Erik M Elster, Ruth Pauli, Graeme Fairchild, Maria McDonald, Sarah Baumann, Justina Sidlauskaite, Stephane De Brito, Christine M Freitag, Kerstin Konrad, Veit Roessner, Inti A Brazil, Patricia L Lockwood, Gregor Kohls
{"title":"Altered Neural Responses to Punishment Learning in Conduct Disorder.","authors":"Erik M Elster, Ruth Pauli, Graeme Fairchild, Maria McDonald, Sarah Baumann, Justina Sidlauskaite, Stephane De Brito, Christine M Freitag, Kerstin Konrad, Veit Roessner, Inti A Brazil, Patricia L Lockwood, Gregor Kohls","doi":"10.1016/j.bpsc.2025.01.003","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Conduct disorder (CD) is associated with deficits in the use of punishment for reinforcement learning (RL) and subsequent decision making, contributing to reckless, antisocial, and aggressive behaviors. Here, we used functional magnetic resonance imaging (fMRI) to examine whether differences in behavioral learning rates derived from computational modeling, particularly for punishment, are reflected in aberrant neural responses in youths with CD compared with typically developing control participants (TDCs).</p><p><strong>Methods: </strong>A total of 75 youths with CD and 99 TDCs (9-18 years, 47% girls) performed a probabilistic RL task with punishment, reward, and neutral contingencies. Using fMRI data in conjunction with computational modeling indices (learning rate α), we investigated group differences for the 3 learning conditions in whole-brain and region of interest (ROI) analyses, including the ventral striatum and insula.</p><p><strong>Results: </strong>Whole-brain analysis revealed typical neural responses for RL in both groups. However, linear regression models for the ROI analyses revealed that only the response pattern of the (anterior) insula during punishment learning was different in participants with CD compared with TDCs.</p><p><strong>Conclusions: </strong>Youths with CD have atypical neural responses to learning from punishment (but not from reward), specifically in the insula. This suggests a selective dysfunction of RL mechanisms in CD that contributes to punishment insensitivity/hyposensitivity as a hallmark of the disorder. Because the (anterior) insula is involved in avoidance behaviors related to negative affect or arousal, insula dysfunction in CD may contribute to inappropriate behavioral decision making, which increases the risk for reckless, antisocial, and aggressive behaviors in affected youth.</p>","PeriodicalId":93900,"journal":{"name":"Biological psychiatry. Cognitive neuroscience and neuroimaging","volume":" ","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2025-01-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Biological psychiatry. Cognitive neuroscience and neuroimaging","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1016/j.bpsc.2025.01.003","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
Background: Conduct disorder (CD) is associated with deficits in the use of punishment for reinforcement learning (RL) and subsequent decision making, contributing to reckless, antisocial, and aggressive behaviors. Here, we used functional magnetic resonance imaging (fMRI) to examine whether differences in behavioral learning rates derived from computational modeling, particularly for punishment, are reflected in aberrant neural responses in youths with CD compared with typically developing control participants (TDCs).
Methods: A total of 75 youths with CD and 99 TDCs (9-18 years, 47% girls) performed a probabilistic RL task with punishment, reward, and neutral contingencies. Using fMRI data in conjunction with computational modeling indices (learning rate α), we investigated group differences for the 3 learning conditions in whole-brain and region of interest (ROI) analyses, including the ventral striatum and insula.
Results: Whole-brain analysis revealed typical neural responses for RL in both groups. However, linear regression models for the ROI analyses revealed that only the response pattern of the (anterior) insula during punishment learning was different in participants with CD compared with TDCs.
Conclusions: Youths with CD have atypical neural responses to learning from punishment (but not from reward), specifically in the insula. This suggests a selective dysfunction of RL mechanisms in CD that contributes to punishment insensitivity/hyposensitivity as a hallmark of the disorder. Because the (anterior) insula is involved in avoidance behaviors related to negative affect or arousal, insula dysfunction in CD may contribute to inappropriate behavioral decision making, which increases the risk for reckless, antisocial, and aggressive behaviors in affected youth.