Dataset Information

Atypical Dynamic Functional Network Connectivity State Engagement during Social-Emotional Processing in Schizophrenia and Autism.

ABSTRACT: Autism spectrum disorder (ASD) and schizophrenia (SZ) are separate clinical entities but share deficits in social-emotional processing and static neural functional connectivity patterns. We compared patients' dynamic functional network connectivity (dFNC) state engagement with typically developed (TD) individuals during social-emotional processing after initially characterizing such dynamics in TD. Young adults diagnosed with ASD (n = 42), SZ (n = 41), or TD (n = 55) completed three functional MRI runs, viewing social-emotional videos with happy, sad, or neutral content. We examined dFNC of 53 spatially independent networks extracted using independent component analysis and applied k-means clustering to windowed dFNC matrices, identifying four unique whole-brain dFNC states. TD showed differential engagement (fractional time, mean dwell time) in three states as a function of emotion. During Happy videos, patients spent less time than TD in a happy-associated state and instead spent more time in the most weakly connected state. During Sad videos, only ASD spent more time than TD in a sad-associated state. Additionally, only ASD showed a significant relationship between dFNC measures and alexithymia and social-emotional recognition task scores, potentially indicating different neural processing of emotions in ASD and SZ. Our results highlight the importance of examining temporal whole-brain reconfiguration of FNC, indicating engagement in unique emotion-specific dFNC states.

SUBMITTER: Hyatt CJ

PROVIDER: S-EPMC9376868 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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Atypical Dynamic Functional Network Connectivity State Engagement during Social-Emotional Processing in Schizophrenia and Autism.

Hyatt Christopher J CJ Wexler Bruce E BE Pittman Brian B Nicholson Alycia A Pearlson Godfrey D GD Corbera Silvia S Bell Morris D MD Pelphrey Kevin K Calhoun Vince D VD Assaf Michal M

Cerebral cortex (New York, N.Y. : 1991) 20220801 16

Autism spectrum disorder (ASD) and schizophrenia (SZ) are separate clinical entities but share deficits in social-emotional processing and static neural functional connectivity patterns. We compared patients' dynamic functional network connectivity (dFNC) state engagement with typically developed (TD) individuals during social-emotional processing after initially characterizing such dynamics in TD. Young adults diagnosed with ASD (n = 42), SZ (n = 41), or TD (n = 55) completed three functional M ...[more]

PMID: 34875687

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Project description:BackgroundAutism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by impairments in social cognition. The biological basis of deficits in social cognition in ASD, and their difficulty in processing emotional face information in particular, remains unclear. Atypical communication within and between brain regions has been reported in ASD. Interregional phase-locking is a neurophysiological mechanism mediating communication among brain areas and is understood to support cognitive functions. In the present study we investigated interregional magnetoencephalographic phase synchronization during the perception of emotional faces in adolescents with ASD.MethodsA total of 22 adolescents with ASD (18 males, mean age =14.2 ± 1.15 years, 22 right-handed) with mild to no cognitive delay and 17 healthy controls (14 males, mean age =14.4 ± 0.33 years, 16 right-handed) performed an implicit emotional processing task requiring perception of happy, angry and neutral faces while we recorded neuromagnetic signals. The faces were presented rapidly (80 ms duration) to the left or right of a central fixation cross and participants responded to a scrambled pattern that was presented concurrently on the opposite side of the fixation point. Task-dependent interregional phase-locking was calculated among source-resolved brain regions.ResultsTask-dependent increases in interregional beta synchronization were observed. Beta-band interregional phase-locking in adolescents with ASD was reduced, relative to controls, during the perception of angry faces in a distributed network involving the right fusiform gyrus and insula. No significant group differences were found for happy or neutral faces, or other analyzed frequency ranges. Significant reductions in task-dependent beta connectivity strength, clustering and eigenvector centrality (all P <0.001) in the right insula were found in adolescents with ASD, relative to controls.ConclusionsReduced beta synchronization may reflect inadequate recruitment of task-relevant networks during emotional face processing in ASD. The right insula, specifically, was a hub of reduced functional connectivity and may play a prominent role in the inability to effectively extract emotional information from faces. These findings suggest that functional disconnection in brain networks mediating emotional processes may contribute to deficits in social cognition in this population.

Project description:Over 90% of children with Autism Spectrum Disorders (ASD) demonstrate atypical sensory behaviors. In fact, hyper- or hyporeactivity to sensory input or unusual interest in sensory aspects of the environment is now included in the DSM-5 diagnostic criteria. However, there are children with sensory processing differences who do not meet an ASD diagnosis but do show atypical sensory behaviors to the same or greater degree as ASD children. We previously demonstrated that children with Sensory Processing Disorders (SPD) have impaired white matter microstructure, and that this white matter microstructural pathology correlates with atypical sensory behavior. In this study, we use diffusion tensor imaging (DTI) fiber tractography to evaluate the structural connectivity of specific white matter tracts in boys with ASD (n = 15) and boys with SPD (n = 16), relative to typically developing children (n = 23). We define white matter tracts using probabilistic streamline tractography and assess the strength of tract connectivity using mean fractional anisotropy. Both the SPD and ASD cohorts demonstrate decreased connectivity relative to controls in parieto-occipital tracts involved in sensory perception and multisensory integration. However, the ASD group alone shows impaired connectivity, relative to controls, in temporal tracts thought to subserve social-emotional processing. In addition to these group difference analyses, we take a dimensional approach to assessing the relationship between white matter connectivity and participant function. These correlational analyses reveal significant associations of white matter connectivity with auditory processing, working memory, social skills, and inattention across our three study groups. These findings help elucidate the roles of specific neural circuits in neurodevelopmental disorders, and begin to explore the dimensional relationship between critical cognitive functions and structural connectivity across affected and unaffected children.

Project description:Schizophrenia and autism spectrum disorder (ASD) are two prevalent neurodevelopmental disorders sharing some similar genetic basis and clinical features. The extent to which they share common neural substrates remains unclear. Resting-state fMRI data were collected from 35 drug-naïve adolescent participants with first-episode schizophrenia (15.6 ± 1.8 years old) and 31 healthy controls (15.4 ± 1.6 years old). Data from 22 participants with ASD (13.1 ± 3.1 years old) and 21 healthy controls (12.9 ± 2.9 years old) were downloaded from the Autism Brain Imaging Data Exchange. Resting-state functional networks were constructed using predefined regions of interest. Multivariate pattern analysis combined with multi-task regression feature selection methods were conducted in two datasets separately. Classification between individuals with disorders and controls was achieved with high accuracy (schizophrenia dataset: accuracy = 83%; ASD dataset: accuracy = 80%). Shared atypical brain connections contributing to classification were mostly present in the default mode network (DMN) and salience network (SN). These functional connections were further related to severity of social deficits in ASD (p = 0.002). Distinct atypical connections were also more related to the DMN and SN, but showed different atypical connectivity patterns between the two disorders. These results suggest some common neural mechanisms contributing to schizophrenia and ASD, and may aid in understanding the pathology of these two neurodevelopmental disorders. Autism Res 2017, 10: 1776-1786. © 2017 International Society for Autism Research, Wiley Periodicals, Inc.Lay summaryAutism spectrum disorder (ASD) and schizophrenia are two common neurodevelopmental disorders which share several genetic and behavioral features. The present study identified common neural mechanisms contributing to ASD and schizophrenia using resting-state functional MRI data. The results may help to understand the pathology of these two neurodevelopmental disorders.

Dataset Information

Atypical Dynamic Functional Network Connectivity State Engagement during Social-Emotional Processing in Schizophrenia and Autism.

Publications

Atypical Dynamic Functional Network Connectivity State Engagement during Social-Emotional Processing in Schizophrenia and Autism.

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