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Neural and behavioral underpinnings of contextual modulations in Autism

Periodic Reporting for period 1 - NBUCA (Neural and behavioral underpinnings of contextual modulations in Autism)

Reporting period: 2015-09-01 to 2017-08-31

Originally discovered in the monkey's ventral premotor area, mirror neurons constitute a particular type of cell that discharges both during execution and observation of the same or similar action. Since their discovery, numerous studies in humans have shown that when observing someone performing an action, our motor system covertly replicates (i.e. simulates) the observed action with high temporal and muscular fidelity, pointing to the existence of a similar mirror system in human primates. This system is thought to play a key role in action comprehension and anticipation, allowing individuals to effectively engage in social interactions on a daily basis.
Social communicative impairments, including deficits in predicting and comprehending other people’s actions, are considered to be among the core deficits associated with Autism Spectrum Disorders (ASDs). It has been suggested that these impairments could be explained in terms of a dysfunction in this “mirror system” (i.e. the broken mirror hypothesis of ASD). While this theory has received considerable attention during the last decade, recent research provides contradictory evidence, with studies reporting either preserved or abnormal activity within this system, and overall suggesting that a dysfunction in this system by itself is unable to give a complete account of ASD symptomatology.
Furthermore, so far, ASD social communicative deficits have been traditionally studied by using non-realistic stimuli embedded in abstract tasks (e.g. observation of hands detached from background) or through standard office-based neuropsychological tests. These tasks are not good models of the world because they lack the contextual cues that are present in everyday-life situations in which ASD individuals are mostly impaired. Thus, a critical aspect that has so far been neglected concerns the context-embedded nature of other’s actions perception. In other words, body movements are not perceived in isolation, but with objects, actors, and the relationships amongst them ‘gluing together’ into a unifying scene. Although contextual processing during action comprehension has been successfully studied in other disorders (e.g. schizophrenia), much less is known about the role that it plays in ASD. Thus, a new research agenda which considers the influence that context, as an intrinsic part of social cognition has on ASD social deficits is timely and clearly needed.
To date, no therapeutic interventions have proven to be widely effective in treating the social symptoms of ASD. These symptoms cause lifelong disabilities for affected individuals and significant burdens on their families, schools, and society. Therefore, a better understanding of ASD is necessary for identifying potential new treatments grounded in experimental evidence.
The general aim of NBUCA is to study the neural and behavioral underpinnings of contextual modulations in ASD during action prediction and comprehension and answer many challenging questions: a) Do children with ASD have a general deficit in integrating context and behavior? b) Does this deficit rely more on the processing of social or non-social contextual information (or both)? c) Are deficits involved in action prediction playing a key role in this disorder? Given these research questions, NBUCA action aims at developing a battery of realistic tasks representing everyday-life situations to be used in different experiments combining brain, behavioral and psychological measures.
NBUCA action comprised the initial development of a set of context-sensitive ecological paradigms to be combined with neural and behavioural measures. Overall, two different paradigms were designed. The first paradigm aimed at preliminary investigating how context was affecting motor resonance responses in neurotypical individuals during action prediction. More specifically, we explored contextual modulations in motor resonance responses related to i) the type of information provided by the context (in terms of ambiguous, congruent or incongruent); and ii) the timing of these contextual effects (in terms of early and late effects). We found that the observation of actions occurring in congruent contexts (i.e. reaching-to-grasp a mug full of coffee with a precision grip) early facilitated motor resonance responses, while the observation of actions in incongruent contexts (i.e. reaching-to-grasp a mug empty with a precision grip) resulted in their later inhibition. When investigating these effects in young adults higher in autistic traits, we found that while the facilitatory effect for congruent actions remained intact, the inhibitory effect diminished as a function of the amount of autistic traits. In other words, adults higher in autistic traits showed difficulties in effectively inhibiting motor activity when the context was requiring it.
The second paradigm was designed to investigate the impact of contextual cues during action prediction in children and young adults with Autism Spectrum Disorders (ASD) and typically developing controls (TD). The paradigm consisted of a familiarization (Implicit Probabilistic Learning Task) and a testing phase (Action Prediction Task). During the familiarization phase, children observed videos depicting a child actor grasping common objects to perform different actions and we asked them to recognize actor’s intention. Importantly, we implicitly biased action-contextual cues associations in terms of their probability of co-occurrence (i.e. given the presence of an orange plate, it was highly probable that the child would grasp an apple for eating). During the testing phase, children observed the same videos but, in this case, the second half remained occluded from view and they were asked to predict action unfolding. During this phase, all possible action-contextual cues associations were equally presented. We reasoned that during this phase, where actions were partially occluded, children’s responses would be biased to contextual priors acquired during the familiarization phase, thus compensating perceptual uncertainty. No differences were observed between groups in recognizing actor’s intention during the familiarization, suggesting that ASD children are able to recognize other people’s actions to the same extent as TD children. However, during the testing phase, children with ASD exhibited a deficit in extracting regularities from the context and in using this information to form predictions. In other words, children with ASD did not benefit from context-based learning experiences when predicting other people’s actions.
Collectively, NBUCA results suggests that contextual information modulates motor resonance responses, an aspect that was classically viewed as automatic. Furthermore, they suggest that children with ASD are not able to combine motor-related information with the broader context in which the observed action is embedded.
Overall, NBUCA results provide new evidence about the role that context plays in ASD and inform current theories on this disorder. This knowledge provides new insights on the cognitive and neural bases of ASD socio-motor symptoms and impacts on the development of innovative evidence-based therapeutic interventions. For instance, NBUCA findings are now being used to develop virtual reality environments to increase awareness on contextual information in patients with social perception disorders.
Explanatory representation of the experimental task used in NBUCA