The missing social instinct

Smooth social interactions in everyday life rely on spontaneous understanding of emotions and intentions of others, conveyed by subtle social cues, such as gaze and facial expressions. In individuals with autism, however, who represent close to 1% of the population, this effortless and spontaneous understanding is impaired, and atypical eye contact as well as difficulties in social interaction are central to the condition. A lack of social instinct has been suggested as the essence of this neurodevelopmental disorder. In this work, I investigated configural face processing, interactions of emotions and eye gaze direction as well as empathy for pain in high- functioning young adults with autism spectrum disorders (ASD) using magnetic resonance imaging and behavioral measures. I also conducted anatomical investigations of white matter in adolescents and adults with autism to investigate structural differences underlying socio-cognitive processing. Findings showed that individuals with ASD process faces in a qualitatively similar manner as controls, namely configurally, as a unified whole. Moreover, the results showed that when participants are explicitly cued to the eye region, activation of cortical areas involved in social and emotional aspects of face processing reaches levels comparable to those observed in controls. When confronted with quick social gaze cues signaling an environmental threat, however, participants with ASD failed to show activation in areas associated with social attention, including brain regions driving eye gaze and emotion processing as well as the attribution of mental states. In contrast, affective empathy, referring to emotional contagion that has us “feeling like others” is preserved in ASD when viewing facial expressions of physical pain in others. Cognitive empathy on the other hand, which is associated with the attribution of mental states to others as well as top-down regulation of emotional arousal, seems impaired in ASD. In addition, across experiments, direct eye contact led to hyperactivation of subcortical regions suggesting hyperarousal in response to direct gaze that could underlie gaze avoidance observed in autism. Finally, we observed signs of delayed maturation in white matter tracts involved in emotional face processing in adolescents with ASD, but not in adults, which could be related to the improvements often observed in social interactions as individuals with autism enter adulthood. The studies conducted here shed light onto neural processes underlying social cognition deficits in ASD and provide clues for improving behavioral therapies.