Preference for biological motion is reduced in ASD: implications for clinical trials and the search for biomarkers

Luke Mason ,Claudia Brogna ,Julian Tillmann ,Bhismadev Chakrabarti ,Carolin Moessnang ,Sven Bölte ,Terje Falck‐Ytter ,Joerg F Hipp ,Antonia San José Cáceres ,Sarah Baumeister ,Jessica Sabet ,Tobias Banaschewski ,Bob Oranje ,Gahan Pandina ,Tony Charman ,David Goyard ,Jack Waldman ,Andreas Meyer‐Lindenberg ,Ineke Cornelissen ,Yvette De Bruijn ,Vincent Frouin ,Will Spooren ,Sara Ambrosino ,René C.w Mandl ,Daisy Crawley ,Null Author_Id ,Emily J.h Jones ,André F Marquand ,Antonio M Persico ,Simon Baron‐Cohen ,Michael Brammer ,Christian F Beckmann ,Rosemary Holt ,Marcel P Zwiers ,Lindsay Ham ,Roberto Sacco ,Declan Murphy ,Roberto Toro ,Daniel Brandeis ,Michael Lombardo ,Maarten Mennes ,Eva Loth ,Marianne Oldehinkel ,Xavier Liogier D’ardhuy ,Jan K Buitelaar ,Carsten Bours ,Caroline Wooldridge ,Sarah Durston ,Frederick Shic ,Chris Chatham ,David J Lythgoe ,Laurence O’dwyer ,Nico Bast ,Flavio Dell’acqua ,Jessica Faulkner ,Meng‐Chuan Lai ,Heike Tost ,Amber N V Ruigrok ,Christine Ecker ,Steve Williams ,Bethany Oakley ,Emily Simonoff ,Pilar Garcés ,Mark H Johnson ,Barbara Ruggeri ,Guillaume Dumas ,Thomas Bougeron

doi:10.1186/s13229-021-00476-0

Abstract

BackgroundThe neurocognitive mechanisms underlying autism spectrum disorder (ASD) remain unclear. Progress has been largely hampered by small sample sizes, variable age ranges and resulting inconsistent findings. There is a pressing need for large definitive studies to delineate the nature and extent of key case/control differences to direct research towards fruitful areas for future investigation. Here we focus on perception of biological motion, a promising index of social brain function which may be altered in ASD. In a large sample ranging from childhood to adulthood, we assess whether biological motion preference differs in ASD compared to neurotypical participants (NT), how differences are modulated by age and sex and whether they are associated with dimensional variation in concurrent or later symptomatology.MethodsEye-tracking data were collected from 486 6-to-30-year-old autistic (N = 282) and non-autistic control (N = 204) participants whilst they viewed 28 trials pairing biological (BM) and control (non-biological, CTRL) motion. Preference for the biological motion stimulus was calculated as (1) proportion looking time difference (BM-CTRL) and (2) peak look duration difference (BM-CTRL).ResultsThe ASD group showed a present but weaker preference for biological motion than the NT group. The nature of the control stimulus modulated preference for biological motion in both groups. Biological motion preference did not vary with age, gender, or concurrent or prospective social communicative skill within the ASD group, although a lack of clear preference for either stimulus was associated with higher social-communicative symptoms at baseline.LimitationsThe paired visual preference we used may underestimate preference for a stimulus in younger and lower IQ individuals. Our ASD group had a lower average IQ by approximately seven points. 18% of our sample was not analysed for various technical and behavioural reasons.ConclusionsBiological motion preference elicits small-to-medium-sized case–control effects, but individual differences do not strongly relate to core social autism associated symptomatology. We interpret this as an autistic difference (as opposed to a deficit) likely manifest in social brain regions. The extent to which this is an innate difference present from birth and central to the autistic phenotype, or the consequence of a life lived with ASD, is unclear.

Highlights

Autism spectrum disorder (ASD) is a lifelong pervasive developmental condition, characterised by social-communication and interaction difficulties and the presence of restricted and repetitive behaviours [2]
The extent to which this is an innate differ‐ ence present from birth and central to the autistic phenotype, or the consequence of a life lived with autism spectrum disorder (ASD), is unclear
Observational studies may provide insights into the mechanisms that underpin symptom emergence and persistence and inform treatment development. Such studies are often characterised by small sample sizes and a focus on limited age ranges (Federici et al categorised studies by age, as either “children”, “adolescents” or “adults” with no studies having a sample that spanned more than one category), leading to inconsistent findings and gaps in the literature

Summary

Introduction

Autism spectrum disorder (ASD) is a lifelong pervasive developmental condition, characterised by social-communication and interaction difficulties and the presence of restricted and repetitive behaviours [2]. Observational studies may provide insights into the mechanisms that underpin symptom emergence and persistence and inform treatment development Such studies are often characterised by small sample sizes (the median N in Federici et al.’s [15] meta-analysis of biological motion in ASD was 31.5) and a focus on limited age ranges (Federici et al categorised studies by age, as either “children”, “adolescents” or “adults” with no studies having a sample that spanned more than one category), leading to inconsistent findings and gaps in the literature. There is a need for rigorous observational studies with large sample sizes to identify neurocognitive mechanisms that can characterise or stratify the ASD phenotype, and serve as endpoints for use in the development of treatments [31]. In a large sample ranging from childhood to adulthood, we assess whether biological motion preference differs in ASD compared to neurotypical participants (NT), how dif‐ ferences are modulated by age and sex and whether they are associated with dimensional variation in concurrent or later symptomatology

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