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      Oxytocin increases eye contact during a real-time, naturalistic social interaction in males with and without autism

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          Abstract

          Autism spectrum conditions (autism) affect ~1% of the population and are characterized by deficits in social communication. Oxytocin has been widely reported to affect social-communicative function and its neural underpinnings. Here we report the first evidence that intranasal oxytocin administration improves a core problem that individuals with autism have in using eye contact appropriately in real-world social settings. A randomized double-blind, placebo-controlled, within-subjects design is used to examine how intranasal administration of 24 IU of oxytocin affects gaze behavior for 32 adult males with autism and 34 controls in a real-time interaction with a researcher. This interactive paradigm bypasses many of the limitations encountered with conventional static or computer-based stimuli. Eye movements are recorded using eye tracking, providing an objective measurement of looking patterns. The measure is shown to be sensitive to the reduced eye contact commonly reported in autism, with the autism group spending less time looking to the eye region of the face than controls. Oxytocin administration selectively enhanced gaze to the eyes in both the autism and control groups (transformed mean eye-fixation difference per second=0.082; 95% CI:0.025–0.14, P=0.006). Within the autism group, oxytocin has the most effect on fixation duration in individuals with impaired levels of eye contact at baseline (Cohen's d=0.86). These findings demonstrate that the potential benefits of oxytocin in autism extend to a real-time interaction, providing evidence of a therapeutic effect in a key aspect of social communication.

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          Most cited references38

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          The "Reading the Mind in the Eyes" Test Revised Version: A Study with Normal Adults, and Adults with Asperger Syndrome or High-functioning Autism

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            Oxytocin, vasopressin, and the neurogenetics of sociality.

            There is growing evidence that the neuropeptides oxytocin and vasopressin modulate complex social behavior and social cognition. These ancient neuropeptides display a marked conservation in gene structure and expression, yet diversity in the genetic regulation of their receptors seems to underlie natural variation in social behavior, both between and within species. Human studies are beginning to explore the roles of these neuropeptides in social cognition and behavior and suggest that variation in the genes encoding their receptors may contribute to variation in human social behavior by altering brain function. Understanding the neurobiology and neurogenetics of social cognition and behavior has important implications, both clinically and for society.
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              Oxytocin modulates neural circuitry for social cognition and fear in humans.

              In non-human mammals, the neuropeptide oxytocin is a key mediator of complex emotional and social behaviors, including attachment, social recognition, and aggression. Oxytocin reduces anxiety and impacts on fear conditioning and extinction. Recently, oxytocin administration in humans was shown to increase trust, suggesting involvement of the amygdala, a central component of the neurocircuitry of fear and social cognition that has been linked to trust and highly expresses oxytocin receptors in many mammals. However, no human data on the effects of this peptide on brain function were available. Here, we show that human amygdala function is strongly modulated by oxytocin. We used functional magnetic resonance imaging to image amygdala activation by fear-inducing visual stimuli in 15 healthy males after double-blind crossover intranasal application of placebo or oxytocin. Compared with placebo, oxytocin potently reduced activation of the amygdala and reduced coupling of the amygdala to brainstem regions implicated in autonomic and behavioral manifestations of fear. Our results indicate a neural mechanism for the effects of oxytocin in social cognition in the human brain and provide a methodology and rationale for exploring therapeutic strategies in disorders in which abnormal amygdala function has been implicated, such as social phobia or autism.
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                Author and article information

                Journal
                Transl Psychiatry
                Transl Psychiatry
                Translational Psychiatry
                Nature Publishing Group
                2158-3188
                February 2015
                10 February 2015
                1 February 2015
                : 5
                : 2
                : e507
                Affiliations
                [1 ]Department of Psychology, The School of Philosophy, Psychology and Language Sciences, University of Edinburgh , Edinburgh, UK
                [2 ]Autism Research Centre, Department of Psychiatry, University of Cambridge , Cambridge, UK
                [3 ]Department of Psychology, University of Cyprus , Nicosia, Cyprus
                [4 ]Center for Applied Neuroscience, University of Cyprus , Nicosia, Cyprus
                [5 ]Department of Psychology, Laboratory for Biological and Personality Psychology, University of Freiburg , Freiburg, Germany
                [6 ]Freiburg Brain Imaging Center, University Medical Center, University of Freiburg , Freiburg, Germany
                [7 ]School of Psychology and Clinical Language Sciences, University of Reading, Whiteknights , Reading, UK
                [8 ]South Essex Partnership University NHS Foundation Trust , Bedford, UK
                [9 ]Department of Psychiatry, University of Cambridge , Cambridge, UK
                [10 ]Cambridgeshire and Peterborough NHS Foundation Trust (CPFT) , Cambridge, UK
                Author notes
                [* ]Department of Psychology, The School of Philosophy, Psychology and Language Sciences, University of Edinburgh , 7 George Square, Edinburgh EH8 9JZ, UK. E-mail: bonnie.auyeung@ 123456ed.ac.uk
                Author information
                http://orcid.org/0000-0002-6649-7895
                Article
                tp2014146
                10.1038/tp.2014.146
                4445747
                25668435
                87b24783-f04e-46d9-b485-7e90188ce0ea
                Copyright © 2015 Macmillan Publishers Limited

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 15 September 2014
                : 03 November 2014
                : 01 December 2014
                Categories
                Original Article

                Clinical Psychology & Psychiatry
                Clinical Psychology & Psychiatry

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