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Autonomic and brain responses associated with empathy deficits in autism spectrum disorder.

ABSTRACT: Accumulating evidence suggests that autonomic signals and their cortical representations are closely linked to emotional processes, and that related abnormalities could lead to social deficits. Although socio-emotional impairments are a defining feature of autism spectrum disorder (ASD), empirical evidence directly supporting the link between autonomic, cortical, and socio-emotional abnormalities in ASD is still lacking. In this study, we examined autonomic arousal indexed by skin conductance responses (SCR), concurrent cortical responses measured by functional magnetic resonance imaging, and effective brain connectivity estimated by dynamic causal modeling in seventeen unmedicated high-functioning adults with ASD and seventeen matched controls while they performed an empathy-for-pain task. Compared to controls, adults with ASD showed enhanced SCR related to empathetic pain, along with increased neural activity in the anterior insular cortex, although their behavioral empathetic pain discriminability was reduced and overall SCR was decreased. ASD individuals also showed enhanced correlation between SCR and neural activities in the anterior insular cortex. Importantly, significant group differences in effective brain connectivity were limited to greater reduction in the negative intrinsic connectivity of the anterior insular cortex in the ASD group, indicating a failure in attenuating anterior insular responses to empathetic pain. These results suggest that aberrant interoceptive precision, as indexed by abnormalities in autonomic activity and its central representations, may underlie empathy deficits in ASD.

SUBMITTER: Gu X

PROVIDER: S-EPMC4545680 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

Project description:Attention Deficit Hyperactivity Disorder (ADHD) and Autism Spectrum Disorders (ASD) are two of the most represented neurodevelopmental conditions in childhood. The diagnostic shift introduced by the DSM-5, allowing a combined diagnosis of ADHD and ASD, poses different clinical challenges related to diagnostic overshadowing, accuracy of clinical judgment and potential delay in an ASD diagnosis in children presenting with ADHD. Here we tried to disentangle the clinical phenotype and specificity of the two co-occurring conditions in relation to autism traits and empathy, by comparing children with ASD with and without comorbid ADHD with children presenting ADHD only and children with typical development. The child versions of the Autism Quotient (C-AQ) and Empathy Quotient (C-EQ) were administered to a total sample of 198 male children between 6 and 14 years old with age appropriate language skills and normal intelligence. Univariate analysis demonstrated no significant differences in the C-AQ total and subscale scores as well as the C-EQ between children with ASD and children with ASD + ADHD, while children with ADHD alone presented an intermediate phenotype between ASD and TD. Furthermore, a receiver operating characteristic (ROC) analysis was applied to discriminate among the different phenotypes. We found that the C-AQ and C-EQ were accurate at distinguishing with satisfactory reliability between: (a) ASD vs. non- ASD (N-ASD) groups comprising both ADHD and TD children (Area Under the Curve AUC 88% for C-AQ and 81% for C-EQ); (b) ASD and TD (AUC 92% for C-AQ and 95% for C-EQ); (c) ASD and ADHD (AUC 80% for C-AQ and 68% for C-EQ). Our data confirm the reliability of the C-AQ and C-EQ as behavioral markers to differentiate ASD (regardless of comorbid ADHD) from an ADHD condition and TD. Interestingly, in our sample an ADHD condition does not increase the severity of the clinical phenotype in terms of autism traits distribution and empathy, suggesting that the psychological measures detected by the two quantitative instruments are independent of ADHD traits. This evidence will contribute to the translational efforts in developing better tailored treatments and preventive strategies.

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Autonomic and brain responses associated with empathy deficits in autism spectrum disorder.

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