Abstract

Autism is a neurodevelopmental condition defined on clinical criteria related to diminished social reciprocity and stereotyped behavior. An influential view explains autism as a social motivation disorder characterized by less attention paid to the social environment and less pleasure experienced with social rewards. However, experimental attempts to validate this theory, by testing the impact of social reward on behavioral choice and brain activity, has yielded mixed results, possibly due to variations in how explicit instructions were about task goals. Here, we specified the putative motivation deficit as an absence of spontaneous valuation in the social domain, unexplained by inattention and correctible by explicit instruction. Since such deficit cannot be assessed with behavioral measures, we used functional neuroimaging (fMRI) to readout covert subjective values, assigned to social and nonsocial stimuli (faces and objects), either explicitly asked to participants (during a likeability judgment task) or not (during age or size estimation tasks). Value-related neural activity observed for objects, or for faces under explicit instructions, was very similar in autistic and control participants, with an activation peak in the ventromedial prefrontal cortex (vmPFC), known as a key node of the brain valuation system. The only difference observed in autistic participants was an absence of the spontaneous valuation normally triggered by faces, even when they were attended for age estimation. Our findings, therefore, suggest that in autism, social stimuli might fail to trigger the automatic activation of the brain valuation system.

Highlights

  • Autism[1, 2]1 refers to a broad spectrum of neurodevelopmental conditions that manifest as altered social interaction, atypical communication along with increased reactivity to the sensory environment, and stereotyped behaviors

  • An influent theory suggests that a major explanatory factor is a lack of social motivation [4]: autistic persons tend to report less pleasure in social activities, and spend less resources seeking social rewards

  • Even if value signals were globally lower in autistic participants during the orthogonal task, there was no significant difference between groups

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Summary

Introduction

Autism[1, 2]1 refers to a broad spectrum of neurodevelopmental conditions that manifest as altered social interaction, atypical communication along with increased reactivity to the sensory environment, and stereotyped behaviors. The results have been somewhat inconsistent: some confirm a lack of response to social rewards [13,14,15], while others report an equivalent or even more pronounced deficit in processing nonsocial rewards such as money [16, 17] (see [18] for a recent meta-analysis) These conflicting results might relate to the type of stimuli used during fMRI scanning [19], and to their ecological relevance in particular, and to the instructions being more or less explicit about the goal to maximize reward in the tasks performed. Autistic persons can pass the false belief task (used to assess the theory of mind) when explicitly asked to do so, even if they do not show evidence of spontaneous belief attribution [20, 21] They can process facial expression, tone of voice, or gaze direction in accordance with instructions, even if they spontaneously ignore these features during natural conversations [21, 22]. We reasoned that autistic persons may not spontaneously monitor the value of Received: 14 September 2020 Revised: 26 June 2021 Accepted: 2 August 2021

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