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      Impaired Learning of Social Compared to Monetary Rewards in Autism

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          Abstract

          A leading hypothesis to explain the social dysfunction in people with autism spectrum disorders (ASD) is that they exhibit a deficit in reward processing and motivation specific to social stimuli. However, there have been few direct tests of this hypothesis to date. Here we used an instrumental reward learning task that contrasted learning with social rewards (pictures of positive and negative faces) against learning with monetary reward (winning and losing money). The two tasks were structurally identical except for the type of reward, permitting direct comparisons. We tested 10 high-functioning people with ASD (7M, 3F) and 10 healthy controls who were matched on gender, age, and education. We found no significant differences between the two groups in terms of overall ability behaviorally to discriminate positive from negative slot machines, reaction-times, and valence ratings, However, there was a specific impairment in the ASD group in learning to choose social rewards, compared to monetary rewards: they had a significantly lower cumulative number of choices of the most rewarding social slot machine, and had a significantly slower initial learning rate for the socially rewarding slot machine, compared to the controls. The findings show a deficit in reward learning in ASD that is greater for social rewards than for monetary rewards, and support the hypothesis of a disproportionate impairment in social reward processing in ASD.

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          Reward processing in autism.

          The social motivation hypothesis of autism posits that infants with autism do not experience social stimuli as rewarding, thereby leading to a cascade of potentially negative consequences for later development. While possible downstream effects of this hypothesis such as altered face and voice processing have been examined, there has not been a direct investigation of social reward processing in autism. Here we use functional magnetic resonance imaging to examine social and monetary rewarded implicit learning in children with and without autism spectrum disorders (ASD). Sixteen males with ASD and sixteen age- and IQ-matched typically developing (TD) males were scanned while performing two versions of a rewarded implicit learning task. In addition to examining responses to reward, we investigated the neural circuitry supporting rewarded learning and the relationship between these factors and social development. We found diminished neural responses to both social and monetary rewards in ASD, with a pronounced reduction in response to social rewards (SR). Children with ASD also demonstrated a further deficit in frontostriatal response during social, but not monetary, rewarded learning. Moreover, we show a relationship between ventral striatum activity and social reciprocity in TD children. Together, these data support the hypothesis that children with ASD have diminished neural responses to SR, and that this deficit relates to social learning impairments.
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            Children with autism fail to orient to naturally occurring social stimuli.

            Children with autism were compared to developmentally matched children with Down syndrome or typical development in terms of their ability to visually orient to two social stimuli (name called, hands clapping) and two nonsocial stimuli (rattle, musical jack-in-the-box), and in terms of their ability to share attention (following another's gaze or point). It was found that, compared to children with Down syndrome or typical development, children with autism more frequently failed to orient to all stimuli, and that this failure was much more extreme for social stimuli. Children with autism who oriented to social stimuli took longer to do so compared to the other two groups of children. Children with autism also exhibited impairments in shared attention. Moreover, for both children with autism and Down syndrome, correlational analyses revealed a relation between shared attention performance and the ability to orient to social stimuli, but no relation between shared attention performance and the ability to orient to nonsocial stimuli. Results suggest that social orienting impairments may contribute to difficulties in shared attention found in autism.
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              Reward circuitry function in autism during face anticipation and outcomes.

              The aim of this study was to investigate reward circuitry responses in autism during reward anticipation and outcomes for monetary and social rewards. During monetary anticipation, participants with autism spectrum disorders (ASDs) showed hypoactivation in right nucleus accumbens and hyperactivation in right hippocampus, whereas during monetary outcomes, participants with ASDs showed hyperactivation in left midfrontal and anterior cingulate gyrus. Groups did not differ in nucleus accumbens responses to faces. The ASD group demonstrated hyperactivation in bilateral amygdala during face anticipation that predicted social symptom severity and in bilateral insular cortex during face outcomes. These results add to the growing body of evidence that autism is characterized by altered functioning of reward circuitry. Additionally, atypical amygdala activation during the processing of social rewards may contribute to the development or expression of autistic features.
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                Author and article information

                Journal
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Research Foundation
                1662-4548
                1662-453X
                01 October 2012
                2012
                : 6
                : 143
                Affiliations
                [1] 1simpleComputations and Neural Systems, California Institute of Technology Pasadena, CA, USA
                [2] 2simpleDivision of Humanities and Social Sciences, California Institute of Technology Pasadena, CA, USA
                Author notes

                Edited by: Guido Biele, University of Oslo, Norway

                Reviewed by: Geoffrey Schoenbaum, University of Maryland School of Medicine, USA; Andrew Barto, University of Massachusetts Amherst, USA

                *Correspondence: Ralph Adolphs, Division of Humanities and Social Sciences, California Institute of Technology, HSS 228-77, Pasadena, CA 91125-7700, USA. e-mail: adolphs@ 123456hss.caltech.edu

                This article was submitted to Frontiers in Decision Neuroscience, a specialty of Frontiers in Neuroscience.

                Article
                10.3389/fnins.2012.00143
                3461406
                23060743
                98b1a57f-15e6-4b20-aa50-f380b96e3e16
                Copyright © 2012 Lin, Rangel and Adolphs.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                History
                : 04 July 2012
                : 11 September 2012
                Page count
                Figures: 6, Tables: 1, Equations: 0, References: 18, Pages: 7, Words: 5225
                Categories
                Neuroscience
                Original Research

                Neurosciences
                social reward,autism,monetary reward
                Neurosciences
                social reward, autism, monetary reward

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