The missing social instinct | EPFL Graph Search

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.

It's All in the Eyes: Subcortical and Cortical Activation during Grotesqueness Perception in Autism

Nouchine Hadjikhani, Loyse Hippolyte, Ophélie Rogier, Britt Russo

Atypical face processing plays a key role in social interaction difficulties encountered by individuals with autism. In the current fMRI study, the Thatcher illusion was used to investigate several aspects of face processing in 20 young adults with high-functioning autism spectrum disorder (ASD) and 20 matched neurotypical controls. "Thatcherized" stimuli were modified at either the eyes or the mouth and participants discriminated between pairs of faces while cued to attend to either of these features in upright and inverted orientation. Behavioral data confirmed sensitivity to the illusion and intact configural processing in ASD. Directing attention towards the eyes vs. the mouth in upright faces in ASD led to (1) improved discrimination accuracy; (2) increased activation in areas involved in social and emotional processing; (3) increased activation in subcortical face-processing areas. Our findings show that when explicitly cued to attend to the eyes, activation of cortical areas involved in face processing, including its social and emotional aspects, can be enhanced in autism. This suggests that impairments in face processing in autism may be caused by a deficit in social attention, and that giving specific cues to attend to the eye-region when performing behavioral therapies aimed at improving social skills may result in a better outcome.

Public Library Science2013

Perception of Social Cues of Danger in Autism Spectrum Disorders

Nouchine Hadjikhani, Loyse Hippolyte, Ophélie Rogier, Torsten Ruest, Britt Russo

Intuitive grasping of the meaning of subtle social cues is particularly affected in autism spectrum disorders (ASD). Despite their relevance in social communication, the effect of averted gaze in fearful faces in conveying a signal of environmental threat has not been investigated using real face stimuli in adults with ASD. Here, using functional MRI, we show that briefly presented fearful faces with averted gaze, previously shown to be a strong communicative signal of environmental danger, produce different patterns of brain activation than fearful faces with direct gaze in a group of 26 normally intelligent adults with ASD compared with 26 matched controls. While implicit cue of threat produces brain activation in attention, emotion processing and mental state attribution networks in controls, this effect is absent in individuals with ASD. Instead, individuals with ASD show activation in the subcortical face-processing system in response to direct eye contact. An effect of differences in looking behavior was excluded in a separate eye tracking experiment. Our data suggest that individuals with ASD are more sensitive to direct eye contact than to social signals of danger conveyed by averted fearful gaze.

Public Library Science2013

Emotional contagion for pain is intact in autism spectrum disorders

Nouchine Hadjikhani, Loyse Hippolyte, Ophélie Rogier, Torsten Ruest

Perceiving others in pain generally leads to empathic concern, consisting of both emotional and cognitive processes. Empathy deficits have been considered as an element contributing to social difficulties in individuals with autism spectrum disorders (ASD). Here, we used functional magnetic resonance imaging and short video clips of facial expressions of people experiencing pain to examine the neural substrates underlying the spontaneous empathic response to pain in autism. Thirty-eight adolescents and adults of normal intelligence diagnosed with ASD and 35 matched controls participated in the study. In contrast to general assumptions, we found no significant differences in brain activation between ASD individuals and controls during the perception of pain experienced by others. Both groups showed similar levels of activation in areas associated with pain sharing, evidencing the presence of emotional empathy and emotional contagion in participants with autism as well as in controls. Differences between groups could be observed at a more liberal statistical threshold, and revealed increased activations in areas involved in cognitive reappraisal in ASD participants compared with controls. Scores of emotional empathy were positively correlated with brain activation in areas involved in embodiment of pain in ASD group only. Our findings show that simulation mechanisms involved in emotional empathy are preserved in high-functioning individuals with autism, and suggest that increased reappraisal may have a role in their apparent lack of caring behavior.

Nature Publishing Group2014