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Social-interactive reward elicits similar neural response in autism and typical development and predicts future social experiences.

ABSTRACT: Challenges in initiating and responding to social-interactive exchanges are a key diagnostic feature of autism spectrum disorder, yet investigations into the underlying neural mechanisms of social interaction have been hampered by reliance on non-interactive approaches. Using an innovative social-interactive neuroscience approach, we investigated differences between youth with autism and youth with typical development in neural response to a chat-based social-interactive reward, as well as factors such as age and self-reported social enjoyment that may account for heterogeneity in that response. We found minimal group differences in neural and behavioral response to social-interactive reward, and variation within both groups was related to self-reported social enjoyment during the task. Furthermore, neural sensitivity to social-interactive reward predicted future enjoyment of a face-to-face social interaction with a novel peer. These findings have important implications for understanding the nature of social reward and peer interactions in typical development as well as for future research informing social interactions in individuals on the autism spectrum.

SUBMITTER: McNaughton KA

PROVIDER: S-EPMC9852551 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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Social-interactive reward elicits similar neural response in autism and typical development and predicts future social experiences.

McNaughton Kathryn A KA Kirby Laura Anderson LA Warnell Katherine Rice KR Alkire Diana D Merchant Junaid S JS Moraczewski Dustin D Yarger Heather A HA Thurm Audrey A Redcay Elizabeth E

Developmental cognitive neuroscience 20230106

Challenges in initiating and responding to social-interactive exchanges are a key diagnostic feature of autism spectrum disorder, yet investigations into the underlying neural mechanisms of social interaction have been hampered by reliance on non-interactive approaches. Using an innovative social-interactive neuroscience approach, we investigated differences between youth with autism and youth with typical development in neural response to a chat-based social-interactive reward, as well as facto ...[more]

PMID: 36640623

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Project description:The current literature suggests that some women are uniquely vulnerable to negative effects of hormonal contraception (HC) on affective processes. However, little data exists as to which factors contribute to such vulnerability. The present study evaluated the impact of prepubertal adverse childhood experiences (ACEs) on reward processing in women taking HC (N = 541) compared to naturally cycling women (N = 488). Participants completed an online survey assessing current and past HC use and exposure to 10 different adverse childhood experiences (ACEs) before puberty (ACE Questionnaire), with participants categorized into groups of low (0-1) versus high (≥2) prepubertal ACE exposure. Participants then completed a reward task rating their expected and experienced valence for images that were either erotic, pleasant (non-erotic), or neutral. Significant interactions emerged between prepubertal ACE exposure and HC use on expected (p = 0.028) and experienced (p = 0.025) valence ratings of erotic images but not pleasant or neutral images. Importantly, follow-up analyses considering whether women experienced HC-induced decreases in sexual desire informed the significant interaction for expected valence ratings of erotic images. For current HC users, prepubertal ACEs interacted with HC-induced decreased sexual desire (p = 0.008), such that high ACE women reporting decreased sexual desire on HC showed substantially decreased ratings for anticipated erotic images compared to both high prepubertal ACE women without decreased sexual desire (p < 0.001) and low prepubertal ACE women also reporting decreased sexual desire (p = 0.010). The interaction was not significant in naturally cycling women reporting previous HC use, suggesting that current HC use could be impacting anticipatory reward processing of sexual stimuli among certain women (e.g., high prepubertal ACE women reporting HC-induced decreases in sexual desire). The study provides rationale for future randomized, controlled trials to account for prepubertal ACE exposure to promote contraceptive selection informed by behavioral evidence.

Project description:UnlabelledBackgroundSocial motivation theory suggests that deficits in social reward processing underlie social impairments in autism spectrum disorders (ASD). However, the extent to which abnormalities in reward processing generalize to other classes of stimuli remains unresolved. The aim of the current study was to examine if reward processing abnormalities in ASD are specific to social stimuli or can be generalized to other classes of reward. Additionally, we sought to examine the results in the light of behavioral impairments in ASD.MethodsParticipants performed adapted versions of the social and monetary incentive delay tasks. Data from 21 unmedicated right-handed male participants with ASD and 21 age- and IQ-matched controls were analyzed using a factorial design to examine the blood-oxygen-level-dependent (BOLD) response during the anticipation and receipt of both reward types.ResultsBehaviorally, the ASD group showed less of a reduction in reaction time (RT) for rewarded compared to unrewarded trials than the control group. In terms of the fMRI results, there were no significant group differences in reward circuitry during reward anticipation. During the receipt of rewards, there was a significant interaction between group and reward type in the left dorsal striatum (DS). The ASD group showed reduced activity in the DS compared to controls for social rewards but not monetary rewards and decreased activation for social rewards compared to monetary rewards. Controls showed no significant difference between the two reward types. Increased activation in the DS during social reward processing was associated with faster response times for rewarded trials, compared to unrewarded trials, in both groups. This is in line with behavioral results indicating that the ASD group showed less of a reduction in RT for rewarded compared to unrewarded trials. Additionally, de-activation to social rewards was associated with increased repetitive behavior in ASD.ConclusionsIn line with social motivation theory, the ASD group showed reduced activation, compared to controls, during the receipt of social rewards in the DS. Groups did not differ significantly during the processing of monetary rewards. BOLD activation in the DS, during social reward processing, was associated with behavioral impairments in ASD.

Dataset Information

Social-interactive reward elicits similar neural response in autism and typical development and predicts future social experiences.

Publications

Social-interactive reward elicits similar neural response in autism and typical development and predicts future social experiences.

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