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      Social Attention in Autism: Neural Sensitivity to Speech Over Background Noise Predicts Encoding of Social Information

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          Abstract

          Autism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by lack of attention to social cues in the environment, including speech. Hypersensitivity to sensory stimuli, such as loud noises, is also extremely common in youth with ASD. While a link between sensory hypersensitivity and impaired social functioning has been hypothesized, very little is known about the neural mechanisms whereby exposure to distracting sensory stimuli may interfere with the ability to direct attention to socially-relevant information. Here, we used functional magnetic resonance imaging (fMRI) in youth with and without ASD (N=54, age range 8–18 years) to ( 1) examine brain responses during presentation of brief social interactions (i.e., two-people conversations) shrouded in ecologically-valid environmental noises, and ( 2) assess how brain activity during encoding might relate to later accuracy in identifying what was heard. During exposure to conversation-in-noise ( vs. conversation or noise alone), both neurotypical youth and youth with ASD showed robust activation of canonical language networks. However, the extent to which youth with ASD activated temporal language regions, including voice-selective cortex (i.e., posterior superior temporal sulcus), predicted later discriminative accuracy in identifying what was heard. Further, relative to neurotypical youth, ASD youth showed significantly greater activity in left-hemisphere speech-processing cortex (i.e., angular gyrus) while listening to conversation-in-noise ( vs. conversation or noise alone). Notably, in youth with ASD, increased activity in this region was associated with higher social motivation and better social cognition measures. This heightened activity in voice-selective/speech-processing regions may serve as a compensatory mechanism allowing youth with ASD to hone in on the conversations they heard in the context of non-social distracting stimuli. These findings further suggest that focusing on social and non-social stimuli simultaneously may be more challenging for youth with ASD requiring the recruitment of additional neural resources to encode socially-relevant information.

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          Sensory processing in autism: a review of neurophysiologic findings.

          Atypical sensory-based behaviors are a ubiquitous feature of autism spectrum disorders (ASDs). In this article, we review the neural underpinnings of sensory processing in autism by reviewing the literature on neurophysiological responses to auditory, tactile, and visual stimuli in autistic individuals. We review studies of unimodal sensory processing and multisensory integration that use a variety of neuroimaging techniques, including electroencephalography (EEG), magnetoencephalography (MEG), and functional MRI. We then explore the impact of covert and overt attention on sensory processing. With additional characterization, neurophysiologic profiles of sensory processing in ASD may serve as valuable biomarkers for diagnosis and monitoring of therapeutic interventions for autism and reveal potential strategies and target brain regions for therapeutic interventions.
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            Topographic mapping of a hierarchy of temporal receptive windows using a narrated story.

            Real-life activities, such as watching a movie or engaging in conversation, unfold over many minutes. In the course of such activities, the brain has to integrate information over multiple time scales. We recently proposed that the brain uses similar strategies for integrating information across space and over time. Drawing a parallel with spatial receptive fields, we defined the temporal receptive window (TRW) of a cortical microcircuit as the length of time before a response during which sensory information may affect that response. Our previous findings in the visual system are consistent with the hypothesis that TRWs become larger when moving from low-level sensory to high-level perceptual and cognitive areas. In this study, we mapped TRWs in auditory and language areas by measuring fMRI activity in subjects listening to a real-life story scrambled at the time scales of words, sentences, and paragraphs. Our results revealed a hierarchical topography of TRWs. In early auditory cortices (A1+), brain responses were driven mainly by the momentary incoming input and were similarly reliable across all scrambling conditions. In areas with an intermediate TRW, coherent information at the sentence time scale or longer was necessary to evoke reliable responses. At the apex of the TRW hierarchy, we found parietal and frontal areas that responded reliably only when intact paragraphs were heard in a meaningful sequence. These results suggest that the time scale of processing is a functional property that may provide a general organizing principle for the human cerebral cortex.
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              Disrupted neural synchronization in toddlers with autism.

              Autism is often described as a disorder of neural synchronization. However, it is unknown how early in development synchronization abnormalities emerge and whether they are related to the development of early autistic behavioral symptoms. Here, we show that disrupted synchronization is evident in the spontaneous cortical activity of naturally sleeping toddlers with autism, but not in toddlers with language delay or typical development. Toddlers with autism exhibited significantly weaker interhemispheric synchronization (i.e., weak "functional connectivity" across the two hemispheres) in putative language areas. The strength of synchronization was positively correlated with verbal ability and negatively correlated with autism severity, and it enabled identification of the majority of autistic toddlers (72%) with high accuracy (84%). Disrupted cortical synchronization, therefore, appears to be a notable characteristic of autism neurophysiology that is evident at very early stages of autism development. Copyright © 2011 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Psychiatry
                Front Psychiatry
                Front. Psychiatry
                Frontiers in Psychiatry
                Frontiers Media S.A.
                1664-0640
                24 April 2020
                2020
                : 11
                : 343
                Affiliations
                [1] 1 Ahmanson-Lovelace Brain Mapping Center, University of California, Los Angeles , Los Angeles, CA, United States
                [2] 2 Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles , Los Angeles, CA, United States
                [3] 3 Staglin IMHRO Center for Cognitive Neuroscience, University of California, Los Angeles , Los Angeles, CA, United States
                Author notes

                Edited by: Kevin A. Pelphrey, University of Virginia, United States

                Reviewed by: Jeroen M. van Baar, Brown University, United States; Derek J. Dean, Vanderbilt University, United States

                *Correspondence: Mirella Dapretto, mirella@ 123456ucla.edu

                This article was submitted to Social Cognition, a section of the journal Frontiers in Psychiatry

                Article
                10.3389/fpsyt.2020.00343
                7194032
                b736b628-459a-4182-ab91-bb24906e2496
                Copyright © 2020 Hernandez, Green, Lawrence, Inada, Liu, Bookheimer and Dapretto

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 03 December 2019
                : 06 April 2020
                Page count
                Figures: 4, Tables: 5, Equations: 0, References: 57, Pages: 14, Words: 8821
                Funding
                Funded by: National Institute of Mental Health 10.13039/100000025
                Award ID: R01MH100028, K08 MH112871, F32 MH105167, F31 MH110140
                Funded by: Simons Foundation Autism Research Initiative 10.13039/100014370
                Award ID: 345389
                Funded by: National Institute of Neurological Disorders and Stroke 10.13039/100000065
                Award ID: F99 NS105206, T32 NS048004
                Funded by: National Institute of Child Health and Human Development 10.13039/100000071
                Award ID: F31 HD088102
                Funded by: National Center for Research Resources 10.13039/100000097
                Award ID: RR12169, RR13642, RR00865
                Categories
                Psychiatry
                Original Research

                Clinical Psychology & Psychiatry
                speech,autism,voice-selective,attention,conversation,noise,aversive,sensory
                Clinical Psychology & Psychiatry
                speech, autism, voice-selective, attention, conversation, noise, aversive, sensory

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