A typical social attention behaviors and its underlying neural mechanism in individuals with autism spectrum disorder

Abstract

The ability to coordinate attention to events or objects between interactive social partners, referred to as social attention, is of great significance for adaptive social behaviors and nonverbal communications in our daily life, helping us to infer other person’s inner state (e.g., intentions, goals) and learn about where important events (e.g., food, danger) occur in the environment. In recent years, many studies have demonstrated that social cues (e.g., eye gaze, head orientation and walking direction of biological motion) can trigger reflexive attentional orienting effects using adapted central cueing paradigm originally designed by Posner. However, not all of us are equally adept at directing attention to where others are focusing on, and this ability is strongly impaired in individuals with autism spectrum disorder (ASD), a highly genetic neurodevelopmental disorder marked by striking social deficits and repetitive behaviors. Here we systematically reviewed recent work on abnormal social attention behaviors and its underlying neural mechanisms in ASD. We first expatiated a typical social attention behaviors indexed by covert and overt attention in ASD. It has been documented that ASD individuals tend to show reduced reflexive orienting effect manifesting itself in both covert attention and overt eye movement compared to typically developing individuals (TD). Yet some controversies concerning the malfunction of social attention in ASD remain to be resolved, based on some evidence demonstrating comparable orienting effect between ASD and TD group. Then we summarized the development course of social attention in ASD. Crucially, atypical orienting to eye gaze is more likely to be observed in younger children but not older children or adults with ASD. It is reasonable to postulate that ASD individuals may acquire this ability through overlearning the association between social cues and targets in everyday life as they grow older. Furthermore, we discussed the neural basis of abnormal social attention behaviors in ASD. Using a combination of psychophysical paradigms and neuroimaging techniques, researchers have reported atypical neural activities in superior temporal gyrus and prefrontal cortex under the supraliminal condition as well as abnormal activation in amygdala under the subliminal condition in the brain of ASD. Moreover, the ASD group showed much less difference in activation of frontoparietal attention networks between social and nonsocial attention task than the TD group, implying disruptive social attention in ASD. Finally, several perspectives on further investigations were put forward given the controversies and insufficient evidence concerning the malfunction of social attention in ASD. Future studies should employ multiple types of social cues (e.g., eye gaze and walking direction of biological motion) in conjunction with more ecological paradigms to investigate conscious and non-conscious social attention behaviors from a developmental approach. More importantly, more neuroimaging studies are needed to explore the functional connections among several key cortical regions and subcortical regions underlying atypical social attention behaviors in ASD. Such efforts will help to facilitate the early diagnosis and intervention of ASD.