Emotional contagion for pain is intact in autism spectrum disorders

Abstract

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.

Figure 1

Scores for autism spectrum disorder (ASD) and control (CON) participants for each of the subcomponents of the EQ test.

Figure 2

Activation for the (PAIN>NO PAIN) condition in participants with ASD (ASD; top panel), control participants (CON) (middle panel) and difference between groups (bottom panel). Separate group data are shown at a threshold of P<0.05, cluster corrected. Between-groups comparison is shown with a threshold of P<0.01.

Figure 3

Areas showing positive correlation with emotional Empathy Quotient (EQ) in autism spectrum disorder (ASD). Data are thresholded at P<0.05, cluster corrected.

Figure 4

Correlation between Autism Spectrum Quotient (AQ) level and activation in the dorsolateral prefrontal cortex (dlPFC), rostrolateral prefrontal cortex (rlPFC), anterior cingulate cortex (ACC) and temporo-parietal junction (TPJ) across all participants.

Figure 5

Schematic description of reaction to other's pain in typical individuals (top panel) and in autism spectrum disorder (ASD; bottom panel), modified from Decety.⁸² In typical individuals, affective arousal (involving subcortical circuits together with the orbito-frontal cortex (OFC) and the superior temporal sulcus (STS)) is followed by emotion understanding, a capacity that develops around the age of 2–3 years, and that overlaps with the theory of mind (ToM)-like processes, involving the medial prefrontal cortex (mPFC) and temporal pole. Emotion understanding leads to the regulation of emotion, through dorsolateral prefrontal cortex (dlPFC) and anterior cingulate cortex (ACC), allowing reappraisal mechanisms to downregulate affective arousal. In ASD, increased affective arousal, possibly due to subcortical circuits abnormality, and deficits in ToM processes lead to the need for increased emotional regulation through reappraisal, via increased activation in dlPFC and ACC. This increased regulation of emotions may be perceived by others as a lack of caring behavior.