James B Wyngaarden, Camille R Johnston, Daniel Sazhin, Jeff B Dennison, Ori Zaff, Dominic Fareri, Michael McCloskey, Lauren B Alloy, David V Smith, Johanna M Jarcho
{"title":"Corticostriatal responses to social reward are linked to trait reward sensitivity and subclinical substance use in young adults.","authors":"James B Wyngaarden, Camille R Johnston, Daniel Sazhin, Jeff B Dennison, Ori Zaff, Dominic Fareri, Michael McCloskey, Lauren B Alloy, David V Smith, Johanna M Jarcho","doi":"10.1093/scan/nsae033","DOIUrl":null,"url":null,"abstract":"<p><p>Aberrant levels of reward sensitivity have been linked to substance use disorder and are characterized by alterations in reward processing in the ventral striatum (VS). Less is known about how reward sensitivity and subclinical substance use relate to striatal function during social rewards (e.g. positive peer feedback). Testing this relation is critical for predicting risk for development of substance use disorder. In this pre-registered study, participants (N = 44) underwent fMRI while completing well-matched tasks that assess neural response to reward in social and monetary domains. Contrary to our hypotheses, aberrant reward sensitivity blunted the relationship between substance use and striatal activation during receipt of rewards, regardless of domain. Moreover, exploratory whole-brain analyses showed unique relations between substance use and social rewards in temporoparietal junction. Psychophysiological interactions demonstrated that aberrant reward sensitivity is associated with increased connectivity between the VS and ventromedial prefrontal cortex during social rewards. Finally, we found that substance use was associated with decreased connectivity between the VS and dorsomedial prefrontal cortex for social rewards, independent of reward sensitivity. These findings demonstrate nuanced relations between reward sensitivity and substance use, even among those without substance use disorder, and suggest altered reward-related engagement of cortico-VS responses as potential predictors of developing disordered behavior.</p>","PeriodicalId":94208,"journal":{"name":"Social cognitive and affective neuroscience","volume":" ","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2024-06-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11182064/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Social cognitive and affective neuroscience","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/scan/nsae033","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0
Abstract
Aberrant levels of reward sensitivity have been linked to substance use disorder and are characterized by alterations in reward processing in the ventral striatum (VS). Less is known about how reward sensitivity and subclinical substance use relate to striatal function during social rewards (e.g. positive peer feedback). Testing this relation is critical for predicting risk for development of substance use disorder. In this pre-registered study, participants (N = 44) underwent fMRI while completing well-matched tasks that assess neural response to reward in social and monetary domains. Contrary to our hypotheses, aberrant reward sensitivity blunted the relationship between substance use and striatal activation during receipt of rewards, regardless of domain. Moreover, exploratory whole-brain analyses showed unique relations between substance use and social rewards in temporoparietal junction. Psychophysiological interactions demonstrated that aberrant reward sensitivity is associated with increased connectivity between the VS and ventromedial prefrontal cortex during social rewards. Finally, we found that substance use was associated with decreased connectivity between the VS and dorsomedial prefrontal cortex for social rewards, independent of reward sensitivity. These findings demonstrate nuanced relations between reward sensitivity and substance use, even among those without substance use disorder, and suggest altered reward-related engagement of cortico-VS responses as potential predictors of developing disordered behavior.
奖赏敏感性的异常水平与药物使用障碍有关,其特征是腹侧纹状体(VS)的奖赏处理发生了改变。人们对奖赏敏感性和亚临床药物使用与社会奖赏(如同伴的积极反馈)过程中纹状体功能的关系知之甚少。测试这种关系对于预测药物使用障碍的发展风险至关重要。在这项预先登记的研究中,参与者(N=44)在完成评估神经对社交和金钱奖励的反应的匹配任务时接受了 fMRI 检查。与我们的假设相反,异常的奖赏敏感性削弱了药物使用与接受奖赏时纹状体激活之间的关系,而与任何领域无关。此外,探索性全脑分析表明,在颞顶交界处,药物使用与社会奖赏之间存在独特的关系。心理生理学交互作用表明,在社交奖励过程中,异常奖励敏感性与 VS 和腹外侧前额叶皮层之间的连接性增加有关。最后,我们发现药物使用与社交奖赏时 VS 和背内侧前额叶皮层之间的连接性降低有关,这与奖赏敏感性无关。这些研究结果表明了奖赏敏感性与药物使用之间的微妙关系,即使在没有药物使用障碍的人群中也是如此,并表明皮质-VS 反应与奖赏相关的参与改变可能是导致行为紊乱的潜在预测因素。