Lee Joonhee Leo, Casamento-Moran Agostina, Bastian Amy J, Cullen Kathleen E, Chib Vikram S
Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, MD 21205.
Center for Movement Studies, Kennedy Krieger Institute, Baltimore, MD 21205.
Proc Natl Acad Sci U S A. 2025 Aug 12;122(32):e2503373122. doi: 10.1073/pnas.2503373122. Epub 2025 Aug 5.
Goal-directed motor performance relies on the brain's ability to distinguish between actions that lead to successful and unsuccessful outcomes. The basal ganglia (BG) and cerebellum (CBL) are integral for processing performance outcomes, yet their functional interactions remain underexplored. We scanned participants' brains with functional magnetic imaging (fMRI) while they performed a skilled motor task for monetary rewards, where outcomes depended on their motor performance and probabilistic events that were not contingent on their performance. Successful motor outcomes increased activity in the ventral striatum (VS), a functional subregion of the BG, whereas unsuccessful motor outcomes engaged the CBL. In contrast, for probabilistic outcomes unrelated to motor performance, the BG and CBL exhibited no differences in activity between successful and unsuccessful outcomes. Dynamic causal modeling revealed that VS-to-CBL connectivity was inhibitory following successful motor outcomes, suggesting that the VS may suppress CBL error processing for correct actions. Conversely, CBL-to-VS connectivity was inhibitory after unsuccessful motor outcomes, potentially preventing reinforcement of erroneous actions. Additionally, interindividual differences in task preference, assessed by having participants choose between performing the motor task or flipping a coin for monetary rewards, were related to inhibitory VS-CBL connectivity. These findings highlight a performance-mediated functional network between the VS and CBL, modulated by motivation and subjective preferences, that supports goal-directed behavior.
目标导向的运动表现依赖于大脑区分导致成功和不成功结果的动作的能力。基底神经节(BG)和小脑(CBL)对于处理表现结果不可或缺,但其功能相互作用仍未得到充分探索。我们使用功能磁共振成像(fMRI)扫描参与者的大脑,同时他们执行一项为获得金钱奖励的熟练运动任务,其中结果取决于他们的运动表现以及与他们的表现无关的概率事件。成功的运动结果会增加腹侧纹状体(VS)的活动,VS是BG的一个功能子区域,而不成功的运动结果则会激活CBL。相比之下,对于与运动表现无关的概率结果,BG和CBL在成功和不成功结果之间的活动没有差异。动态因果模型显示,成功的运动结果后,VS到CBL的连接是抑制性的,这表明VS可能会抑制CBL对正确动作的错误处理。相反,不成功的运动结果后,CBL到VS的连接是抑制性的,这可能会阻止对错误动作的强化。此外,通过让参与者在执行运动任务或抛硬币以获得金钱奖励之间进行选择来评估的任务偏好的个体差异,与抑制性的VS - CBL连接有关。这些发现突出了VS和CBL之间由动机和主观偏好调节的表现介导的功能网络,该网络支持目标导向行为。