Evidence from pupillometry and fMRI indicates reduced neural response during vicarious social pain but not physical pain in autism

Abstract

Autism spectrum disorder (ASD) is characterized by substantial social deficits. The notion that dysfunctions in neural circuits involved in sharing another's affect explain these deficits is appealing, but has received only modest experimental support. Here we evaluated a complex paradigm on the vicarious social pain of embarrassment to probe social deficits in ASD as to whether it is more potent than paradigms currently in use. To do so we acquired pupillometry and fMRI in young adults with ASD and matched healthy controls. During a simple vicarious physical pain task no differences emerged between groups in behavior, pupillometry, and neural activation of the anterior insula (AIC) and anterior cingulate cortex (ACC). In contrast, processing complex vicarious social pain yielded reduced responses in ASD on all physiological measures of sharing another's affect. The reduced activity within the AIC was thereby explained by the severity of autistic symptoms in the social and affective domain. Additionally, behavioral responses lacked correspondence with the anterior cingulate and anterior insula cortex activity found in controls. Instead, behavioral responses in ASD were associated with hippocampal activity. The observed dissociation echoes the clinical observations that deficits in ASD are most pronounced in complex social situations and simple tasks may not probe the dysfunctions in neural pathways involved in sharing affect. Our results are highly relevant because individuals with ASD may have preserved abilities to share another's physical pain but still have problems with the vicarious representation of more complex emotions that matter in life.

Keywords: autism spectrum disorder; embarrassment; empathy; social complexity; social neuroscience; vicarious emotions; vicarious physical pain; vicarious social pain.

Figure 1

Experimental paradigms to induce physical pain (PP) and social pain (SP). A: The upper row illustrates one example stimulus of the experimental paradigm to induce PP (left) and one of the neutral control condition (PN, right, stimuli were taken from Jackson et al., 2005). The lower row illustrates one example stimulus of the experimental paradigm to induce SP (left) and one of the neutral control condition (SN, right [Krach et al., 2011]. Sketches depict a protagonist, indicated by the red arrow above his/her head, in potentially embarrassing or neutral situations. During the fMRI measurements, each sketch was accompanied by a sentence introducing the current scenario. B: The sequence of events during the functional MRI scanning is exemplified for PP/PN (upper row) and SP/SN (lower row) together with the subsequent rating periods and low‐level baselines. The red arrow illustrates the weighting procedure of the PP and SP events with the intensity ratings provided after stimulus presentation. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Brain activation during physical pain (PP) and social pain (SP). A: Brain activation for main effect of task (PP‐PN) for patients with autism spectrum disorders (ASD) and healthy controls (HC). B: Brain activation for main effect of task (SP‐SN) for patients with ASD and HCs. C: Parameter estimates of the left anterior insula cortex (AIC) and the anterior cingulate cortex (ACC) show reduction of SP‐related activation in the ASD group. Parameter estimates are plotted together with standard errors at the peak voxel and illustrate the contrast of SP‐SN for each group within the left AIC and the ACC (see also Supporting Information Fig. S2 and Table II). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 3

Association of anterior insula (AIC) activation with individual differences in symptom severity as measured with the autism diagnostic observational schedule (ADOS). Spearman's rho correlation coefficients (r _s) are depicted together with the slope of the linear fit between symptom severity and AIC activation. The association of symptom severity in the domain of social affect with AIC activation significantly differs between physical and social pain (P = 0.007) and individuals with autism spectrum disorders show less pronounced AIC activation with stronger symptom severity.

Figure 4

Association of within‐subject variability in the intensity of the vicarious physical pain (PP) and social pain (SP) with hemodynamic responses in both groups. A: Neural network comprising the left anterior insula cortex (AIC) and the anterior cingulate cortex (ACC) that was significantly associated with the intensity of the self‐report during PP in the healthy control (HC) group. In patients with autism spectrum disorders (ASD) there was no significant correspondence between the intensity of the self‐report and the hemodynamic response during PP. B: Neural network comprising the left AIC and the ACC that was significantly associated with the intensity of the self‐report during SP in the HC group. In patients with ASD there was no significant correspondence between the intensity of the self‐report and the hemodynamic response during SP. C: Direct comparison between ASD and HC in terms of correspondence between SP self‐report and hemodynamic response. Stronger associations in ASD are coded in red, stronger associations in HC are coded in green. Parameter estimates of areas showing significant differences between groups are plotted together with standard errors at the peak voxel (Supporting Information Fig. S2 and Table IV). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]