Zhe Liu, Robert Reiner, Yonatan Loewenstein, Eran Lottem
{"title":"Value modulation of self-defeating impulsivity.","authors":"Zhe Liu, Robert Reiner, Yonatan Loewenstein, Eran Lottem","doi":"10.1016/j.biopsych.2024.09.017","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Impulse control is a critical aspect of cognitive functioning. Intuitively, whether an action is executed prematurely depends on its associated reward, yet the link between value and impulsivity remains poorly understood. Three frameworks for impulsivity offer contrasting views: impulsive behavior may be valuable because it is associated with hidden internal reward (e.g., reduction of mental effort). Alternatively, it can emerge from exploration, which is disadvantageous in the short term, but can yield long-term benefits. Finally, impulsivity may reflect Pavlovian bias, an inherent tendency that occurs even when its outcome is negative.</p><p><strong>Methods: </strong>To test these hypotheses, we trained seventeen male mice to withhold licking while anticipating variable rewards. We then measured and optogenetically manipulated dopamine release in the ventral striatum.</p><p><strong>Results: </strong>We found that higher reward magnitudes correlated with increased impulsivity. This behavior was well explained by a Pavlovian-bias model. Furthermore, we observed negative dopamine signals during premature licking, suggesting that in this task, impulsivity is not merely an unsuccessful attempt at obtaining a reward. Rather, it is a failure to overcome the urge to act prematurely despite knowledge of the negative consequences of such impulsive action.</p><p><strong>Conclusion: </strong>Our findings underscore the integral role value plays in regulating impulsivity and suggest that the dopaminergic system influences impulsivity through the mediation of value learning.</p>","PeriodicalId":8918,"journal":{"name":"Biological Psychiatry","volume":null,"pages":null},"PeriodicalIF":9.6000,"publicationDate":"2024-09-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Biological Psychiatry","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1016/j.biopsych.2024.09.017","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Background: Impulse control is a critical aspect of cognitive functioning. Intuitively, whether an action is executed prematurely depends on its associated reward, yet the link between value and impulsivity remains poorly understood. Three frameworks for impulsivity offer contrasting views: impulsive behavior may be valuable because it is associated with hidden internal reward (e.g., reduction of mental effort). Alternatively, it can emerge from exploration, which is disadvantageous in the short term, but can yield long-term benefits. Finally, impulsivity may reflect Pavlovian bias, an inherent tendency that occurs even when its outcome is negative.
Methods: To test these hypotheses, we trained seventeen male mice to withhold licking while anticipating variable rewards. We then measured and optogenetically manipulated dopamine release in the ventral striatum.
Results: We found that higher reward magnitudes correlated with increased impulsivity. This behavior was well explained by a Pavlovian-bias model. Furthermore, we observed negative dopamine signals during premature licking, suggesting that in this task, impulsivity is not merely an unsuccessful attempt at obtaining a reward. Rather, it is a failure to overcome the urge to act prematurely despite knowledge of the negative consequences of such impulsive action.
Conclusion: Our findings underscore the integral role value plays in regulating impulsivity and suggest that the dopaminergic system influences impulsivity through the mediation of value learning.
期刊介绍:
Biological Psychiatry is an official journal of the Society of Biological Psychiatry and was established in 1969. It is the first journal in the Biological Psychiatry family, which also includes Biological Psychiatry: Cognitive Neuroscience and Neuroimaging and Biological Psychiatry: Global Open Science. The Society's main goal is to promote excellence in scientific research and education in the fields related to the nature, causes, mechanisms, and treatments of disorders pertaining to thought, emotion, and behavior. To fulfill this mission, Biological Psychiatry publishes peer-reviewed, rapid-publication articles that present new findings from original basic, translational, and clinical mechanistic research, ultimately advancing our understanding of psychiatric disorders and their treatment. The journal also encourages the submission of reviews and commentaries on current research and topics of interest.