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Mentalizing and motivation neural function during social interactions in autism spectrum disorders.

ABSTRACT: Autism Spectrum Disorders (ASDs) are characterized by core deficits in social functions. Two theories have been suggested to explain these deficits: mind-blindness theory posits impaired mentalizing processes (i.e. decreased ability for establishing a representation of others' state of mind), while social motivation theory proposes that diminished reward value for social information leads to reduced social attention, social interactions, and social learning. Mentalizing and motivation are integral to typical social interactions, and neuroimaging evidence points to independent brain networks that support these processes in healthy individuals. However, the simultaneous function of these networks has not been explored in individuals with ASDs. We used a social, interactive fMRI task, the Domino game, to explore mentalizing- and motivation-related brain activation during a well-defined interval where participants respond to rewards or punishments (i.e. motivation) and concurrently process information about their opponent's potential next actions (i.e. mentalizing). Thirteen individuals with high-functioning ASDs, ages 12-24, and 14 healthy controls played fMRI Domino games against a computer-opponent and separately, what they were led to believe was a human-opponent. Results showed that while individuals with ASDs understood the game rules and played similarly to controls, they showed diminished neural activity during the human-opponent runs only (i.e. in a social context) in bilateral middle temporal gyrus (MTG) during mentalizing and right Nucleus Accumbens (NAcc) during reward-related motivation (Pcluster < 0.05 FWE). Importantly, deficits were not observed in these areas when playing against a computer-opponent or in areas related to motor and visual processes. These results demonstrate that while MTG and NAcc, which are critical structures in the mentalizing and motivation networks, respectively, activate normally in a non-social context, they fail to respond in an otherwise identical social context in ASD compared to controls. We discuss implications to both the mind-blindness and social motivation theories of ASD and the importance of social context in research and treatment protocols.

SUBMITTER: Assaf M

PROVIDER: S-EPMC3815022 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Mentalizing and motivation neural function during social interactions in autism spectrum disorders.

Assaf Michal M Hyatt Christopher J CJ Wong Christina G CG Johnson Matthew R MR Schultz Robert T RT Hendler Talma T Pearlson Godfrey D GD

NeuroImage. Clinical 20130919

Autism Spectrum Disorders (ASDs) are characterized by core deficits in social functions. Two theories have been suggested to explain these deficits: mind-blindness theory posits impaired mentalizing processes (i.e. decreased ability for establishing a representation of others' state of mind), while social motivation theory proposes that diminished reward value for social information leads to reduced social attention, social interactions, and social learning. Mentalizing and motivation are integr ...[more]

PMID: 24273716

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Project description:Background:Recognition of symptoms of Social anxiety (SA) may be difficult among individuals with Autism Spectrum Disorders (ASD) because of overlap between social anxiety and autistic symptomatology. The main aim of our study was thus to explore the association between symptoms of social anxiety and clinical characteristics of ASD in order to identify individuals experiencing concomitant ASD and social anxiety disorder. We also described the prevalence of SA in a sample of children and adolescents with ASD. Method:79 children and adolescents with ASD (with and without intellectual disability) and 28-matched control participants were recruited in two French Expert Centers for ASD, coordinated by the Fundation FondaMental. Psychiatric comorbidities, anxiety disorders and depression were screened with standard tools (Liebowitz social anxiety scale, Hamilton Depression and Anxiety Rating Scale) and correlated to autistic features and social skills assessed with the social responsiveness scale 2 (SRS-2) and the repetitive behavior scale (RBS-R). We performed bivariate analysis between the social anxiety level and the scores measured with different clinical scales. We then adjusted the observed relationships with the alterations of SRS-2 and RBS-R scores. Results:After adjustment, the level of social anxiety appeared as significantly associated with alterations in social reciprocity and particularly with the SRS-2 "social communication" and "social motivation" sub-scores, but not with RBS-R score. Conclusions:We confirm previous reports showing that individuals with ASD are at high risk for specific anxiety disorders. In particular, high levels of impairments in social motivation and social communication (SRS-2) are indicative of comorbid disorders namely, social anxiety and ASD. Our findings clearly inform diagnostic assessment in ASD and stress the need to take comorbid anxiety disorders into consideration to improve treatment of ASD. To further clarify the impact of social anxiety on social competences and socio-adaptive handicap, longitudinal studies and cluster analysis will be needed in the future.

Project description:ContextImpaired social cognition is a cardinal feature of Autism Spectrum Disorders (ASD) and Schizophrenia (SZ). However, the functional neuroanatomy of social cognition in either disorder remains unclear due to variability in primary literature. Additionally, it is not known whether deficits in ASD and SZ arise from similar or disease-specific disruption of the social cognition network.ObjectiveTo identify regions most robustly implicated in social cognition processing in SZ and ASD.Data sourcesSystematic review of English language articles using MEDLINE (1995-2010) and reference lists.Study selectionStudies were required to use fMRI to compare ASD or SZ subjects to a matched healthy control group, provide coordinates in standard stereotactic space, and employ standardized facial emotion recognition (FER) or theory of mind (TOM) paradigms.Data extractionActivation foci from studies meeting inclusion criteria (n = 33) were subjected to a quantitative voxel-based meta-analysis using activation likelihood estimation, and encompassed 146 subjects with ASD, 336 SZ patients and 492 healthy controls.ResultsBoth SZ and ASD showed medial prefrontal hypoactivation, which was more pronounced in ASD, while ventrolateral prefrontal dysfunction was associated mostly with SZ. Amygdala hypoactivation was observed in SZ patients during FER and in ASD during more complex ToM tasks. Both disorders were associated with hypoactivation within the Superior Temporal Sulcus (STS) during ToM tasks, but activation in these regions was increased in ASD during affect processing. Disease-specific differences were noted in somatosensory engagement, which was increased in SZ and decreased in ASD. Reduced thalamic activation was uniquely seen in SZ.ConclusionsReduced frontolimbic and STS engagement emerged as a shared feature of social cognition deficits in SZ and ASD. However, there were disease- and stimulus-specific differences. These findings may aid future studies on SZ and ASD and facilitate the formulation of new hypotheses regarding their pathophysiology.

Project description:BackgroundAutism spectrum disorder (ASD) is a neurodevelopmental condition with key deficits in social functioning. It is widely assumed that the biological underpinnings of social impairment are neurofunctional alterations in the "social brain," a neural circuitry involved in inferring the mental state of a social partner. However, previous evidence comes from small-scale studies and findings have been mixed. We therefore carried out the to-date largest study on neural correlates of mentalizing in ASD.MethodsAs part of the Longitudinal European Autism Project, we performed functional magnetic resonance imaging at six European sites in a large, well-powered, and deeply phenotyped sample of individuals with ASD (N = 205) and typically developing (TD) individuals (N = 189) aged 6 to 30 years. We presented an animated shapes task to assess and comprehensively characterize social brain activation during mentalizing. We tested for effects of age, diagnosis, and their association with symptom measures, including a continuous measure of autistic traits.ResultsWe observed robust effects of task. Within the ASD sample, autistic traits were moderately associated with functional activation in one of the key regions of the social brain, the dorsomedial prefrontal cortex. However, there were no significant effects of diagnosis on task performance and no effects of age and diagnosis on social brain responses. Besides a lack of mean group differences, our data provide no evidence for meaningful differences in the distribution of brain response measures. Extensive control analyses suggest that the lack of case-control differences was not due to a variety of potential confounders.ConclusionsContrary to prior reports, this large-scale study does not support the assumption that altered social brain activation during mentalizing forms a common neural marker of ASD, at least with the paradigm we employed. Yet, autistic individuals show socio-behavioral deficits. Our work therefore highlights the need to interrogate social brain function with other brain measures, such as connectivity and network-based approaches, using other paradigms, or applying complementary analysis approaches to assess individual differences in this heterogeneous condition.

Dataset Information

Mentalizing and motivation neural function during social interactions in autism spectrum disorders.

Publications

Mentalizing and motivation neural function during social interactions in autism spectrum disorders.

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