Neural and behavioural indices of face processing in siblings of children with autism spectrum disorder (ASD): A longitudinal study from infancy to mid-childhood

Bosiljka Milosavljevic,Susie Chandler,Emily J H Jones ,Andrew Pickles,Ágnes Volein ,Leslie Tucker,Mayada Elsabbagh,Kristelle Hudry,Elizabeth Shephard,Patrick Bolton,Simon Baron‐Cohen ,Charlotte Tye,Greg Pasco,Rachael Bedford,Luke Mason,Tony Charman,Holly Garwood,Mark H Johnson,Janice Fernandes,Teodora Gliga

doi:10.1016/j.cortex.2020.02.008

Abstract

Impaired face processing is proposed to play a key role in the early development of autism spectrum disorder (ASD) and to be an endophenotypic trait which indexes genetic risk for the disorder. However, no published work has examined the development of face processing abilities from infancy into the school-age years and how they relate to ASD symptoms in individuals with or at high-risk for ASD. In this novel study we investigated neural and behavioural measures of face processing at age 7 months and again in mid-childhood (age 7 years) as well as social-communication and sensory symptoms in siblings at high (n = 42) and low (n = 35) familial risk for ASD. In mid-childhood, high-risk siblings showed atypical P1 and N170 event-related potential correlates of face processing and, for high-risk boys only, poorer face and object recognition ability compared to low-risk siblings. These neural and behavioural atypicalities were associated with each other and with higher social-communication and sensory symptoms in mid-childhood. Additionally, more atypical neural correlates of object (but not face) processing in infancy were associated with less right-lateralised (more atypical) N170 amplitudes and greater social-communication problems in mid-childhood. The implications for models of face processing in ASD are discussed.

Highlights

Autism spectrum disorder (ASD) is a neurodevelopmental condition characterised by social-communication impairments, restricted and repetitive behaviours and sensory atypicalities (American Psychiatric Association, 2013)
Face processing was assessed at age 7 months using eye-tracking measures of attention to face stimuli and neurophysiological correlates of face processing; we previously reported on these infant measures in relation to ASD outcomes at age 3 years and found atypical event-related potential (ERP) indices of face processing in high-risk infants who met diagnostic criteria for ASD (Elsabbagh et al, 2012; Tye et al, In submission) and atypically increased attention to face stimuli in high-risk infants that was independent of ASD outcomes (Elsabbagh et al, 2013) and was associated with poorer face recognition ability in early childhood
We addressed the following research questions and hypotheses: Question/Hypothesis 1: Cross-sectionally, do high-risk and low-risk siblings differ in face processing abilities in mid-childhood and are atypicalities in high-risk siblings driven by the subset of children with ASD? Following previous research, we predicted that high-risk siblings, regardless of ASD diagnosis, would show poorer face recognition performance and atypical neural correlates of face processing compared to low-risk siblings

Summary

Introduction

Autism spectrum disorder (ASD) is a neurodevelopmental condition characterised by social-communication impairments, restricted and repetitive behaviours and sensory atypicalities (American Psychiatric Association, 2013). Neurophysiological correlates of face processing such as the P1 and N170 event-related potential (ERP) components have been found to be atypical in children and adults with ASD (Kovarski et al, 2019; Neuhaus et al, 2015; Tye et al, 2013, see Kang et al, 2018; Sysoeva et al, 2018). The N170 is larger over the right than left hemisphere, larger and faster for face than non-face stimuli, and slower and/or larger when configural information concerning spatial relationships between facial features is disrupted (as is the case for inverted faces, for example); as such this component is thought to reflect early face-selective processes including extraction of configural information and categorisation of a stimulus as a face (Bentin et al, 1996; Ince et al, 2016; Itier & Taylor, 1999). In ASD, reduced right-hemisphere lateralisation of the N170 (Kovarski et al, 2019; Tye et al, 2013), slowed P1 (Neuhaus et al, 2016) and N170 (Kang et al, 2018; Sysoeva et al, 2018) latencies, reduced N170 amplitude (Kovarski et al, 2019) and increases (Batty et al, 2011) or decreases in P1 amplitudes (Kovarski et al, 2019) have been reported, suggestive of alterations in neural mechanisms underlying face processing

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