Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications

<p><b>Abstract</b></p> <p>Most behavioral training regimens in autism spectrum disorders (ASD) rely on reward-based reinforcement strategies. Although proven to significantly increase both cognitive and social outcomes and successfully reduce aberrant behaviors, this ap...

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Main Authors: Kohls Gregor, Chevallier Coralie, Troiani Vanessa, Schultz Robert T
Format: Article
Language:English
Published: BMC 2012-06-01
Series:Journal of Neurodevelopmental Disorders
Subjects:
Online Access:http://www.jneurodevdisorders.com/content/4/1/10
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author Kohls Gregor
Chevallier Coralie
Troiani Vanessa
Schultz Robert T
author_facet Kohls Gregor
Chevallier Coralie
Troiani Vanessa
Schultz Robert T
author_sort Kohls Gregor
collection DOAJ
description <p><b>Abstract</b></p> <p>Most behavioral training regimens in autism spectrum disorders (ASD) rely on reward-based reinforcement strategies. Although proven to significantly increase both cognitive and social outcomes and successfully reduce aberrant behaviors, this approach fails to benefit a substantial number of affected individuals. Given the enormous amount of clinical and financial resources devoted to behavioral interventions, there is a surprisingly large gap in our knowledge of the basic reward mechanisms of learning in ASD. Understanding the mechanisms for reward responsiveness and reinforcement-based learning is urgently needed to better inform modifications that might improve current treatments. The fundamental goal of this review is to present a fine-grained literature analysis of reward function in ASD with reference to a validated neurobiological model of reward: the ‘wanting’/’liking’ framework. Despite some inconsistencies within the available literature, the evaluation across three converging sets of neurobiological data (neuroimaging, electrophysiological recordings, and neurochemical measures) reveals good evidence for disrupted reward-seeking tendencies in ASD, particularly in social contexts. This is most likely caused by dysfunction of the dopaminergic–oxytocinergic ‘wanting’ circuitry, including the ventral striatum, amygdala, and ventromedial prefrontal cortex. Such a conclusion is consistent with predictions derived from diagnostic criteria concerning the core social phenotype of ASD, which emphasize difficulties with spontaneous self-initiated seeking of social encounters (that is, social motivation). Existing studies suggest that social ‘wanting’ tendencies vary considerably between individuals with ASD, and that the degree of social motivation is both malleable and predictive of intervention response. Although the topic of reward responsiveness in ASD is very new, with much research still needed, the current data clearly point towards problems with incentive-based motivation and learning, with clear and important implications for treatment. Given the reliance of behavioral interventions on reinforcement-based learning principles, we believe that a systematic focus on the integrity of the reward system in ASD promises to yield many important clues, both to the underlying mechanisms causing ASD and to enhancing the efficacy of existing and new interventions.</p>
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spelling doaj.art-db46ef91c10c42f281c9da1fd1e1c9582022-12-21T21:18:25ZengBMCJournal of Neurodevelopmental Disorders1866-19552012-06-01411010.1186/1866-1955-4-10Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implicationsKohls GregorChevallier CoralieTroiani VanessaSchultz Robert T<p><b>Abstract</b></p> <p>Most behavioral training regimens in autism spectrum disorders (ASD) rely on reward-based reinforcement strategies. Although proven to significantly increase both cognitive and social outcomes and successfully reduce aberrant behaviors, this approach fails to benefit a substantial number of affected individuals. Given the enormous amount of clinical and financial resources devoted to behavioral interventions, there is a surprisingly large gap in our knowledge of the basic reward mechanisms of learning in ASD. Understanding the mechanisms for reward responsiveness and reinforcement-based learning is urgently needed to better inform modifications that might improve current treatments. The fundamental goal of this review is to present a fine-grained literature analysis of reward function in ASD with reference to a validated neurobiological model of reward: the ‘wanting’/’liking’ framework. Despite some inconsistencies within the available literature, the evaluation across three converging sets of neurobiological data (neuroimaging, electrophysiological recordings, and neurochemical measures) reveals good evidence for disrupted reward-seeking tendencies in ASD, particularly in social contexts. This is most likely caused by dysfunction of the dopaminergic–oxytocinergic ‘wanting’ circuitry, including the ventral striatum, amygdala, and ventromedial prefrontal cortex. Such a conclusion is consistent with predictions derived from diagnostic criteria concerning the core social phenotype of ASD, which emphasize difficulties with spontaneous self-initiated seeking of social encounters (that is, social motivation). Existing studies suggest that social ‘wanting’ tendencies vary considerably between individuals with ASD, and that the degree of social motivation is both malleable and predictive of intervention response. Although the topic of reward responsiveness in ASD is very new, with much research still needed, the current data clearly point towards problems with incentive-based motivation and learning, with clear and important implications for treatment. Given the reliance of behavioral interventions on reinforcement-based learning principles, we believe that a systematic focus on the integrity of the reward system in ASD promises to yield many important clues, both to the underlying mechanisms causing ASD and to enhancing the efficacy of existing and new interventions.</p>http://www.jneurodevdisorders.com/content/4/1/10Autism spectrum disordersRewardSocial motivationVentral striatumVentromedial prefrontal cortexAmygdalaDopamineOxytocinOpioidsTreatment
spellingShingle Kohls Gregor
Chevallier Coralie
Troiani Vanessa
Schultz Robert T
Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications
Journal of Neurodevelopmental Disorders
Autism spectrum disorders
Reward
Social motivation
Ventral striatum
Ventromedial prefrontal cortex
Amygdala
Dopamine
Oxytocin
Opioids
Treatment
title Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications
title_full Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications
title_fullStr Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications
title_full_unstemmed Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications
title_short Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications
title_sort social wanting dysfunction in autism neurobiological underpinnings and treatment implications
topic Autism spectrum disorders
Reward
Social motivation
Ventral striatum
Ventromedial prefrontal cortex
Amygdala
Dopamine
Oxytocin
Opioids
Treatment
url http://www.jneurodevdisorders.com/content/4/1/10
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