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      Autism Spectrum Disorders and Schizophrenia: Meta-Analysis of the Neural Correlates of Social Cognition

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          Abstract

          Context

          Impaired social cognition is a cardinal feature of Autism Spectrum Disorders (ASD) and Schizophrenia (SZ). However, the functional neuroanatomy of social cognition in either disorder remains unclear due to variability in primary literature. Additionally, it is not known whether deficits in ASD and SZ arise from similar or disease-specific disruption of the social cognition network.

          Objective

          To identify regions most robustly implicated in social cognition processing in SZ and ASD.

          Data Sources

          Systematic review of English language articles using MEDLINE (1995–2010) and reference lists.

          Study Selection

          Studies were required to use fMRI to compare ASD or SZ subjects to a matched healthy control group, provide coordinates in standard stereotactic space, and employ standardized facial emotion recognition (FER) or theory of mind (TOM) paradigms.

          Data Extraction

          Activation foci from studies meeting inclusion criteria (n = 33) were subjected to a quantitative voxel-based meta-analysis using activation likelihood estimation, and encompassed 146 subjects with ASD, 336 SZ patients and 492 healthy controls.

          Results

          Both SZ and ASD showed medial prefrontal hypoactivation, which was more pronounced in ASD, while ventrolateral prefrontal dysfunction was associated mostly with SZ. Amygdala hypoactivation was observed in SZ patients during FER and in ASD during more complex ToM tasks. Both disorders were associated with hypoactivation within the Superior Temporal Sulcus (STS) during ToM tasks, but activation in these regions was increased in ASD during affect processing. Disease-specific differences were noted in somatosensory engagement, which was increased in SZ and decreased in ASD. Reduced thalamic activation was uniquely seen in SZ.

          Conclusions

          Reduced frontolimbic and STS engagement emerged as a shared feature of social cognition deficits in SZ and ASD. However, there were disease- and stimulus-specific differences. These findings may aid future studies on SZ and ASD and facilitate the formulation of new hypotheses regarding their pathophysiology.

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          Most cited references78

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          The positive and negative syndrome scale (PANSS) for schizophrenia.

          The variable results of positive-negative research with schizophrenics underscore the importance of well-characterized, standardized measurement techniques. We report on the development and initial standardization of the Positive and Negative Syndrome Scale (PANSS) for typological and dimensional assessment. Based on two established psychiatric rating systems, the 30-item PANSS was conceived as an operationalized, drug-sensitive instrument that provides balanced representation of positive and negative symptoms and gauges their relationship to one another and to global psychopathology. It thus constitutes four scales measuring positive and negative syndromes, their differential, and general severity of illness. Study of 101 schizophrenics found the four scales to be normally distributed and supported their reliability and stability. Positive and negative scores were inversely correlated once their common association with general psychopathology was extracted, suggesting that they represent mutually exclusive constructs. Review of five studies involving the PANSS provided evidence of its criterion-related validity with antecedent, genealogical, and concurrent measures, its predictive validity, its drug sensitivity, and its utility for both typological and dimensional assessment.
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            Neurobiology of emotion perception I: The neural basis of normal emotion perception.

            There is at present limited understanding of the neurobiological basis of the different processes underlying emotion perception. We have aimed to identify potential neural correlates of three processes suggested by appraisalist theories as important for emotion perception: 1) the identification of the emotional significance of a stimulus; 2) the production of an affective state in response to 1; and 3) the regulation of the affective state. In a critical review, we have examined findings from recent animal, human lesion, and functional neuroimaging studies. Findings from these studies indicate that these processes may be dependent upon the functioning of two neural systems: a ventral system, including the amygdala, insula, ventral striatum, and ventral regions of the anterior cingulate gyrus and prefrontal cortex, predominantly important for processes 1 and 2 and automatic regulation of emotional responses; and a dorsal system, including the hippocampus and dorsal regions of anterior cingulate gyrus and prefrontal cortex, predominantly important for process 3. We suggest that the extent to which a stimulus is identified as emotive and is associated with the production of an affective state may be dependent upon levels of activity within these two neural systems.
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              Neural systems for recognizing emotion.

              Recognition of emotion draws on a distributed set of structures that include the occipitotemporal neocortex, amygdala, orbitofrontal cortex and right frontoparietal cortices. Recognition of fear may draw especially on the amygdala and the detection of disgust may rely on the insula and basal ganglia. Two important mechanisms for recognition of emotions are the construction of a simulation of the observed emotion in the perceiver, and the modulation of sensory cortices via top-down influences.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                5 October 2011
                : 6
                : 10
                : e25322
                Affiliations
                [1 ]Department of Child and Adolescent Psychiatry, Institute of Psychiatry, King's College London, London, United Kingdom
                [2 ]Section of Neurobiology of Psychosis, Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, United Kingdom
                [3 ]Department of Child and Adolescent Psychiatry and Psychology, Institute of Neuroscience, University of Barcelona, Barcelona, Spain
                [4 ]Child and Adolescent Mental Health Services, South London and Maudsley NHS Foundation Trust, London, United Kingdom
                University of Adelaide, Australia
                Author notes

                Conceived and designed the experiments: SF ET. Performed the experiments: SF GS MK. Analyzed the data: SF GS MK. Contributed reagents/materials/analysis tools: SF GS MK. Wrote the paper: SF GS MK RC ET.

                Article
                PONE-D-11-10972
                10.1371/journal.pone.0025322
                3187762
                21998649
                7f1b4921-bb31-4745-97cf-a53a33bc2fdc
                Sugranyes et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 18 June 2011
                : 31 August 2011
                Page count
                Pages: 13
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Neurological System
                Neuroanatomy
                Neuroscience
                Neuroanatomy
                Medicine
                Anatomy and Physiology
                Neurological System
                Neuroanatomy
                Clinical Research Design
                Meta-Analyses
                Mental Health
                Psychiatry
                Adolescent Psychiatry
                Child Psychiatry
                Psychoses
                Schizophrenia
                Neurology
                Developmental and Pediatric Neurology
                Pediatrics
                Developmental and Pediatric Neurology
                Social and Behavioral Sciences
                Psychology
                Neuropsychology

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                Uncategorized

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