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      Reduced engagement with social stimuli in 6-month-old infants with later autism spectrum disorder: a longitudinal prospective study of infants at high familial risk

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          Abstract

          Background

          Autism spectrum disorder (ASD) is a neurodevelopmental disorder that affects more than 1 % of the population and close to 20 % of prospectively studied infants with an older sibling with ASD. Although significant progress has been made in characterizing the emergence of behavioral symptoms of ASD, far less is known about the underlying disruptions to early learning. Recent models suggest that core aspects of the causal path to ASD may only be apparent in early infancy. Here, we investigated social attention in 6- and 12-month-old infants who did and did not meet criteria for ASD at 24 months using both cognitive and electrophysiological methods. We hypothesized that a reduction in attention engagement to faces would be associated with later ASD.

          Methods

          In a prospective longitudinal design, we used measures of both visual attention (habituation) and brain function (event-related potentials to faces and objects) at 6 and 12 months and investigated the relationship to ASD outcome at 24 months.

          Results

          High-risk infants who met criteria for ASD at 24 months showed shorter epochs of visual attention, faster but less prolonged neural activation to faces, and delayed sensitization responses (increases in looking) to faces at 6 months; these differences were less apparent at 12 months. These findings are consistent with disrupted engagement of sustained attention to social stimuli.

          Conclusions

          These findings suggest that there may be fundamental early disruptions to attention engagement that may have cascading consequences for later social functioning.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s11689-016-9139-8) contains supplementary material, which is available to authorized users.

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          Most cited references72

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          Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies.

          This article reviews behavioral and electrophysiological studies of face processing and discusses hypotheses for understanding the nature of face processing impairments in autism. Based on results of behavioral studies, this study demonstrates that individuals with autism have impaired face discrimination and recognition and use atypical strategies for processing faces characterized by reduced attention to the eyes and piecemeal rather than configural strategies. Based on results of electrophysiological studies, this article concludes that face processing impairments are present early in autism, by 3 years of age. Such studies have detected abnormalities in both early (N170 reflecting structural encoding) and late (NC reflecting recognition memory) stages of face processing. Event-related potential studies of young children and adults with autism have found slower speed of processing of faces, a failure to show the expected speed advantage of processing faces versus nonface stimuli, and atypical scalp topography suggesting abnormal cortical specialization for face processing. Other electrophysiological studies have suggested that autism is associated with early and late stage processing impairments of facial expressions of emotion (fear) and decreased perceptual binding as reflected in reduced gamma during face processing. This article describes two types of hypotheses-cognitive/perceptual and motivational/affective--that offer frameworks for understanding the nature of face processing impairments in autism. This article discusses implications for intervention.
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            Autism from 2 to 9 years of age.

            Autism represents an unusual pattern of development beginning in the infant and toddler years. To examine the stability of autism spectrum diagnoses made at ages 2 through 9 years and identify features that predicted later diagnosis. Prospective study of diagnostic classifications from standardized instruments including a parent interview (Autism Diagnostic Interview-Revised [ADI-R]), an observational scale (Pre-Linguistic Autism Diagnostic Observation Schedule/Autism Diagnostic Observation Schedule [ADOS]), and independent clinical diagnoses made at ages 2 and 9 years compared with a clinical research team's criterion standard diagnoses. Three inception cohorts: consecutive referrals for autism assessment to (1) state-funded community autism centers, (2) a private university autism clinic, and (3) case controls with developmental delay from community clinics. At 2 years of age, 192 autism referrals and 22 developmentally delayed case controls; 172 children seen at 9 years of age. Consensus best-estimate diagnoses at 9 years of age. Percentage agreement between best-estimate diagnoses at 2 and 9 years of age was 67, with a weighted kappa of 0.72. Diagnostic change was primarily accounted for by movement from pervasive developmental disorder not otherwise specified to autism. Each measure at age 2 years was strongly prognostic for autism at age 9 years, with odds ratios of 6.6 for parent interview, 6.8 for observation, and 12.8 for clinical judgment. Once verbal IQ (P = .001) was taken into account at age 2 years, the ADI-R repetitive domain (P = .02) and the ADOS social (P = .05) and repetitive domains (P = .005) significantly predicted autism at age 9 years. Diagnostic stability at age 9 years was very high for autism at age 2 years and less strong for pervasive developmental disorder not otherwise specified. Judgment of experienced clinicians, trained on standard instruments, consistently added to information available from parent interview and standardized observation.
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              Differences in white matter fiber tract development present from 6 to 24 months in infants with autism.

              Evidence from prospective studies of high-risk infants suggests that early symptoms of autism usually emerge late in the first or early in the second year of life after a period of relatively typical development. The authors prospectively examined white matter fiber tract organization from 6 to 24 months in high-risk infants who developed autism spectrum disorders (ASDs) by 24 months. The participants were 92 high-risk infant siblings from an ongoing imaging study of autism. All participants had diffusion tensor imaging at 6 months and behavioral assessments at 24 months; a majority contributed additional imaging data at 12 and/or 24 months. At 24 months, 28 infants met criteria for ASDs and 64 infants did not. Microstructural properties of white matter fiber tracts reported to be associated with ASDs or related behaviors were characterized by fractional anisotropy and radial and axial diffusivity. The fractional anisotropy trajectories for 12 of 15 fiber tracts differed significantly between the infants who developed ASDs and those who did not. Development for most fiber tracts in the infants with ASDs was characterized by higher fractional anisotropy values at 6 months followed by slower change over time relative to infants without ASDs. Thus, by 24 months of age, those with ASDs had lower values. These results suggest that aberrant development of white matter pathways may precede the manifestation of autistic symptoms in the first year of life. Longitudinal data are critical to characterizing the dynamic age-related brain and behavior changes underlying this neurodevelopmental disorder.
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                Author and article information

                Contributors
                e.jones@bbk.ac.uk
                kmv486@gmail.com
                rkinc78@uw.edu
                rlowy@uw.edu
                Karen.Barnes@seattlechildrens.org
                estesa@u.washington.edu
                geraldine.dawson@duke.edu
                sjwebb@uw.edu
                Journal
                J Neurodev Disord
                J Neurodev Disord
                Journal of Neurodevelopmental Disorders
                BioMed Central (London )
                1866-1947
                1866-1955
                15 March 2016
                15 March 2016
                2016
                : 8
                : 7
                Affiliations
                [ ]Centre for Brain and Cognitive Development, Birkbeck College, University of London, London, UK
                [ ]Center on Human Development and Disability, University of Washington, Seattle, WA USA
                [ ]Center for Child Health, Behavior and Development, Seattle Children’s Hospital, Seattle, WA USA
                [ ]Department of Speech and Hearing Sciences, University of Washington, Seattle, WA USA
                [ ]Department of Psychiatry and Behavioral Sciences, Duke University, Durham, NC USA
                [ ]Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, WA USA
                Article
                9139
                10.1186/s11689-016-9139-8
                4791854
                26981158
                236a1c2f-7fb0-4bf1-9c6d-4d916f62d978
                © Jones et al. 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 9 March 2015
                : 17 February 2016
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Neurosciences
                asd,habituation,event-related potential,social attention,social information processing

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