Modeling impulsivity and risk aversion in the subthalamic nucleus with deep brain stimulation

Valerie Voon, Luis Manssuer, Yi-Jie Zhao, Qiong Ding, Ying Zhao, Linbin Wang, Tao Wang, Peng Huang, Yixin Pan, Bomin Sun, Dianyou Li
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Abstract

Risk evaluation is ubiquitous in decisions. Deep brain stimulation of the subthalamic nucleus is effective for Parkinson’s disease and obsessive–compulsive disorder, and can be associated with impulsivity and hypomania. Subthalamic stimulation has seemingly contrasting effects on impulsivity enhancing conflict-induced impulsivity but decreasing risk taking. Here, using a card gambling task paired with intracranial recordings (n = 25) and within-subject case control acute stimulation (n = 15) of the right subthalamic nucleus, we dissociated objective risk and uncertainty and subjective physiological markers of risk. Acute stimulation decreased risk taking (P = 0.010, Cohen’s d = 0.72) and increased subthalamic theta activity (P < 0.001, Cohen’s d = 0.72). Critically, stimulation negatively shifted the relationship between subthalamic physiology and a measure of evidence accumulation similar to observations with stimulation-induced conflict processing. This highlights the phenotypic and physiological heterogeneity of impulsivity, yet linking mechanisms underlying stimulation-induced conflict and risk. Finally, stimulation-induced risk seeking implicates the ventral subthalamic nucleus and dissociating anatomical and functional connectivity with the mesial prefrontal cortex. Our findings have implications for conceptualizations of impulsivity, and clinical relevance for neuropsychiatric disorders. Using a card gambling task paired with intracranial recordings and deep brain stimulation of the right subthalamic nucleus, the authors dissociate objective and subjective markers of risk taking and demonstrate the role of stimulation localization on risk-related behavior.

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用深部脑刺激模拟丘脑下核的冲动性和风险规避性
风险评估在决策中无处不在。对丘脑下核的深部脑刺激对帕金森病和强迫症有效,但也可能与冲动和躁狂症有关。刺激丘脑下核对冲动性的影响似乎截然不同,它能增强冲突诱发的冲动性,但却会降低冒险性。在这里,我们使用了一项与颅内记录(n = 25)和对右丘下核急性刺激(n = 15)的受试者内病例对照相匹配的纸牌赌博任务,将客观风险和不确定性与风险的主观生理标记区分开来。急性刺激降低了风险承担(P = 0.010,Cohen's d = 0.72),增加了丘脑下θ活动(P < 0.001,Cohen's d = 0.72)。重要的是,刺激负向改变了丘脑下生理学与证据积累测量之间的关系,这与刺激诱发冲突处理的观察结果类似。这凸显了冲动的表型和生理异质性,同时也将刺激诱发冲突和风险的内在机制联系起来。最后,刺激诱发的风险寻求牵涉到腹侧丘脑下核以及与中侧前额叶皮层的解剖和功能连接。我们的研究结果对冲动的概念化和神经精神疾病的临床相关性都有影响。作者利用颅内记录和对右侧丘脑下核的深部脑刺激来完成一项纸牌赌博任务,将风险承担的客观和主观标记区分开来,并证明了刺激定位对风险相关行为的作用。
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