Atypical Intrinsic Functional Connectivity of Core Face Perception System Is Associated with Symptom Severity in ASD

Background:  One of the core symptoms of Autism Spectrum Disorder (ASD) is a deficit in social communication. Individuals with ASD have impairments in face processing, a crucial component of reciprocal social interactions, including deficits in gaze processing and face identification. Face processing relies on the core face perception system, which includes the fusiform face area (FFA), occipital face area (OFA), and the posterior superior temporal sulcus (pSTS). 

Objectives:  Given the observed deficits in face perception in ASD and the prevalent theory that ASD is a disorder of network dysfunction and abnormal brain connectivity, we examined the functional network organization of the core face perception system in children and adolescents with ASD using intrinsic functional connectivity (iFC).

Methods:  We performed whole-brain iFC analysis using bilateral FFA, OFA and pSTS as seed regions (Tahmasebi et al., 2012) in 35 children and adolescents with ASD (aged 8-17 years) and 36 typically developing (TD) participants matched for age, gender, IQ, and in-scanner head motion. 

Results:  Between-group comparisons revealed two main clusters of differential iFC shared across most seeds. Underconnectivity (ASD < TD) with the right IFG, part of the extended face perception system (Fairhall & Ishai, 2007), was found for bilateral FFA, right OFA, and bilateral pSTS seeds. The degree of underconnectivity between right IFG and right FFA, and between right IFG and right OFA was correlated with ADOS-2 Total scores, such that weaker connectivity, compared to TD, was associated with greater symptom severity. Overconnectivity (ASD > TD) with the PCC was found for the bilateral FFA and OFA seeds. Additionally, right FFA seed also yielded overconnectivity in or close to default mode network (DMN) nodes, including the mid orbital gyrus and bilateral angular gyri. The extent of overconnectivity between right FFA and DMN regions was also correlated with ADOS-2 Total scores: Individuals with ASD with greater connectivity between right FFA and DMN regions had more ASD symptoms. 

Conclusions:  Our findings indicate atypical iFC patterns of core face perception regions in children and adolescents with ASD. Individuals with ASD exhibited reduced segregation between the core face perception system and out-of-network regions, such as the DMN, and reduced integration between the core and extended face perception systems. The link between increased ASD symptomatology and atypical connectivity patterns of the core face perception system suggests that compromised face perception network integrity may contribute to social communication deficits observed in ASD.