Evaluation of the Social Motivation Hypothesis of Autism

Clements, Caitlin C.; Zoltowski, Alisa; Yankowitz, Lisa; Yerys, Benjamin E.; Herrington, John D.

doi:10.1001/jamapsychiatry.2018.1100

Cited by 228 publications

(214 citation statements)

References 71 publications

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“…Together with deviant structural and functional connectivity between frontal cortical areas and striatum in autism (46,50,51), structural covariation in striatum and frontal areas may underlie atypical functional fronto-striatal connectivity, and this has been associated with repetitive behavior and executive functioning impairments in autism (3,44). In the present study, the density of caudate nuclei increase simultaneously with densities decreasing on other areas in autism, which fits with the results of a few functional studies that indicate inverse functional changes of these areas (52). Particularly, the special pattern of GM densities changes in frontal and striatal areas might serve an important role in autism-related symptoms.…”

Section: Discussionsupporting

confidence: 89%

Gray matter covariations and core symptoms of autism. The EU-AIMS Longitudinal European Autism Project

Mei

Llera

Floris

et al. 2020

Preprint

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BackgroundVoxel-based Morphometry (VBM) studies in Autism Spectrum Disorder (autism) have yielded diverging results. This might partly be attributed to structural alterations being associating with the combined influence of several regions rather than with a single region. Further, these structural covariation differences may relate to continuous measures of autism rather than with categorical case-control contrasts. The current study aimed to identify structural covariation alterations in autism, and assessed canonical correlations between brain covariation patterns and core autism symptoms.MethodsWe studied 347 individuals with autism and 252 typically developing individuals, aged between 6 and 30 years, who have been deeply phenotyped in the Longitudinal European Autism Project (LEAP). All participants’ VBM maps were decomposed into spatially independent components using Independent Component Analysis. A Generalized Linear Model (GLM) was used to examine case-control differences. Next, Canonical Correlation Analysis (CCA) was performed to separately explore the integrated effects between all the brain sources of gray matter variation and two sets of core autism symptoms.ResultsGLM analyses showed significant case-control differences for two independent components. The first component was primarily associated with decreased density of bilateral insula, inferior frontal gyrus, orbitofrontal cortex, and increased density of caudate nucleus in the autism group relative to typically developing individuals. The second component was related to decreased densities of the bilateral amygdala, hippocampus, and parahippocampal gyrus in the autism group relative to typically developing individuals. The CCA results showed significant correlations between components that involved variation of thalamus, putamen, precentral gyrus, frontal, parietal, and occipital lobes, and the cerebellum, and repetitive, rigid and stereotyped behaviors and abnormal sensory behaviors in autism individuals.LimitationsOnly 55.9% of the participants with autism had complete questionnaire data on continuous parent-reported symptom measures.ConclusionsCovaried areas associated with autism diagnosis and/or symptoms are scattered across the whole brain and include the limbic system, basal ganglia, thalamus, cerebellum, precentral gyrus, and parts of the frontal, parietal, and occipital lobes. Some of these areas potentially subserve social-communicative behavior whereas others may underpin sensory processing and integration, and motor behavior.

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Section: Discussionsupporting

confidence: 89%

Gray matter covariations and core symptoms of autism. The EU-AIMS Longitudinal European Autism Project

Mei

Llera

Floris

et al. 2020

Preprint

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“…Extensive neuroimaging research has implicated the brain's reward network in delay discounting, with individual differences in reward system activation related to behavioral differences in delay discounting and to atypical discounting behaviors in clinical groups (see Peters & Büchel, and Lempert et al, for reviews). Thus, discounting tasks may help inform current debates in the literature about the extent to which ASD is characterized by atypical reward processing (Clements et al, ). Additionally, although delay and social discounting tasks both involve reward processing, only social discounting involves the reward of giving to another, which may recruit social‐cognitive brain networks outside of the reward system (Morelli, Sacchet, & Zaki, ).…”

Section: Introductionmentioning

confidence: 99%

Social and delay discounting in autism spectrum disorder

et al. 2019

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Current literature is divided over whether and how processes such as perspective taking and reward sensitivity differ between individuals with autism spectrum disorder (ASD) versus neurotypical individuals. Discounting tasks may provide novel insight into how these processes operate. In delay discounting tasks, participants choose between smaller immediate rewards and larger delayed rewards, and in social discounting tasks, participants choose between a smaller monetary rewards for themselves versus a larger reward for partners of varied social distance (e.g., a close friend vs. an acquaintance). Delay and social discounting tasks thus implicitly measure the subjective value of rewards given to one's future self and to others, capturing constructs such as perspective taking, reward processing, and social closeness, all of which have been discussed as core cognitive mechanisms underlying ASD. Despite extensive research on discounting in other clinical populations, few studies have examined delay discounting in ASD and no research has examined social discounting in ASD. The goal of the current study was to assess delay and social discounting for monetary rewards in a single sample of adolescents and adults with ASD compared to a matched neurotypical sample. Overall, adults and adolescents with ASD valued both future rewards and rewards given to others less than their typical counterparts did, but rates of discounting were not significantly correlated across temporal and social domains. These results extend an important behavioral paradigm for understanding both perspective taking and reward processing to autism.Lay Summary: Discounting tasks-which experimentally measure the subjective value of different rewards-have been used with a variety of clinical populations, but are underexplored in ASD. We found that compared to neurotypical individuals, individuals with ASD showed diminished subjective value for future rewards (compared to immediate rewards) and rewards for others (compared to rewards for self). This finding has implications for understanding perspective taking, reward processing, and social closeness in ASD.

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“…All these results suggest that the worsening of social interaction deficits associated with clinical ADHD in children with ASD might be related to the speech processing network in the left SFG. Furthermore, all the evidence supports the importance of the frontal lobe in social processing and social networks [Casartelli & Molteni, ; Clements et al, ; Greimel et al, ; Kana et al, ], which are affected by ADHD comorbidities in children with ASD. However, more research is required to enable the modeling of these systems.…”

Section: Discussionmentioning

confidence: 81%

Effects of the Co‐occurrence of Anxiety and Attention‐Deficit/Hyperactivity Disorder on Intrinsic Functional Network Centrality among Children with Autism Spectrum Disorder

et al. 2019

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Children with autism spectrum disorder (ASD) present with a high co‐occurrence of anxiety and attention‐deficit/hyperactivity disorder (ADHD). However, it remains unclear how the co‐occurrence of anxiety and ADHD in children with ASD alters whole‐brain functional networks. Here, we aimed to examine anxiety‐ and ADHD‐related brain network centrality in children with ASD separately and their relationships with ASD symptoms. Clinical anxiety and ADHD levels in children with ASD, aged 6–13 years old, were assessed. Participants were categorized into four groups: ASD only (n = 28), ASD + anxiety (n = 19), ASD + ADHD (n = 25), and ASD + both anxiety and ADHD (n = 28). Subsequently, we compared voxel‐wise network degree centrality (DC) among the four groups. We found that: (a) compared with ASD only, children with ASD + anxiety showed higher DC in the left middle temporal gyrus, right lingual gyrus, and left cuneus, and lower DC in the right precuneus; (b) children with ASD + ADHD presented higher DC in the right calcarine and left superior frontal gyrus (SFG) compared with ASD only; (c) children with ASD + both displayed higher DC in the right calcarine and lower centrality in the right middle occipital gyrus compared with ASD only; and (d) across all children with ASD, there was a positive correlation between DC of the right calcarine with nonverbal behavior scores, and DC of the left SFG was negatively correlated with social scores. Our findings suggest that the right calcarine, left SFG, and default mode network nodes play important roles in the co‐occurrence of anxiety and ADHD among children with ASD. Autism Res 2019, 12: 1057–1068. © 2019 International Society for Autism Research, Wiley Periodicals, Inc. Lay Summary The co‐occurrence of anxiety and attention‐deficit/hyperactivity disorder (ADHD) has been shown to influence the brain function of children with ASD. In order to gain a better understanding of this, the present study compared degree centrality, the amount of effective brain functional connectivity that reflects the characteristics of brain networks, among four groups: ASD only, ASD + anxiety, ASD + ADHD, and ASD + both anxiety and ADHD. We found that some areas located in the language processing network and primary visual cortex were associated with the co‐occurrence of ADHD, and some other areas located in the default mode network were associated with the co‐occurrence of both anxiety and ADHD. These findings provide more knowledge about the neural basis underlying behavioral changes related to the co‐occurrence of anxiety and ADHD in children with ASD.

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Evaluation of the Social Motivation Hypothesis of Autism

Cited by 228 publications

References 71 publications

Gray matter covariations and core symptoms of autism. The EU-AIMS Longitudinal European Autism Project

Gray matter covariations and core symptoms of autism. The EU-AIMS Longitudinal European Autism Project

Social and delay discounting in autism spectrum disorder

Effects of the Co‐occurrence of Anxiety and Attention‐Deficit/Hyperactivity Disorder on Intrinsic Functional Network Centrality among Children with Autism Spectrum Disorder

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