Abstract

Objective: Despite the fact that autism spectrum disorder (ASD) is a common psychiatric diagnosis, knowledge about the special behavioral and neurobiological female phenotype is still scarce. The present study aimed to investigate neural correlates of empathy for physical and social pain and to assess the impact of egocentric perspective taking on social pain empathy in complex social situations in women and girls with ASD. Methods: Nine female individuals with high functioning ASD were compared to nine matched peers without ASD during two functional magnetic resonance imaging (fMRI) experiments, examining empathy for physical and social pain using well-established paradigms. Participants viewed multiple pictorial stimuli depicting a social target in either physically painful or socially unpleasant situations. In the social situations, the participant either shared the social target’s knowledge about the inappropriateness of the situation (observed social target is aware about the embarrassment of the situation; e.g., tripping in public) or not (observed social target is unaware about the embarrassment of the situation; e.g., open zipper). Results: Females with ASD did not rate the physical pain stimuli differently from non-clinical controls. Social pain situations, however, posed a greater challenge to females with ASD: For non-shared knowledge situations, females with ASD rated the social target’s embarrassment as more intense. Thus, compared to non-clinical controls, females with ASD had a stronger egocentric perspective of the situation rather than sharing the social target’s perspective. On the neural systems level, both groups showed activation of areas of the so-called empathy network that was attenuated in females with ASD during empathy for physical and social pain with a particular reduction in insula activation. Conclusion: Females with high functioning ASD are able to share another person’s physical or social pain on the neural systems level. However, hypoactivation of the anterior insula in contrast to individuals without ASD suggests that they are less able to rely on their shared representations of emotions along with difficulties to take over a person’s perspective and to make a clear distinction between their own and someone else’s experience of embarrassment.

Highlights

  • Autism spectrum disorder (ASD) is a pervasive neurodevelopmental disorder involving impairments in two core domains: social interaction, including verbal as well as non-verbal communication, and stereotyped, repetitive behaviors and interests [1]

  • F-CG and Female participants with ASD (F-ASD) both rated the protagonist’s physical pain as more intense for PP compared to no pain (NP), and the general intensity level of pain ratings as well as the responsiveness to PP vs. NP did not differ between groups (main effect of Group: F(1,16) = 0.18, p = .679; Group × Condition interaction: F(1,16) = 1.43, p = .249)

  • On the neural systems level, participants of both groups showed increased activations of the anterior cingulate cortex (ACC) during PP compared to NP (F-CG at −2, 26, 46, t(32) = 6.44, p < .001, k = 587; F-ASD at −6, 18, 36, t(32) = 5.12, p = .002, k = 407; see Figure 2A and Table 3)

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Summary

Introduction

Autism spectrum disorder (ASD) is a pervasive neurodevelopmental disorder involving impairments in two core domains: social interaction, including verbal as well as non-verbal communication, and stereotyped, repetitive behaviors and interests [1]. Neuroanatomical and neurofunctional differences between sexes/genders have been described [6], research on the female peculiarities is still insufficient and results are often inconsistent One reason for this lack of knowledge about the female ASD phenotype is the striking underrepresentation of females with ASD in neuroimaging research in general with an overall sex ratio of 8:1 (male:female). Research in mouse models for neurodevelopmental disorders suggests specific impairments in reward-directed learning only in male mice but not in females [10]. The relevance of such efforts and generalizability to human social cognition and the ASD phenotype, remains unclear. Thereby, we aim to broaden our perspective on the ASD phenotypes and to test specific assumptions about how the complexity of the social situation modulates the empathic response in females with ASD

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