Roles and interplay of reinforcement-based and error-based processes during reaching and gait in neurotypical adults and individuals with Parkinson's disease.

IF 3.8 2区 生物学 Q1 BIOCHEMICAL RESEARCH METHODS PLoS Computational Biology Pub Date : 2024-10-14 eCollection Date: 2024-10-01 DOI:10.1371/journal.pcbi.1012474
Adam M Roth, John H Buggeln, Joanna E Hoh, Jonathan M Wood, Seth R Sullivan, Truc T Ngo, Jan A Calalo, Rakshith Lokesh, Susanne M Morton, Stephen Grill, John J Jeka, Michael J Carter, Joshua G A Cashaback
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Abstract

From a game of darts to neurorehabilitation, the ability to explore and fine tune our movements is critical for success. Past work has shown that exploratory motor behaviour in response to reinforcement (reward) feedback is closely linked with the basal ganglia, while movement corrections in response to error feedback is commonly attributed to the cerebellum. While our past work has shown these processes are dissociable during adaptation, it is unknown how they uniquely impact exploratory behaviour. Moreover, converging neuroanatomical evidence shows direct and indirect connections between the basal ganglia and cerebellum, suggesting that there is an interaction between reinforcement-based and error-based neural processes. Here we examine the unique roles and interaction between reinforcement-based and error-based processes on sensorimotor exploration in a neurotypical population. We also recruited individuals with Parkinson's disease to gain mechanistic insight into the role of the basal ganglia and associated reinforcement pathways in sensorimotor exploration. Across three reaching experiments, participants were given either reinforcement feedback, error feedback, or simultaneously both reinforcement & error feedback during a sensorimotor task that encouraged exploration. Our reaching results, a re-analysis of a previous gait experiment, and our model suggests that in isolation, reinforcement-based and error-based processes respectively boost and suppress exploration. When acting in concert, we found that reinforcement-based and error-based processes interact by mutually opposing one another. Finally, we found that those with Parkinson's disease had decreased exploration when receiving reinforcement feedback, supporting the notion that compromised reinforcement-based processes reduces the ability to explore new motor actions. Understanding the unique and interacting roles of reinforcement-based and error-based processes may help to inform neurorehabilitation paradigms where it is important to discover new and successful motor actions.

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神经畸形成人和帕金森病患者在伸手和步态过程中基于强化和基于错误的过程的作用和相互作用。
从飞镖游戏到神经康复,探索和微调运动的能力对于成功至关重要。过去的工作表明,针对强化(奖励)反馈的探索性运动行为与基底神经节密切相关,而针对错误反馈的运动修正通常归因于小脑。虽然我们过去的研究表明,这些过程在适应过程中是可以分离的,但它们如何对探索行为产生独特的影响,目前还不得而知。此外,神经解剖学证据显示,基底神经节和小脑之间存在直接和间接的联系,这表明基于强化和基于错误的神经过程之间存在相互作用。在这里,我们研究了神经畸形人群中基于强化和基于错误的神经过程在感觉运动探索中的独特作用和相互作用。我们还招募了帕金森病患者,以便从机理上深入了解基底神经节和相关强化通路在感觉运动探索中的作用。在三项伸手实验中,参与者在完成鼓励探索的感觉运动任务时分别获得强化反馈、错误反馈或同时获得强化和错误反馈。我们的伸手实验结果、对之前步态实验的重新分析以及我们的模型表明,在孤立的情况下,基于强化的过程和基于错误的过程会分别促进和抑制探索。当两者共同作用时,我们发现强化过程和错误过程会相互影响,相互抵消。最后,我们发现帕金森病患者在接受强化反馈时探索能力下降,这支持了强化过程受损会降低探索新运动动作能力的观点。了解强化过程和错误过程的独特作用和相互作用可能有助于为神经康复范例提供信息,因为在神经康复范例中,发现新的和成功的运动动作非常重要。
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来源期刊
PLoS Computational Biology
PLoS Computational Biology BIOCHEMICAL RESEARCH METHODS-MATHEMATICAL & COMPUTATIONAL BIOLOGY
CiteScore
7.10
自引率
4.70%
发文量
820
审稿时长
2.5 months
期刊介绍: PLOS Computational Biology features works of exceptional significance that further our understanding of living systems at all scales—from molecules and cells, to patient populations and ecosystems—through the application of computational methods. Readers include life and computational scientists, who can take the important findings presented here to the next level of discovery. Research articles must be declared as belonging to a relevant section. More information about the sections can be found in the submission guidelines. Research articles should model aspects of biological systems, demonstrate both methodological and scientific novelty, and provide profound new biological insights. Generally, reliability and significance of biological discovery through computation should be validated and enriched by experimental studies. Inclusion of experimental validation is not required for publication, but should be referenced where possible. Inclusion of experimental validation of a modest biological discovery through computation does not render a manuscript suitable for PLOS Computational Biology. Research articles specifically designated as Methods papers should describe outstanding methods of exceptional importance that have been shown, or have the promise to provide new biological insights. The method must already be widely adopted, or have the promise of wide adoption by a broad community of users. Enhancements to existing published methods will only be considered if those enhancements bring exceptional new capabilities.
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