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      Visual-Tactile Spatial Multisensory Interaction in Adults With Autism and Schizophrenia

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          Abstract

          Background: Individuals with autism spectrum disorder (ASD) and schizophrenia (SZ) exhibit multisensory processing difficulties and social impairments, with growing evidence that the former contributes to the latter. However, this work has largely reported on separate cohorts, introducing method variance as a barrier to drawing broad conclusions across studies. Further, very few studies have addressed touch, resulting in sparse knowledge about how these two clinical groups may integrate somatic information with other senses.

          Methods: In this study, we compared adults with ASD ( n = 29), SZ ( n = 24), and typical developmental histories (TD, n = 37) on two tasks requiring visual-tactile spatial multisensory processing. In the first task (crossmodal congruency), participants judged the location of a tactile stimulus in the presence or absence of simultaneous visual input that was either spatially congruent or incongruent, with poorer performance for incongruence an index of spatial multisensory interaction. In the second task, participants reacted to touch in the presence or absence of dynamic visual stimuli that appeared to approach or recede from the body. Within a certain radius around the body, defined as peripersonal space (PPS), an approaching visual or auditory stimulus reliably speeds reaction times (RT) to touch; outside of this radius, in extrapersonal space (EPS), there is no multisensory effect. PPS can be defined both by its size (radius) and slope (sharpness of the PPS-EPS boundary). Clinical measures were administered to explore relations with visual-tactile processing.

          Results: Neither clinical group differed from controls on the crossmodal congruency task. The ASD group had significantly smaller and more sharply-defined PPSs compared to the other two groups. Small PPS size was related to social symptom severity across groups, but was largely driven by the TD group, without significant effects in either clinical group.

          Conclusions: These results suggest that: (1) spatially static visual-tactile facilitation is intact in adults with ASD and SZ, (2) spatially dynamic visual-tactile facilitation impacting perception of the body boundary is affected in ASD but not SZ, and (3) body boundary perception is related to social-emotional function, but not in a way that maps on to clinical status.

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          Most cited references82

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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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            Autistic traits in the general population: a twin study.

            Recent research has indicated that autism is not a discrete disorder and that family members of autistic probands have an increased likelihood of exhibiting autistic symptoms with a wide range of severity, often below the threshold for a diagnosis of an autism spectrum disorder. To examine the distribution and genetic structure of autistic traits in the general population using a newly established quantitative measure of autistic traits, the Social Responsiveness Scale (formerly known as the Social Reciprocity Scale). The sample consisted of 788 pairs of twins aged 7 to 15 years, randomly selected from the pool of participants in a large epidemiologic study (the Missouri Twin Study). One parent of each pair of twins completed the Social Responsiveness Scale on each child. The data were subjected to structural equation modeling. Autistic traits as measured by the Social Responsiveness Scale were continuously distributed and moderately to highly heritable. Levels of severity of autistic traits at or above the previously published mean for patients with pervasive developmental disorder not otherwise specified were found in 1.4% of boys and 0.3% of girls. Structural equation modeling revealed no evidence for the existence of sex-specific genetic influences, and suggested specific mechanisms by which females may be relatively protected from vulnerability to autistic traits. These data indicate that the social deficits characteristic of autism spectrum disorders are common. Given the continuous distribution of these traits, it may be arbitrary where cutoffs are made between research designations of being "affected" vs "unaffected" with a pervasive developmental disorder. The genes influencing autistic traits appear to be the same for boys and girls. Lower prevalence (and severity) of autistic traits in girls may be the result of increased sensitivity to early environmental influences that operate to promote social competency.
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              Visuospatial properties of ventral premotor cortex.

              In macaque ventral premotor cortex, we recorded the activity of neurons that responded to both visual and tactile stimuli. For these bimodal cells, the visual receptive field extended from the tactile receptive field into the adjacent space. Their tactile receptive fields were organized topographically, with the arms represented medially, the face represented in the middle, and the inside of the mouth represented laterally. For many neurons, both the visual and tactile responses were directionally selective, although many neurons also responded to stationary stimuli. In the awake monkeys, for 70% of bimodal neurons with a tactile response on the arm, the visual receptive field moved when the arm was moved. In contrast, for 0% the visual receptive field moved when the eye or head moved. Thus the visual receptive fields of most "arm + visual" cells were anchored to the arm, not to the eye or head. In the anesthetized monkey, the effect of arm position was similar. For 95% of bimodal neurons with a tactile response on the face, the visual receptive field moved as the head was rotated. In contrast, for 15% the visual receptive field moved with the eye and for 0% it moved with the arm. Thus the visual receptive fields of most "face + visual" cells were anchored to the head, not to the eye or arm. To construct a visual receptive field anchored to the arm, it is necessary to integrate the position of the arm, head, and eye. For arm + visual cells, the spontaneous activity, the magnitude of the visual response, and sometimes both were modulated by the position of the arm (37%), the head (75%), and the eye (58%). In contrast, to construct a visual receptive field that is anchored to the head, it is necessary to use the position of the eye, but not of the head or the arm. For face + visual cells, the spontaneous activity and/or response magnitude was modulated by the position of the eyes (88%), but not of the head or the arm (0%). Visual receptive fields anchored to the arm can encode stimulus location in "arm-centered" coordinates, and would be useful for guiding arm movements. Visual receptive fields anchored to the head can likewise encode stimuli in "head-centered" coordinates, useful for guiding head movements. Sixty-three percent of face + visual neurons responded during voluntary movements of the head. We suggest that "body-part-centered" coordinates provide a general solution to a problem of sensory-motor integration: sensory stimuli are located in a coordinate system anchored to a particular body part.
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                Author and article information

                Contributors
                Journal
                Front Psychiatry
                Front Psychiatry
                Front. Psychiatry
                Frontiers in Psychiatry
                Frontiers Media S.A.
                1664-0640
                23 October 2020
                2020
                : 11
                : 578401
                Affiliations
                [1] 1Center for Neural Science, New York University , New York, NY, United States
                [2] 2Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center , Nashville, TN, United States
                [3] 3Vanderbilt Brain Institute, Vanderbilt University , Nashville, TN, United States
                [4] 4Department of Hearing and Speech Sciences, Vanderbilt University Medical Center , Nashville, TN, United States
                [5] 5Medical Scientist Training Program, Vanderbilt University School of Medicine , Nashville, TN, United States
                [6] 6School of Criminology and Justice Policty, Northeastern University , Boston, MA, United States
                [7] 7Core Scientific , Seattle, WA, United States
                [8] 8Department of Psychiatry and Seaver Center for Autism Research, Mount Sinai Hospital , New York, NY, United States
                [9] 9Department of Psychology, Vanderbilt University , Nashville, TN, United States
                [10] 10Vanderbilt Frist Center for Autism and Innovation , Nashville, TN, United States
                Author notes

                Edited by: Amy Pinkham, The University of Texas at Dallas, United States

                Reviewed by: Jessica Ann Wojtalik, Case Western Reserve University, United States; Antigona Martinez, Nathan Kline Institute for Psychiatric Research, United States; Francesca Garbarini, University of Turin, Italy

                *Correspondence: Carissa J. Cascio carissa.cascio@ 123456vumc.org

                This article was submitted to Social Cognition, a section of the journal Frontiers in Psychiatry

                Article
                10.3389/fpsyt.2020.578401
                7644602
                33192716
                2bf8a825-6417-4222-8f71-45a901eb5456
                Copyright © 2020 Noel, Failla, Quinde-Zlibut, Williams, Gerdes, Tracy, Zoltowski, Foss-Feig, Nichols, Armstrong, Heckers, Blake, Wallace, Park and Cascio.

                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) and the copyright owner(s) 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
                : 08 July 2020
                : 22 September 2020
                Page count
                Figures: 4, Tables: 1, Equations: 1, References: 83, Pages: 13, Words: 9332
                Funding
                Funded by: National Institute of Mental Health 10.13039/100000025
                Award ID: 5T32MH064913
                Award ID: R21MH109225
                Award ID: T32MH18921
                Funded by: National Institute of General Medical Sciences 10.13039/100000057
                Award ID: T32-GM007347
                Funded by: National Center for Advancing Translational Sciences 10.13039/100006108
                Award ID: TL1TR002244
                Award ID: UL1 TR000445
                Funded by: Eunice Kennedy Shriver National Institute of Child Health and Human Development 10.13039/100009633
                Award ID: U54HD083211
                Funded by: National Eye Institute 10.13039/100000053
                Categories
                Psychiatry
                Original Research

                Clinical Psychology & Psychiatry
                cross-modal congruency effect,peripersonal space,depth,logistic regression,psychopathology,somatic,developmental disorders,tactile perception

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