Shared and Distinct Patterns of Functional Connectivity to Emotional Faces in Autism Spectrum Disorder and Attention-Deficit/Hyperactivity Disorder Children

Kristina Safar,Elizabeth Kelley,Robert Nicolson,Jennifer Crosbie,Margot J Taylor,Stelios Georgiades,Elizabeth W Pang,Jason P Lerch,Muhammed Ayub,Kathrina De Villa,Alana Iaboni,Marlee M Vandewouw,Evdokia Anagnostou,Russell Schachar

doi:10.3389/fpsyg.2022.826527

Abstract

Impairments in emotional face processing are demonstrated by individuals with neurodevelopmental disorders (NDDs), including autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD), which is associated with altered emotion processing networks. Despite accumulating evidence of high rates of diagnostic overlap and shared symptoms between ASD and ADHD, functional connectivity underpinning emotion processing across these two neurodevelopmental disorders, compared to typical developing peers, has rarely been examined. The current study used magnetoencephalography to investigate whole-brain functional connectivity during the presentation of happy and angry faces in 258 children (5–19 years), including ASD, ADHD and typically developing (TD) groups to determine possible differences in emotion processing. Data-driven clustering was also applied to determine whether the patterns of connectivity differed among diagnostic groups. We found reduced functional connectivity in the beta band in ASD compared to TD, and a further reduction in the ADHD group compared to the ASD and the TD groups, across emotions. A group-by-emotion interaction in the gamma frequency band was also observed. Greater connectivity to happy compared to angry faces was found in the ADHD and TD groups, while the opposite pattern was seen in ASD. Data-driven subgrouping identified two distinct subgroups: NDD-dominant and TD-dominant; these subgroups demonstrated emotion- and frequency-specific differences in connectivity. Atypicalities in specific brain networks were strongly correlated with the severity of diagnosis-specific symptoms. Functional connectivity strength in the beta network was negatively correlated with difficulties in attention; in the gamma network, functional connectivity strength to happy faces was positively correlated with adaptive behavioural functioning, but in contrast, negatively correlated to angry faces. Our findings establish atypical frequency- and emotion-specific patterns of functional connectivity between NDD and TD children. Data-driven clustering further highlights a high degree of comorbidity and symptom overlap between the ASD and ADHD children.

Highlights

Facial expressions facilitate social communication by providing extensive social cues offering insight into others’ emotional state and intentions; emotion recognition is essential for successful social functioning (Adolphs, 2002)
We capitalised on the superb resolution of MEG in the temporal, spatial and oscillatory domains to identify distinct patterns of functional connectivity between autism spectrum disorder (ASD), attentiondeficit/hyperactivity disorder (ADHD) and controls on an emotional face processing task
With the large sample size in this study, we were able to apply data-driven clustering methods to determine that ASD and ADHD children as neurodevelopmental disorders (NDDs) share similarities in underpinning neural mechanisms

Summary

Introduction

Facial expressions facilitate social communication by providing extensive social cues offering insight into others’ emotional state and intentions; emotion recognition is essential for successful social functioning (Adolphs, 2002). Atypical activation of core and extended face processing areas, including the primary visual cortex, fusiform gyri (FG), superior temporal sulcus (STS), amygdalae and insulae in ASD compared to typical development (TD), is well established (Critchley et al, 2000a, 2000b; Haxby et al, 2000; Pierce et al, 2001; Hubl et al, 2003; Ashwin et al, 2007; Deeley et al, 2007; Gobbini et al, 2007; Pelphrey et al, 2007; Corbett et al, 2009; di Martino et al, 2009; Leung et al, 2015, 2018, 2019), with several of these studies reporting under-activation of these areas to emotional faces in children and adults with the disorder. Functional resonance imaging (fMRI) studies have shown that children with ASD demonstrate under-activation of the FG and the amygdalae to faces and emotional faces (Wang et al, 2004; Pierce and Redcay, 2008; Corbett et al, 2009). Using magnetoencephalography (MEG), Leung et al (2019) demonstrated that children (7–10 years) with ASD show late under-activation in the thalamus and posterior cingulate cortex to happy and angry faces compared to TD peers

Methods

Results

Conclusion