Abstract

Naturalistic movie paradigms are exquisitely dynamic by nature, yet dedicated analytical methods typically remain static. Here, we deployed a dynamic inter-subject functional correlation (ISFC) analysis to study movie-driven functional brain changes in a population of male young adults diagnosed with autism spectrum disorder (ASD). We took inspiration from the resting-state research field in generating a set of whole-brain ISFC states expressed by the analysed ASD and typically developing (TD) subjects along time.Change points of state expression often involved transitions between different scenes of the movie, resulting in the reorganisation of whole-brain ISFC patterns to recruit different functional networks. Both subject populations showed idiosyncratic state expression at dedicated time points, but only TD subjects were also characterised by episodes of homogeneous recruitment. The temporal fluctuations in both quantities, as well as in cross-population dissimilarity, were tied to contextual movie cues.The prominent idiosyncrasy seen in ASD subjects was linked to individual symptomatology by partial least squares analysis, as different temporal sequences of ISFC states were expressed by subjects suffering from social and verbal communication impairments, as opposed to nonverbal communication deficits and stereotypic behaviours. Furthermore, the temporal expression of several of these states was correlated with the movie context, the presence of faces on screen, or overall luminosity.Overall, our results support the use of dynamic analytical frameworks to fully exploit the information obtained by naturalistic stimulation paradigms. They also show that autism should be understood as a multi-faceted disorder, in which the functional brain alterations seen in a given subject will vary as a function of the extent and balance of expressed symptoms.

Highlights

  • Naturalistic paradigms, in which the scanned volunteer is exposed to an ecological experimental design, have been gaining interest in functional magnetic resonance imaging studies over the recent years

  • inter-subject functional correlation (ISFC) estimates of the combined typically developing (TD) and autism spectrum disorder (ASD) populations were aggregated, and subjected to k-means clustering for the generation of ISFC states

  • ISFC state expression differs as a function of individual ASD symptomatology

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Summary

Introduction

Naturalistic paradigms, in which the scanned volunteer is exposed to an ecological experimental design, have been gaining interest in functional magnetic resonance imaging (fMRI) studies over the recent years. Compared to traditional task-based recordings that alternate between task and rest epochs, they enable to probe brain function in more realistic settings, which has provided insights into our understanding of previously scarcely explored facets of cognition: this includes, for example, music perception with auditory stimuli (Toiviainen et al, 2014; Burunat et al, 2016); theory of mind and the understanding of emotional responses upon audiovisual stimulation (Hasson et al, 2004; Wolf et al., 2010; Lahnakoski et al, 2012; Karim and Perlman, 2017); or reward processing in cognitive control when playing a video game (Huskey et al, 2018). Data-driven approaches extracting information without the need for prior knowledge have been applied in the form of independent component analysis variants (Cong et al, 2014) or machine learning (Mandelkow et al, 2016; Hu et al, 2017)

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