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      Reduced Volume of the Arcuate Fasciculus in Adults with High-Functioning Autism Spectrum Conditions

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          Abstract

          Atypical language is a fundamental feature of autism spectrum conditions (ASC), but few studies have examined the structural integrity of the arcuate fasciculus, the major white matter tract connecting frontal and temporal language regions, which is usually implicated as the main transfer route used in processing linguistic information by the brain. Abnormalities in the arcuate have been reported in young children with ASC, mostly in low-functioning or non-verbal individuals, but little is known regarding the structural properties of the arcuate in adults with ASC or, in particular, in individuals with ASC who have intact language, such as those with high-functioning autism or Asperger syndrome. We used probabilistic tractography of diffusion-weighted imaging to isolate and scrutinize the arcuate in a mixed-gender sample of 18 high-functioning adults with ASC (17 Asperger syndrome) and 14 age- and IQ-matched typically developing controls. Arcuate volume was significantly reduced bilaterally with clearest differences in the right hemisphere. This finding remained significant in an analysis of all male participants alone. Volumetric reduction in the arcuate was significantly correlated with the severity of autistic symptoms as measured by the Autism-Spectrum Quotient. These data reveal that structural differences are present even in high-functioning adults with ASC, who presented with no clinically manifest language deficits and had no reported developmental language delay. Arcuate structural integrity may be useful as an index of ASC severity and thus as a predictor and biomarker for ASC. Implications for future research are discussed.

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          Perisylvian language networks of the human brain.

          Early anatomically based models of language consisted of an arcuate tract connecting Broca's speech and Wernicke's comprehension centers; a lesion of the tract resulted in conduction aphasia. However, the heterogeneous clinical presentations of conduction aphasia suggest a greater complexity of perisylvian anatomical connections than allowed for in the classical anatomical model. This article re-explores perisylvian language connectivity using in vivo diffusion tensor magnetic resonance imaging tractography. Diffusion tensor magnetic resonance imaging data from 11 right-handed healthy male subjects were averaged, and the arcuate fasciculus of the left hemisphere reconstructed from this data using an interactive dissection technique. Beyond the classical arcuate pathway connecting Broca's and Wernicke's areas directly, we show a previously undescribed, indirect pathway passing through inferior parietal cortex. The indirect pathway runs parallel and lateral to the classical arcuate fasciculus and is composed of an anterior segment connecting Broca's territory with the inferior parietal lobe and a posterior segment connecting the inferior parietal lobe to Wernicke's territory. This model of two parallel pathways helps explain the diverse clinical presentations of conduction aphasia. The anatomical findings are also relevant to the evolution of language, provide a framework for Lichtheim's symptom-based neurological model of aphasia, and constrain, anatomically, contemporary connectionist accounts of language.
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            Ventral and dorsal pathways for language.

            Built on an analogy between the visual and auditory systems, the following dual stream model for language processing was suggested recently: a dorsal stream is involved in mapping sound to articulation, and a ventral stream in mapping sound to meaning. The goal of the study presented here was to test the neuroanatomical basis of this model. Combining functional magnetic resonance imaging (fMRI) with a novel diffusion tensor imaging (DTI)-based tractography method we were able to identify the most probable anatomical pathways connecting brain regions activated during two prototypical language tasks. Sublexical repetition of speech is subserved by a dorsal pathway, connecting the superior temporal lobe and premotor cortices in the frontal lobe via the arcuate and superior longitudinal fascicle. In contrast, higher-level language comprehension is mediated by a ventral pathway connecting the middle temporal lobe and the ventrolateral prefrontal cortex via the extreme capsule. Thus, according to our findings, the function of the dorsal route, traditionally considered to be the major language pathway, is mainly restricted to sensory-motor mapping of sound to articulation, whereas linguistic processing of sound to meaning requires temporofrontal interaction transmitted via the ventral route.
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              Autism spectrum disorders: developmental disconnection syndromes.

              Autism is a common and heterogeneous childhood neurodevelopmental disorder. Analogous to broad syndromes such as mental retardation, autism has many etiologies and should be considered not as a single disorder but, rather, as 'the autisms'. However, recent genetic findings, coupled with emerging anatomical and functional imaging studies, suggest a potential unifying model in which higher-order association areas of the brain that normally connect to the frontal lobe are partially disconnected during development. This concept of developmental disconnection can accommodate the specific neurobehavioral features that are observed in autism, their emergence during development, and the heterogeneity of autism etiology, behaviors and cognition.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                12 May 2016
                2016
                : 10
                : 214
                Affiliations
                [1] 1Department of Psychology, Bournemouth University Dorset, UK
                [2] 2Medical Research Council Cognition and Brain Sciences Unit Cambridge, UK
                [3] 3Brain Mapping Unit, Department of Psychiatry, University of Cambridge Cambridge, UK
                [4] 4Autism Research Centre, Department of Psychiatry, University of Cambridge Cambridge, UK
                [5] 5Cambridge Lifespan Asperger Syndrome Service Clinic, Cambridgeshire and Peterborough National Health Service Foundation Trust Cambridge, UK
                [6] 6Center of Functionally Integrative Neuroscience (CFIN), Department of Clinical Medicine, Aarhus University Aarhus, Denmark
                [7] 7Centre for Cognition and Decision Making, National Research University Higher School of Economics Moscow, Russia
                [8] 8Brain Language Laboratory, Freie Universität Berlin Berlin, Germany
                [9] 9Department of Psychiatry, Charité–Universitätsmedizin Berlin Berlin, Germany
                Author notes

                Edited by: Joshua Oon Soo Goh, National Taiwan University, Taiwan

                Reviewed by: Stephanie Ameis, University of Toronto, Canada; Hsiang-Yuan Lin, National Taiwan University Hospital and College of Medicine, Taiwan

                *Correspondence: Rachel L. Moseley, rmoseley@ 123456bournemouth.ac.uk
                Article
                10.3389/fnhum.2016.00214
                4867673
                27242478
                b6766238-f3b9-421a-98ec-9d9336ede73e
                Copyright © 2016 Moseley, Correia, Baron-Cohen, Shtyrov, Pulvermüller and Mohr.

                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) or licensor 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
                : 28 October 2015
                : 25 April 2016
                Page count
                Figures: 4, Tables: 2, Equations: 0, References: 129, Pages: 15, Words: 0
                Funding
                Funded by: Medical Research Council 10.13039/501100000265
                Award ID: MC_US_a060_0034, MC_A060_5PQ90
                Categories
                Neuroscience
                Original Research

                Neurosciences
                autism,asperger syndrome,diffusion-weighted imaging (dwi),arcuate fasciculus,language

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