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
{"title":"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。","authors":"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","doi":"10.1371/journal.pcbi.1012474","DOIUrl":null,"url":null,"abstract":"<p><p>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.</p>","PeriodicalId":20241,"journal":{"name":"PLoS Computational Biology","volume":null,"pages":null},"PeriodicalIF":3.8000,"publicationDate":"2024-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11472932/pdf/","citationCount":"0","resultStr":"{\"title\":\"Roles and interplay of reinforcement-based and error-based processes during reaching and gait in neurotypical adults and individuals with Parkinson's disease.\",\"authors\":\"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\",\"doi\":\"10.1371/journal.pcbi.1012474\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>From a game of darts to neurorehabilitation, the ability to explore and fine tune our movements is critical for success. 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Roles and interplay of reinforcement-based and error-based processes during reaching and gait in neurotypical adults and individuals with Parkinson's disease.
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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