Impaired social brain network for processing dynamic facial expressions in autism spectrum disorders

Wataru Sato,Shota Uono,Takanori Kochiyama,Motomi Toichi

doi:10.1186/1471-2202-13-99

Abstract

BackgroundImpairment of social interaction via facial expressions represents a core clinical feature of autism spectrum disorders (ASD). However, the neural correlates of this dysfunction remain unidentified. Because this dysfunction is manifested in real-life situations, we hypothesized that the observation of dynamic, compared with static, facial expressions would reveal abnormal brain functioning in individuals with ASD.We presented dynamic and static facial expressions of fear and happiness to individuals with high-functioning ASD and to age- and sex-matched typically developing controls and recorded their brain activities using functional magnetic resonance imaging (fMRI).ResultRegional analysis revealed reduced activation of several brain regions in the ASD group compared with controls in response to dynamic versus static facial expressions, including the middle temporal gyrus (MTG), fusiform gyrus, amygdala, medial prefrontal cortex, and inferior frontal gyrus (IFG). Dynamic causal modeling analyses revealed that bi-directional effective connectivity involving the primary visual cortex–MTG–IFG circuit was enhanced in response to dynamic as compared with static facial expressions in the control group. Group comparisons revealed that all these modulatory effects were weaker in the ASD group than in the control group.ConclusionsThese results suggest that weak activity and connectivity of the social brain network underlie the impairment in social interaction involving dynamic facial expressions in individuals with ASD.

Highlights

Impairment of social interaction via facial expressions represents a core clinical feature of autism spectrum disorders (ASD)
These results suggest that weak activity and connectivity of the social brain network underlie the impairment in social interaction involving dynamic facial expressions in individuals with ASD
Because dynamic facial expressions are realistic mediums for social interaction, our results suggest that the weak activation in these social brain regions is related to the real-life impairments in communication via facial expressions experienced by individuals with ASD

Summary

Introduction

Impairment of social interaction via facial expressions represents a core clinical feature of autism spectrum disorders (ASD). Several previous behavioral studies reported that individuals with ASD exhibited less attention [3], attenuated emotional behaviors [4], and reduced and/or inappropriate facial reactions [5] in Several neuroimaging studies using functional magnetic resonance imaging (fMRI) and positron emission tomography tested the neural substrates of impaired facial-expression processing in ASD and reported inconsistent findings Almost all these studies used photos of emotional facial expressions as stimuli and found that individuals with ASD showed abnormal activities in several brain regions, including the posterior superior temporal sulcus (STS) or its adjacent regions such as the middle temporal gyrus (MTG) [6,7,8], the posterior fusiform gyrus (FG) [7,9,10,11,12,13], amygdala (AMY) [6,7,8,12], medial prefrontal cortex (MPFC) at around the medial superior frontal gyrus [8,14], and the inferior frontal gyrus (IFG) [9,15,16]. Whether the neural substrates of impaired expression processing in ASD can be traced to reduced activity in any specific brain region and/or to reduced connectivity among the regions, which has been suggested in other lines of ASD research (cf. [29]), remains unknown

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Discussion

Conclusion