflects an altered sensorimotor control due to cerebellar abnormalities, rather than a deficit in the volitional control of eye movements. This study contributes to a growing body of evidence implicating this structure in the physiopathology of autism.

The influence of prior reputation and reciprocity on dynamic trust-building in adults with and without autism spectrum disorder.

The present study was designed to investigate the effects of reputational priors and direct reciprocity on the dynamics of trust building in adults with (N = 17) and without (N = 25) autism spectrum disorder (ASD) using a multi-round Trust Game (MTG). On each round, participants, who played as investors, were required to maximize their benefits by updating their prior expectations (the partner's positive or negative reputation), based on the partner's directed reciprocity, and adjusting their own investment decisions accordingly. Results showed that reputational priors strongly oriented the initial decision to trust, operationalized as the amount of investment the investor shares with the counterpart. However, while typically developed participants were mainly affected by the direct reciprocity, and rapidly adopted the optimal Tit-for-Tat strategy, participants with ASD continued to rely on reputational priors throughout the game, even when experience of the counterpart's actual behavior contradicted their prior-based expectations. In participants with ASD, the effect of the reputational prior never disappeared, and affected judgments of trustworthiness and reciprocity of the partner even after completion of the game. Moreover, the weight of prior reputation positively correlated with the severity of the ASD participant's social impairments while the reciprocity score negatively correlated with the severity of repetitive and stereotyped behaviors, as measured by the Autism Diagnostic Interview-Revised (ADI-R). In line with Bayesian theoretical accounts, the present findings indicate that individuals with ASD have difficulties encoding incoming social information and using it to revise and flexibly update prior social expectations, and that this deficit might severely hinder social learning and everyday life interactions.

Cerebellar anatomical alterations and attention to eyes in autism.

The cerebellum is implicated in social cognition and is likely to be involved in the pathophysiology of autism spectrum disorder (ASD). The goal of our study was to explore cerebellar morphology in adults with ASD and its relationship to eye contact, as measured by fixation time allocated on the eye region using an eye-tracking device. Two-hundred ninety-four subjects with ASD and controls were included in our study and underwent a structural magnetic resonance imaging scan. Global segmentation and cortical parcellation of the cerebellum were performed. A sub-sample of 59 subjects underwent an eye tracking protocol in order to measure the fixation time allocated to the eye region. We did not observe any difference in global cerebellar volumes between ASD patients and controls; however, regional analyses found a decrease of the volume of the right anterior cerebellum in subjects with ASD compared to controls. There were significant correlations between fixation time on eyes and the volumes of the vermis and Crus I. Our results suggest that cerebellar morphology may be related to eye avoidance and reduced social attention. Eye tracking may be a promising neuro-anatomically based stratifying biomarker of ASD.

Reduced sensitivity to social priors during action prediction in adults with autism spectrum disorders.

An extensive amount of evidence has documented a diminished ability to predict and understand other people's action in individuals with autism spectrum disorders (ASD). Recently, two theoretical accounts, the "Hypo-priors" and the "Aberrant precision" hypotheses, have suggested that attenuated Bayesian priors or an imbalance of the precision ascribed to sensory evidence relative to prior expectations may be responsible for the atypical perceptual experience and difficulties with action understanding in ASD. In the present study, we aimed to directly investigate whether difficulties in the appreciation of others' intentions can be accounted for by abnormal interaction between these two types of information: (i) the sensory evidence conveyed by movement kinematics, and (ii) the observer's expectations, acquired from past experience or derived from prior knowledge. To test this hypothesis, we contrasted the ability to infer Non-Social and Social intentions in adults with and without ASD, using a series of tasks in which both sensory evidence and prior expectations were manipulated. The results showed that attenuated effect of prior expectations in ASD individuals does not result from a generalized impairment in mentalizing, but one confined to social intentions. Attenuated priors in the social domain predicted the severity of clinical symptoms in the area of social interaction. Importantly, however, we found that reduced priors in the social domain could be compensated by ASD through observational learning, i.e. through deriving statistical regularities from observed behaviours. This capacity to balance reduced social expectations by learning inversely correlated with the severity of repetitive and stereotyped behaviours. Collectively, these findings suggest that adults with ASD exhibit a disturbance in the inferential mechanism that integrates sensory evidence into prior beliefs to produce accurate inferences about other people's intentions.

The distinctive role of executive functions in implicit emotion regulation.

Several theoretical models stress the role of executive functions in emotion regulation (ER). However, most of the previous studies on ER employed explicit regulatory strategies that could have engaged executive functions, beyond regulatory processes per se. Recently, there has been renewed interest in implicit forms of ER, believed to be closer to daily-life requirements. While various studies have shown that implicit and explicit ER engage partially overlapping neurocognitive processes, the contribution of different executive functions in implicit ER has not been investigated. In the present study, we presented participants with negatively valenced pictures of varying emotional intensity preceded by short texts describing them as either fictional or real. This manipulation was meant to induce a spontaneous emotional down-regulation. We recorded electrodermal activity (EDA) and subjective reports of emotion arousal. Executive functions (updating, switching, and inhibition) were also assessed. No difference was found between the fictional and real condition on EDA. A diminished self-reported arousal was observed, however, when pictures were described as fictional for high- and mild-intensity material, but not for neutral material. The amount of down-regulation in the fictional condition was found to be predicted by interindividual variability in updating performances, but not by the other measures of executive functions, suggesting its implication even in implicit forms of ER. The relationship between down-regulation and updating was significant only for high-intensity material. We discuss the role of updating in relation to the consciousness of one's emotional state.

Gaze direction detection in autism spectrum disorder.

Detecting where our partners direct their gaze is an important aspect of social interaction. An atypical gaze processing has been reported in autism. However, it remains controversial whether children and adults with autism spectrum disorder interpret indirect gaze direction with typical accuracy. This study investigated whether the detection of gaze direction toward an object is less accurate in autism spectrum disorder. Individuals with autism spectrum disorder (n = 33) and intelligence quotients-matched and age-matched controls (n = 38) were asked to watch a series of synthetic faces looking at objects, and decide which of two objects was looked at. The angle formed by the two possible targets and the face varied following an adaptive procedure, in order to determine individual thresholds. We found that gaze direction detection was less accurate in autism spectrum disorder than in control participants. Our results suggest that the precision of gaze following may be one of the altered processes underlying social interaction difficulties in autism spectrum disorder.

Reduced saccadic inhibition of return to moving eyes in autism spectrum disorders.

Inhibition of Return (IOR) refers to slower reaction time to a target presented at the same location as a preceding stimulus. Here, we examine reflexive attention orienting via the saccadic IOR using a shift in gaze direction (i.e. from averted to direct) in faces presented as a peripheral cue, in upright and inverted orientations, in adults with Autism Spectrum Disorder (ASD) and typically developed comparison participants. While both groups showed an IOR in the inverted face condition, this effect was reduced in participants with ASD in the upright face condition, as compared to comparison participants, suggesting that moving eyes do not trigger reflexive exogenous orienting in individuals with ASD. Impaired reflexive orienting to eye gaze might severely compromise the later development of social functions in ASD, such as joint attention, face emotion recognition and mindreading.

The paradox of fiction: Emotional response toward fiction and the modulatory role of self-relevance.

For over forty years, philosophers have struggled with the "paradox of fiction", which is the issue of how we can get emotionally involved with fictional characters and events. The few neuroscientific studies investigating the distinction between the processing of real and fictional entities have evidenced that midline cortical structures and lateral fronto-parietal regions are more engaged for real and fictional entities, respectively. Interestingly, the former network is engaged in autobiographical memory retrieval and self-reference, processes that are known to boost emotional reactivity, while the latter underpins emotion regulation. Thus, a possible modulation of the emotional response according to the nature (real or fictional) of the stimulus is conceivable. To test this hypothesis, we presented short emotional (negative and positive) and neutral video as fictional or real. For negative material, we found that subjective emotional experience, but not physiological arousal measured by electrodermal activity, was reduced in the fictional condition. Moreover, the amount of personal memories linked to the scenes counteracted this effect boosting the subjective emotional response. On the contrary, personal memories elicited by the scenes, but not fiction, modulate the emotional response for positive material. These results suggest that when a stimulus triggers a personal memory, the emotional response is less prone to be modulated by contextual factors, and suggest that personal engagement could be responsible for emotional reaction toward fiction. We discuss these results in the emotion regulation framework and underline their implications in informing theoretical accounts of emotion in the neuroscientific domain and the philosophical debate on the paradox of emotional response to fiction.

Atypical Social Judgment and Sensitivity to Perceptual Cues in Autism Spectrum Disorders.

Evaluation of faces is an important dimension of social relationships. A degraded sensitivity to facial perceptual cues might contribute to atypical social interactions in autism spectrum disorder (ASD). The current study investigated whether face based social judgment is atypical in ASD and if so, whether it could be related to a degraded sensitivity to facial perceptual cues. Individuals with ASD (n = 33) and IQ- and age-matched controls (n = 38) were enrolled in this study. Watching a series of photographic or synthetic faces, they had to judge them for "kindness". In synthetic stimuli, the amount of perceptual cues available could be either large or small. We observed that social judgment was atypical in the ASD group on photographic stimuli, but, contrarily to the prediction based on the degraded sensitivity hypothesis, analyses on synthetic stimuli found a similar performance and a similar effect of the amount of perceptual cues in both groups. Further studies on perceptual differences between photographs and synthetic pictures of faces might help understand atypical social judgment in ASD.

The sense of agency in autism spectrum disorders: a dissociation between prospective and retrospective mechanisms?

While a large number of studies have reported impairments in social and interpersonal abilities in individuals with autism spectrum disorder (ASD), relatively few studies have focused on self-related knowledge in this population. One of the processes implicated in the physical dimension of the Self is the sense of agency (SoA), i.e., the experience of initiating and controlling one's own actions and producing desired changes in the world via these actions. So far, the few studies investigating SoA in ASD have reported contrasting results, with some showing spared, others impaired SoA. Here, we review the existing literature and suggest that the distinction between prospective and retrospective mechanisms of the SoA might help reconcile the existing findings. In the light of a multi-componential model of SoA, we propose the view that a specific impairment at the level of prospective mechanisms acting on internal agency signals (i.e., the intention, action selection, or command produced to achieve the goal) may be responsible for the reduced SoA in ASD, along with spared retrospective mechanisms. Future research should shed light on the impact of abnormal SoA on social and self-related dysfunctions in ASD.

Accelerated time course of saccadic inhibition of return in individuals with autism spectrum disorders.

The inhibition of return (IOR) refers the observer's slower response time when the target stimulus appears on the previously attended location. In the present study, we examined the time course of saccadic IOR by using five stimuli onset asynchronies (SOAs) in a group of adults with autism spectrum disorders (ASDs) and a comparison group. The results showed that the IOR effect occurred earlier (300 ms SOA) in participants with ASDs, relative to the comparison participants (500 and 700 ms SOAs). The ASD group also committed a greater number of anticipatory saccades, which positively correlated with scores on restricted and repetitive behaviors, as assessed by the Autism Diagnostic Interview-Revised (ADI-R; Lord et al. in J Autism Dev Disord 24:659-685, 1994). These findings reveal an accelerated time course for saccadic IOR along with diminished volitional oculomotor control in participants with ASDs. We discussed these results with reference to the atypical and the superior visual search abilities often reported in this population.