Autistic traits predict poor integration between top-down contextual expectations and movement kinematics during action observation

L Amoruso,C Urgesi,A Finisguerra

doi:10.1038/s41598-018-33827-8

L Amoruso, C Urgesi + Show 1 more

Open Access

https://doi.org/10.1038/s41598-018-33827-8

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Abstract

Autism is associated with difficulties in predicting and understanding other people’s actions. There is evidence that autistic traits are distributed across a spectrum and that subclinical forms of autistic impairments can also be measured in the typical population. To investigate the association between autistic traits and motor responses to others’ actions, we quantified these traits and measured cortico-spinal excitability modulations in M1 during the observation of actions embedded in congruent, incongruent and ambiguous contexts. In keeping with previous studies, we found that actions observed in congruent contexts elicited an early facilitation of M1 responses, and actions observed in incongruent contexts, resulted in a later inhibition. Correlational analysis revealed no association between autistic traits and the facilitation for congruent contexts. However, we found a significant correlation between motor inhibition and autistic traits, specifically related to social skills and attention to details. Importantly, the influence of these factors was independent from each other, and from the observer’s gender. Thus, results suggest that individuals with higher social deficits and greater detail-processing style are more impaired in suppressing action simulation in M1 when a mismatch between kinematics and context occurs. This points to difficult integration between kinematics and contextual representations in the autistic-like brain.

Highlights

Comprehending the intentions underlying other people’s actions from observing their movements constitutes a crucial ability in humans’ everyday-life
The dependent-sample t-test performed on the log-transformed amplitudes of motor-evoked potentials (MEPs) recorded from the First Dorsal Interosseous (FDI) and the ECR baseline blocks revealed no main effect of muscle (t21 = 1.68, p = 0.10), suggesting that MEPs recorded from both muscles were comparable
The inhibitory index in the later time-window (500 ms) positively correlated with the Autism Spectrum Quotient (AQ) total score (r = 0.679; p = 0.001), showing that the higher the level of autistic traits the higher the level of motor responses for actions observed in incongruent contexts as compared to ambiguous ones

Summary

Introduction

Comprehending the intentions underlying other people’s actions from observing their movements constitutes a crucial ability in humans’ everyday-life. Socio-motor impairments, including difficulties in action prediction and comprehension, are considered to be among the core deficits associated with Autism Spectrum Disorders (ASD)[6] It has been argued[7] that these impairments could be explained in terms of a global dysfunction in the MNS (i.e., the broken mirror theory of ASD). Evidence of mirror-like activity in humans comes from single-pulse transcranial magnetic stimulation (spTMS) studies measuring motor facilitation over the primary motor cortex (M1) during action observation. To get an insight into the possible reasons for this discrepancy, it is important to note that socio-motor deficits in ASD have been traditionally studied by using non-realistic stimuli (i.e., meaningless movements, snapshots of hands detached from background) These stimuli are not good replicas of the world because they lack the context of everyday-life situations[17]. This integrative aspect, which is inherent to the processing of naturalistic scenes, seems to be missing in most previous studies measuring action comprehension in ASD

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