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      Adaptive sensory coding of gaze direction in schizophrenia

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          Abstract

          Schizophrenia has been associated with differences in how the visual system processes sensory input. A fundamental mechanism that regulates sensory processing in the brain is gain control, whereby the responses of sensory neurons to a given stimulus are modulated in accordance with the spatial and temporal context. Some studies indicate an impairment of certain cortical gain control mechanisms in schizophrenia in low-level vision, reflected, for instance, in how the visual appearance of a stimulus is affected by the presence of other stimuli around it. In the present study, we investigated higher-level, social vision in schizophrenia, namely the perception of other people's direction of gaze (i.e. a type of face processing). Recent computational modelling work indicates that perceptual aftereffects—changes in perception that occur following repeated exposure to faces that display a specific direction of gaze—are indicative of two distinct forms of gain control involved in the coding of gaze direction across sensory neurons. We find that individuals with schizophrenia display strong perceptual aftereffects following repeated exposure to faces with averted gaze, and a modelling analysis indicates similarly robust gain control in the form of (i) short-term adjustment of channel sensitivities in response to the recent sensory history and (ii) divisive normalization of the encoded gaze direction. Together, this speaks to the typical coding of other people's direction of gaze in the visual system in schizophrenia, including flexible gain control, despite the social–cognitive impairments that can occur in this condition.

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          Most cited references58

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          Abnormal neural oscillations and synchrony in schizophrenia.

          Converging evidence from electrophysiological, physiological and anatomical studies suggests that abnormalities in the synchronized oscillatory activity of neurons may have a central role in the pathophysiology of schizophrenia. Neural oscillations are a fundamental mechanism for the establishment of precise temporal relationships between neuronal responses that are in turn relevant for memory, perception and consciousness. In patients with schizophrenia, the synchronization of beta- and gamma-band activity is abnormal, suggesting a crucial role for dysfunctional oscillations in the generation of the cognitive deficits and other symptoms of the disorder. Dysfunctional oscillations may arise owing to anomalies in the brain's rhythm-generating networks of GABA (gamma-aminobutyric acid) interneurons and in cortico-cortical connections.
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            Normalization as a canonical neural computation.

            There is increasing evidence that the brain relies on a set of canonical neural computations, repeating them across brain regions and modalities to apply similar operations to different problems. A promising candidate for such a computation is normalization, in which the responses of neurons are divided by a common factor that typically includes the summed activity of a pool of neurons. Normalization was developed to explain responses in the primary visual cortex and is now thought to operate throughout the visual system, and in many other sensory modalities and brain regions. Normalization may underlie operations such as the representation of odours, the modulatory effects of visual attention, the encoding of value and the integration of multisensory information. Its presence in such a diversity of neural systems in multiple species, from invertebrates to mammals, suggests that it serves as a canonical neural computation.
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              Social cognition in schizophrenia.

              Individuals with schizophrenia exhibit impaired social cognition, which manifests as difficulties in identifying emotions, feeing connected to others, inferring people's thoughts and reacting emotionally to others. These social cognitive impairments interfere with social connections and are strong determinants of the degree of impaired daily functioning in such individuals. Here, we review recent findings from the fields of social cognition and social neuroscience and identify the social processes that are impaired in schizophrenia. We also consider empathy as an example of a complex social cognitive function that integrates several social processes and is impaired in schizophrenia. This information may guide interventions to improve social cognition in patients with this disorder.
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                Author and article information

                Journal
                R Soc Open Sci
                R Soc Open Sci
                RSOS
                royopensci
                Royal Society Open Science
                The Royal Society
                2054-5703
                December 2018
                12 December 2018
                12 December 2018
                : 5
                : 12
                : 180886
                Affiliations
                [1 ]School of Psychology, UNSW Sydney, Sydney, New South Wales 2052, Australia
                [2 ]Department of Cognitive Science, Macquarie University , Sydney, New South Wales 2109, Australia
                [3 ]ARC Centre of Excellence for Cognition and Its Disorders , Sydney, Australia
                [4 ]School of Social Sciences and Psychology, Western Sydney University , Sydney, New South Wales 2150, Australia
                Author notes
                Author for correspondence: Colin J. Palmer e-mail: colin.palmer@ 123456unsw.edu.au
                [†]

                These authors contributed equally to the study.

                Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.4302935.

                Author information
                http://orcid.org/0000-0002-1058-3428
                http://orcid.org/0000-0002-9676-814X
                http://orcid.org/0000-0003-1043-6118
                http://orcid.org/0000-0002-2988-3121
                Article
                rsos180886
                10.1098/rsos.180886
                6304156
                5d89d47a-33cf-407e-9071-f9e9fe38c455
                © 2018 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 7 June 2018
                : 30 October 2018
                Funding
                Funded by: Australian Research Council Centre of Excellence for Cognition and its Disorders;
                Award ID: CE110001021
                Funded by: Society for Mental Health Research, Australia;
                Funded by: ARC CCD Cross Program Support Scheme;
                Funded by: Australian Research Council Discovery Project grant;
                Award ID: DP160102239
                Categories
                1001
                205
                Psychology and Cognitive Neuroscience
                Research Article
                Custom metadata
                December, 2018

                schizophrenia,gaze perception,adaptation,aftereffects,normalization,visual processing

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