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Age Group Differences in Executive Network Functional Connectivity and Relationships with Social Behavior in Men with Autism Spectrum Disorder.

ABSTRACT: Background:Research suggests adults with autism spectrum disorder (ASD) may use executive functions to compensate for social difficulties. Given hallmark age-related declines in executive functioning and the executive brain network in normal aging, there is concern that older adults with ASD may experience further declines in social functioning as they age. In a male-only sample, we hypothesized: 1) older adults with ASD would demonstrate greater ASD-related social behavior than young adults with ASD, 2) adults with ASD would demonstrate a greater age group reduction in connectivity of the executive brain network than neurotypical (NT) adults, and 3) that behavioral and neural mechanisms of executive functioning would predict ASD-related social difficulties in adults with ASD. Methods:Participants were a cross-sectional sample of non-intellectually disabled young (ages 18-25) and middle-aged (ages 40-70) adult men with ASD and NT development (young adult ASD: n=24; middle-age ASD: n=25; young adult NT: n=15; middle-age NT: n=21). We assessed ASD-related social behavior via the self-report Social Responsiveness Scale-2 (SRS-2) Total Score, with exploratory analyses of the Social Cognition Subscale. We assessed neural executive function via connectivity of the resting-state executive network (EN) as measured by independent component analysis. Correlations were investigated between SRS-2 Total Scores (with exploratory analyses of the Social Cognition Subscale), EN functional connectivity of the dorsolateral prefrontal cortex (dlPFC), and a behavioral measure of executive function, Tower of London (ToL) Total Moves. Results:We did not confirm a significant age group difference for adults with ASD on the SRS-2 Total Score; however, exploratory analysis revealed middle-age men with ASD had higher scores on the SRS-2 Social Cognition Subscale than young adult men with ASD. Exacerbated age group reductions in EN functional connectivity were confirmed (left dlPFC) in men with ASD compared to NT, such that older adults with ASD demonstrated the greatest levels of hypoconnectivity. A significant correlation was confirmed between dlPFC connectivity and the SRS-2 Total Score in middle-age men with ASD, but not young adult men with ASD. Furthermore, exploratory analysis revealed a significant correlation with the SRS-2 Social Cognition Subscale for young and middle-aged ASD groups and ToL Total Moves. Conclusions:Our findings suggest that ASD-related difficulties in social cognition and EN hypoconnectivity may get worse with age in men with ASD and is related to executive functioning. Further, exacerbated EN hypoconnectivity associated with older age in ASD may be a mechanism of increased ASD-related social cognition difficulties in older adults with ASD. Given the cross-sectional nature of this sample, longitudinal replication is needed.

SUBMITTER: Walsh MJM

PROVIDER: S-EPMC7220036 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Age Group Differences in Executive Network Functional Connectivity and Relationships with Social Behavior in Men with Autism Spectrum Disorder.

Walsh Melissa J M MJM Baxter Leslie C LC Smith Christopher J CJ Braden B Blair BB

Research in autism spectrum disorders 20190330

<h4>Background</h4>Research suggests adults with autism spectrum disorder (ASD) may use executive functions to compensate for social difficulties. Given hallmark age-related declines in executive functioning and the executive brain network in normal aging, there is concern that older adults with ASD may experience further declines in social functioning as they age. In a male-only sample, we hypothesized: 1) older adults with ASD would demonstrate greater ASD-related social behavior than young ad ...[more]

PMID: 32405319

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Project description:Although reduced social attention and increased nonsocial attention have been reported in individuals with autism spectrum disorder (ASD), the studies have relied on predominantly male samples and have been underpowered to examine sex differences. These processes may differ for females with ASD, who have been shown to be dissimilar to males in social motivation and nonsocial features, including circumscribed interests (CI). The goal of this study was to compare social and nonsocial visual attention between males and females with ASD on a validated eye-tracking paradigm. Eighty-five school-aged (6-10 years) males and females with and without ASD completed a paired preference task of face and object stimuli (half of which related to common CI). After covarying for chronological and mental age, the presence of concurrently presented CI images reduced prioritization and attention to faces for males more than females, replicating previous findings. ASD females maintained comparable attention patterns to typically developing females, suggesting that previous findings of reduced social attention and increased attention to CI-related objects in autism may be specific to males. These findings are also inconsistent with the "extreme male brain" theory of autism. The more normative orienting and attention to social stimuli for females with ASD may indicate distinct phenotypic characteristics relative to males and possibly serve as a protective effect. Autism Res 2018, 11: 1264-1275. © 2018 International Society for Autism Research, Wiley Periodicals, Inc. LAY SUMMARY: As autism is more commonly diagnosed in males, less is known about females with autism. Two areas of interest include the interests held by individuals with autism and how socially motivated they are. We used eye tracking as a way to understand these two areas. Our data reveal that elementary school-aged females (6-10 years) with autism attended to faces comparatively to females without autism, suggesting that (1) they were more socially motivated than males with autism and (2) the images of common interests were less motivating to them.

Project description:Autism spectrum disorder (ASD) is more prevalent in males than females, but the underlying neurobiology of this sex bias remains unclear. Given its involvement in ASD, its role in sensorimotor, cognitive, and socio-affective processes, and its developmental sensitivity to sex hormones, the cerebellum is a candidate for understanding this sex difference. The current study used resting-state functional magnetic resonance imaging (fMRI) to investigate sex-dependent differences in cortico-cerebellar organization in ASD. We collected resting-state fMRI scans from 47 females (23 ASD, 24 controls) and 120 males (56 ASD, 65 controls). Using a measure of global functional connectivity (FC), we ran a linear mixed effects analysis to determine whether there was a sex-by-diagnosis interaction in resting-state FC. Subsequent seed-based analyses from the resulting clusters were run to clarify the global connectivity effects. Two clusters in the bilateral cerebellum exhibited a diagnosis-by-sex interaction in global connectivity. These cerebellar clusters further showed a pattern of interaction with regions in the cortex, including bilateral fusiform, middle occipital, middle frontal, and precentral gyri, cingulate cortex, and precuneus. Post hoc tests revealed a pattern of cortico-cerebellar hyperconnectivity in ASD females and a pattern of hypoconnectivity in ASD males. Furthermore, cortico-cerebellar FC in females more closely resembled that of control males than that of control females. These results shed light on the sex-specific pathophysiology of ASD and are indicative of potentially divergent neurodevelopmental trajectories for each sex. This sex-dependent, aberrant cerebellar connectivity in ASD might also underlie some of the motor and/or socio-affective difficulties experienced by members of this population, but the symptomatic correlate(s) of these brain findings remain unknown. Clinical Trial Registration: www.ClinicalTrials.gov, NIH Clinical Study Protocol 10-M-0027 (ZIA MH002920-09) identifier #NCT01031407.

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Age Group Differences in Executive Network Functional Connectivity and Relationships with Social Behavior in Men with Autism Spectrum Disorder.

Publications

Age Group Differences in Executive Network Functional Connectivity and Relationships with Social Behavior in Men with Autism Spectrum Disorder.

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