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Age-dependent changes in the neural substrates of empathy in autism spectrum disorder.

ABSTRACT: In typical development, empathic abilities continue to refine during adolescence and early adulthood. Children and adolescents with autism spectrum disorders (ASD) show deficits in empathy, whereas adults with ASD may have developed compensatory strategies. We aimed at comparing developmental trajectories in the neural mechanisms underlying empathy in individuals with ASD and typically developing control (TDC) subjects. Using an explicit empathizing paradigm and functional magnetic resonance imaging, 27 participants with ASD and 27 TDC aged 12-31 years were investigated. Participants were asked to empathize with emotional faces and to either infer the face's emotional state (other-task) or to judge their own emotional response (self-task). Differential age-dependent changes were evident during the self-task in the right dorsolateral prefrontal cortex, right medial prefrontal cortex, right inferior parietal cortex, right anterior insula and occipital cortex. Age-dependent decreases in neural activation in TDC were paralleled by either increasing or unchanged age-dependent activation in ASD. These data suggest ASD-associated deviations in the developmental trajectories of self-related processing during empathizing. In TDC, age-dependent modulations of brain areas may reflect the 'fine-tuning' of cortical networks by reduction of task-unspecific brain activity. Increased age-related activation in individuals with ASD may indicate the development of compensatory mechanisms.

SUBMITTER: Schulte-Ruther M

PROVIDER: S-EPMC4127013 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

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Age-dependent changes in the neural substrates of empathy in autism spectrum disorder.

Schulte-Rüther Martin M Greimel Ellen E Piefke Martina M Kamp-Becker Inge I Remschmidt Helmut H Fink Gereon R GR Herpertz-Dahlmann Beate B Konrad Kerstin K

Social cognitive and affective neuroscience 20130618 8

In typical development, empathic abilities continue to refine during adolescence and early adulthood. Children and adolescents with autism spectrum disorders (ASD) show deficits in empathy, whereas adults with ASD may have developed compensatory strategies. We aimed at comparing developmental trajectories in the neural mechanisms underlying empathy in individuals with ASD and typically developing control (TDC) subjects. Using an explicit empathizing paradigm and functional magnetic resonance ima ...[more]

PMID: 23784073

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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:Patients with autism spectrum disorder (ASD) often require sedation or general anesthesia. ASD is thought to arise from deficits in GABAergic signaling leading to abnormal neurodevelopment. We sought to investigate differences in how ASD patients respond to the GABAergic drug propofol by comparing the propofol-induced electroencephalogram (EEG) of ASD and neurotypical (NT) patients. This investigation was a prospective observational study. Continuous 4-channel frontal EEG was recorded during routine anesthetic care of patients undergoing endoscopic procedures between July 1, 2014 and May 1, 2016. Study patients were defined as those with previously diagnosed ASD by DSM-V criteria, aged 2-30 years old. NT patients were defined as those lacking neurological or psychiatric abnormalities, aged 2-30 years old. The primary outcome was changes in propofol-induced alpha (8-13 Hz) and slow (0.1-1 Hz) oscillation power by age. A post hoc analysis was performed to characterize incidence of burst suppression during propofol anesthesia. The primary risk factor of interest was a prior diagnosis of ASD. Outcomes were compared between ASD and NT patients using Bayesian methods. Compared to NT patients, slow oscillation power was initially higher in ASD patients (17.05 vs. 14.20 dB at 2.33 years), but progressively declined with age (11.56 vs. 13.95 dB at 22.5 years). Frontal alpha power was initially lower in ASD patients (17.65 vs. 18.86 dB at 5.42 years) and continued to decline with age (6.37 vs. 11.89 dB at 22.5 years). The incidence of burst suppression was significantly higher in ASD vs. NT patients (23.0% vs. 12.2%, p < 0.01) despite reduced total propofol dosing in ASD patients. Ultimately, we found that ASD patients respond differently to propofol compared to NT patients. A similar pattern of decreased alpha power and increased sensitivity to burst suppression develops in older NT adults; one interpretation of our data could be that ASD patients undergo a form of accelerated neuronal aging in adolescence. Our results suggest that investigations of the propofol-induced EEG in ASD patients may enable insights into the underlying differences in neural circuitry of ASD and yield safer practices for managing patients with ASD.

Project description:There has been increasing evidence of White Matter (WM) microstructural disintegrity and connectome disruption in Autism Spectrum Disorder (ASD). We evaluated the effects of age on WM microstructure by examining Diffusion Tensor Imaging (DTI) metrics and connectome Edge Density (ED) in a large dataset of ASD and control patients from different age cohorts. N = 583 subjects from four studies from the National Database of Autism Research were included, representing four different age groups: (1) A Longitudinal MRI Study of Infants at Risk of Autism [infants, median age: 7 (interquartile range 1) months, n = 155], (2) Biomarkers of Autism at 12 months [toddlers, 32 (11)m, n = 102], (3) Multimodal Developmental Neurogenetics of Females with ASD [adolescents, 13.1 (5.3) years, n = 230], (4) Atypical Late Neurodevelopment in Autism [young adults, 19.1 (10.7)y, n = 96]. For each subject, we created Fractional Anisotropy (FA), Mean- (MD), Radial- (RD), and Axial Diffusivity (AD) maps as well as ED maps. We performed voxel-wise and tract-based analyses to assess the effects of age, ASD diagnosis and sex on DTI metrics and connectome ED. We also optimized, trained, tested, and validated different combinations of machine learning classifiers and dimensionality reduction algorithms for prediction of ASD diagnoses based on tract-based DTI and ED metrics. There is an age-dependent increase in FA and a decline in MD and RD across WM tracts in all four age cohorts, as well as an ED increase in toddlers and adolescents. After correction for age and sex, we found an ASD-related decrease in FA and ED only in adolescents and young adults, but not in infants or toddlers. While DTI abnormalities were mostly limited to the corpus callosum, connectomes showed a more widespread ASD-related decrease in ED. Finally, the best performing machine-leaning classification model achieved an area under the receiver operating curve of 0.70 in an independent validation cohort. Our results suggest that ASD-related WM microstructural disintegrity becomes evident in adolescents and young adults-but not in infants and toddlers. The ASD-related decrease in ED demonstrates a more widespread involvement of the connectome than DTI metrics, with the most striking differences being localized in the corpus callosum.

Project description:Impairments in social communication (coupled with intact nonsocial language skills) are common in autism spectrum disorder (ASD). However, the neural correlates of these social communication deficits in adolescents and young adults with ASD are not fully understood. The communication checklist self-report (CC-SR) was administered to adolescents and young adults with ASD (n = 52) and typically developing (TD) controls (n = 64) to assess structural-language, pragmatic-language, and social-engagement. One high-resolution T1-weighted structural image was obtained from each participant. FreeSurfer was used to quantify cortical thickness. A main effect of diagnosis, with the ASD group performing worse than the TD group on all three CC-SR scales, and a diagnosis by scale interaction, driven by low social-engagement self-ratings in the ASD group, were found. There were also group differences in the relationship between scores on two of the three CC-SR scales and cortical thickness in multiple regions (pragmatic-language: left rostral frontal; social-engagement: left medial prefrontal). These interactions were driven by poorer self-ratings of language/social skills associated with decreased cortical thickness in the ASD group, while in the TD group worse self-ratings were associated with thicker cortex. Self-ratings of language/social-communication were lower in the ASD than the TD group. Moreover, language/social-communication self-ratings showed a different relationship with cortical thickness for the ASD and TD groups in the left inferior frontal region for pragmatic language ratings and the left medial prefrontal cortex for social engagement ratings. These findings suggest thinner cortex is associated with more impaired pragmatic language and social communication abilities in ASD. Autism Res 2018, 11: 1175-1186. © 2018 International Society for Autism Research, Wiley Periodicals, Inc. LAY SUMMARY: The present study examines the associations between brain structure and language/social communication ability in adolescents and young adults with autism spectrum disorder (ASD) as compared to neurotypical adolescents and young adults. We utilized thickness of the cerebral cortex as a measure of brain structure, and we found different correlations between language or social communication ability and cortical thickness in distinct regions for the ASD and TD groups. These findings suggest that for regions implicated in language/social communication ability, decreased cortical thickness is associated with more impaired pragmatic language and social communication abilities in ASD.

Project description:Recent longitudinal neuroimaging and neurophysiological studies have shown that tracking relative age-related changes in neural signals, rather than a static snapshot of a neural measure, could offer higher sensitivity for discriminating typically developing (TD) individuals from those with autism spectrum disorder (ASD). It is not clear, however, which aspects of age-related changes (trajectories) would be optimal for identifying atypical brain development in ASD. Using a large cross-sectional data set (Autism Brain Imaging Data Exchange [ABIDE] repository; releases I and II), we aimed to explore age-related changes in cortical thickness (CT) in TD and ASD populations (age range 6-30 years old). Cortical thickness was estimated from T1-weighted MRI images at three scales of spatial coarseness (three parcellations with different numbers of regions of interest). For each parcellation, three polynomial models of age-related changes in CT were tested. Specifically, to characterize alterations in CT trajectories, we compared the linear slope, curvature, and aberrancy of CT trajectories across experimental groups, which was estimated using linear, quadratic, and cubic polynomial models, respectively. Also, we explored associations between age-related changes with ASD symptomatology quantified as the Autism Diagnostic Observation Schedule (ADOS) scores. While no overall group differences in cortical thickness were observed across the entire age range, ASD and TD populations were different in terms of age-related changes, which were located primarily in frontal and tempo-parietal areas. These atypical age-related changes were also associated with ADOS scores in the ASD group and used to predict ASD from TD development. These results indicate that the curvature is the most reliable feature for localizing brain areas developmentally atypical in ASD with a more pronounced effect with symptomatology and is the most sensitive in predicting ASD development.

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.

Dataset Information

Age-dependent changes in the neural substrates of empathy in autism spectrum disorder.

Publications

Age-dependent changes in the neural substrates of empathy in autism spectrum disorder.

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