Abstract
Atypical reciprocal social interactions involving emotional facial expressions are a core clinical feature of autism spectrum disorder (ASD). Previous functional magnetic resonance imaging (fMRI) studies have demonstrated that some social brain regions, including subcortical (e.g., amygdala) and neocortical regions (e.g., fusiform gyrus, FG) are less activated during the processing of facial expression stimuli in individuals with ASD. However, the functional networking patterns between the subcortical and cortical regions in processing emotional facial expressions remain unclear. We investigated this issue in ASD (n = 31) and typically developing (TD; n = 31) individuals using fMRI. Participants viewed dynamic facial expressions of anger and happiness and their corresponding mosaic images. Regional brain activity analysis revealed reduced activation of several social brain regions, including the amygdala, in the ASD group compared with the TD group in response to dynamic facial expressions vs. dynamic mosaics (p < 0.05, = 0.19). Dynamic causal modeling (DCM) analyses were then used to compare models with forward, backward, and bi-directional effective connectivity between the amygdala and neocortical networks. The results revealed that: (1) the model with effective connectivity from the amygdala to the neocortex best fit the data of both groups; and (2) the same model best accounted for group differences. Coupling parameter (i.e., effective connectivity) analyses showed that the modulatory effects of dynamic facial processing were substantially weaker in the ASD group than in the TD group. These findings suggest that atypical modulation from the amygdala to the neocortex underlies impairment in social interaction involving dynamic facial expressions in individuals with ASD.
Highlights
Individuals with autism spectrum disorder (ASD) exhibit atypical social interactions (American Psychiatric Association, 2013)
region of interest (ROI) analyses were conducted for predefined social brain regions, including the amygdala, V5, fusiform gyrus (FG), superior temporal sulcus (STS) region, and inferior frontal gyrus (IFG), using a multivariate analysis of covariance (MANCOVA) with group, stimulus type, and emotion as factors and sex and age as covariates
Follow-up univariate t-tests for the difference between dynamic facial expressions vs. dynamic mosaics confirmed significantly reduced activity in the ASD group compared with that in the typically developing (TD) group in the amygdala, V5/MT, and FG (t(60) > 2.08; p < 0.05), group differences were marginally significant in the STS region (t(60) = 1.54; p < 0.1) and not significant in the IFG (t(60) = 0.61; p > 0.1; Supplementary Figure S2)
Summary
Individuals with autism spectrum disorder (ASD) exhibit atypical social interactions (American Psychiatric Association, 2013). Abundant neuroimaging and neuropsychological evidence from TD individuals suggests that these brain regions are involved in the specific processing of social stimuli, such as emotional processing in the amygdala (for a review, see Calder et al, 2001), visual analysis of faces in the FG and STS region (for a review, see Haxby et al, 2000), and motor resonance in the IFG (for a review, see Rizzolatti et al, 2001) These regions have been called the ‘‘social brain’’ regions (Brothers et al, 1990; Adolphs, 2003; Blakemore, 2008) and were proposed to be impaired in individuals with ASD (Baron-Cohen et al, 2000; Emery and Perrett, 2000; Johnson et al, 2005; Bachevalier and Loveland, 2006; Frith, 2007; Pelphrey and Carter, 2008).
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