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      Young adolescents with autism show abnormal joint attention network: A gaze contingent fMRI study

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          Abstract

          Behavioral research has revealed deficits in the development of joint attention (JA) as one of the earliest signs of autism. While the neural basis of JA has been studied predominantly in adults, we recently demonstrated a protracted development of the brain networks supporting JA in typically developing children and adolescents. The present eye-tracking/fMRI study now extends these findings to adolescents with autism. Our results show that in adolescents with autism JA is subserved by abnormal activation patterns in brain areas related to social cognition abnormalities which are at the core of ASD including the STS and TPJ, despite behavioral maturation with no behavioral differences. Furthermore, in the autism group we observed increased neural activity in a network of social and emotional processing areas during interactions with their mother. Moreover, data indicated that less severely affected individuals with autism showed higher frontal activation associated with self-initiated interactions. Taken together, this study provides first-time data of JA in children/adolescents with autism incorporating the interactive character of JA, its reciprocity and motivational aspects. The observed functional differences in adolescents ASD suggest that persistent developmental differences in the neural processes underlying JA contribute to social interaction difficulties in ASD.

          Highlights

          • Gaze-contingent fMRI task to study joint attention in a developmental sample with autism

          • JA in the autism group elicited abnormal activation in social cognition related areas.

          • The interaction partner's familiarity modulated brain activity in the autism group.

          • In the autism group frontal activation is related to the severity of communication deficits.

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          Most cited references70

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          Assignment of functional activations to probabilistic cytoarchitectonic areas revisited.

          Probabilistic cytoarchitectonic maps in standard reference space provide a powerful tool for the analysis of structure-function relationships in the human brain. While these microstructurally defined maps have already been successfully used in the analysis of somatosensory, motor or language functions, several conceptual issues in the analysis of structure-function relationships still demand further clarification. In this paper, we demonstrate the principle approaches for anatomical localisation of functional activations based on probabilistic cytoarchitectonic maps by exemplary analysis of an anterior parietal activation evoked by visual presentation of hand gestures. After consideration of the conceptual basis and implementation of volume or local maxima labelling, we comment on some potential interpretational difficulties, limitations and caveats that could be encountered. Extending and supplementing these methods, we then propose a supplementary approach for quantification of structure-function correspondences based on distribution analysis. This approach relates the cytoarchitectonic probabilities observed at a particular functionally defined location to the areal specific null distribution of probabilities across the whole brain (i.e., the full probability map). Importantly, this method avoids the need for a unique classification of voxels to a single cortical area and may increase the comparability between results obtained for different areas. Moreover, as distribution-based labelling quantifies the "central tendency" of an activation with respect to anatomical areas, it will, in combination with the established methods, allow an advanced characterisation of the anatomical substrates of functional activations. Finally, the advantages and disadvantages of the various methods are discussed, focussing on the question of which approach is most appropriate for a particular situation.
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            The role of the right temporoparietal junction in social interaction: how low-level computational processes contribute to meta-cognition.

            Accumulating evidence from cognitive neuroscience indicates that the right inferior parietal cortex, at the junction with the posterior temporal cortex, plays a critical role in various aspects of social cognition such as theory of mind and empathy. With a quantitative meta-analysis of 70 functional neuroimaging studies, the authors demonstrate that this area is also engaged in lower-level (bottom-up) computational processes associated with the sense of agency and reorienting attention to salient stimuli. It is argued that this domain-general computational mechanism is crucial for higher level social cognitive processing.
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              Early social attention impairments in autism: social orienting, joint attention, and attention to distress.

              This study investigated social attention impairments in autism (social orienting, joint attention, and attention to another's distress) and their relations to language ability. Three- to four-year-old children with autism spectrum disorder (ASD; n = 72), 3- to 4-year-old developmentally delayed children (n = 34), and 12- to 46-month-old typically developing children (n = 39), matched on mental age, were compared on measures of social orienting, joint attention, and attention to another's distress. Children with autism performed significantly worse than the comparison groups in all of these domains. Combined impairments in joint attention and social orienting were found to best distinguish young children with ASD from those without ASD. Structural equation modeling indicated that joint attention was the best predictor of concurrent language ability. Social orienting and attention to distress were indirectly related to language through their relations with joint attention. These results help to clarify the nature of social attention impairments in autism, offer clues to developmental mechanisms, and suggest targets for early intervention. ((c) 2004 APA, all rights reserved)
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                Author and article information

                Contributors
                Journal
                Neuroimage Clin
                Neuroimage Clin
                NeuroImage : Clinical
                Elsevier
                2213-1582
                09 January 2017
                2017
                09 January 2017
                : 14
                : 112-121
                Affiliations
                [a ]Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, Germany
                [b ]Translational Brain Research in Psychiatry and Neurology, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital Aachen, Germany
                [c ]Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Jülich Research Center, Germany
                [d ]Department of Psychiatry, University Hospital Cologne, Germany
                [e ]Max Planck Institute of Psychiatry, Munich, Germany
                [f ]Department of Humanities, Social and Political Science, ETH Zurich, Switzerland
                [g ]Department of Neurology, University Hospital Cologne, Germany
                [h ]Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, Germany
                Author notes
                [* ]Corresponding author at: Neuenhofer Weg 21, 52074 Aachen, Germany.Neuenhofer Weg 21Aachen52074Germany eoberwelland@ 123456ukaachen.de
                Article
                S2213-1582(17)30006-2
                10.1016/j.nicl.2017.01.006
                5279905
                28180069
                ae6cc6dc-18e3-4894-8557-dc3c9db02f8e
                © 2017 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 9 November 2016
                : 22 December 2016
                : 7 January 2017
                Categories
                Regular Article

                social interaction,eye-tracking,familiarity,functional magnetic resonance imaging,temporoparietal junction,superior temporal sulcus

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