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 respons...
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creator | Roth, Adam M Buggeln, John H Hoh, Joanna E Wood, Jonathan M Sullivan, Seth R Ngo, Truc T Calalo, Jan A Lokesh, Rakshith Morton, Susanne M Grill, Stephen Jeka, John J Carter, Michael J Cashaback, Joshua G A |
description | 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. |
doi_str_mv | 10.1371/journal.pcbi.1012474 |
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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.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1012474</identifier><identifier>PMID: 39401183</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Aged ; Basal Ganglia - physiopathology ; Biology and Life Sciences ; Care and treatment ; Cerebellum - physiopathology ; Computational Biology ; Engineering and Technology ; Female ; Gait ; Gait - physiology ; Health aspects ; Humans ; Male ; Medicine and Health Sciences ; Middle Aged ; Parkinson Disease - physiopathology ; Parkinson Disease - rehabilitation ; Parkinson's disease ; Physical Sciences ; Psychomotor Performance - physiology ; Reinforcement, Psychology ; Research and Analysis Methods ; Reward ; Social Sciences</subject><ispartof>PLoS computational biology, 2024-10, Vol.20 (10), p.e1012474</ispartof><rights>Copyright: © 2024 Roth et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Roth et al 2024 Roth et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c377t-3a418bf03efc99f39828e0e5f987f91abe8a82cd3905f9d5282242b928295f083</cites><orcidid>0000-0002-9154-9503 ; 0000-0002-0675-4271 ; 0009-0000-2890-6312 ; 0000-0002-8642-6648 ; 0000-0002-7347-275X ; 0000-0002-8835-9696</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11472932/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11472932/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2915,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39401183$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Roth, Adam M</creatorcontrib><creatorcontrib>Buggeln, John H</creatorcontrib><creatorcontrib>Hoh, Joanna E</creatorcontrib><creatorcontrib>Wood, Jonathan M</creatorcontrib><creatorcontrib>Sullivan, Seth R</creatorcontrib><creatorcontrib>Ngo, Truc T</creatorcontrib><creatorcontrib>Calalo, Jan A</creatorcontrib><creatorcontrib>Lokesh, Rakshith</creatorcontrib><creatorcontrib>Morton, Susanne M</creatorcontrib><creatorcontrib>Grill, Stephen</creatorcontrib><creatorcontrib>Jeka, John J</creatorcontrib><creatorcontrib>Carter, Michael J</creatorcontrib><creatorcontrib>Cashaback, Joshua G A</creatorcontrib><title>Roles and interplay of reinforcement-based and error-based processes during reaching and gait in neurotypical adults and individuals with Parkinson's disease</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>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. 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Buggeln, John H ; Hoh, Joanna E ; Wood, Jonathan M ; Sullivan, Seth R ; Ngo, Truc T ; Calalo, Jan A ; Lokesh, Rakshith ; Morton, Susanne M ; Grill, Stephen ; Jeka, John J ; Carter, Michael J ; Cashaback, Joshua G A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c377t-3a418bf03efc99f39828e0e5f987f91abe8a82cd3905f9d5282242b928295f083</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Basal Ganglia - physiopathology</topic><topic>Biology and Life Sciences</topic><topic>Care and treatment</topic><topic>Cerebellum - physiopathology</topic><topic>Computational Biology</topic><topic>Engineering and Technology</topic><topic>Female</topic><topic>Gait</topic><topic>Gait - physiology</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Male</topic><topic>Medicine and Health Sciences</topic><topic>Middle Aged</topic><topic>Parkinson Disease - physiopathology</topic><topic>Parkinson Disease - rehabilitation</topic><topic>Parkinson's disease</topic><topic>Physical Sciences</topic><topic>Psychomotor Performance - physiology</topic><topic>Reinforcement, Psychology</topic><topic>Research and Analysis Methods</topic><topic>Reward</topic><topic>Social Sciences</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Roth, Adam M</creatorcontrib><creatorcontrib>Buggeln, John H</creatorcontrib><creatorcontrib>Hoh, Joanna E</creatorcontrib><creatorcontrib>Wood, Jonathan M</creatorcontrib><creatorcontrib>Sullivan, Seth R</creatorcontrib><creatorcontrib>Ngo, Truc T</creatorcontrib><creatorcontrib>Calalo, Jan A</creatorcontrib><creatorcontrib>Lokesh, Rakshith</creatorcontrib><creatorcontrib>Morton, Susanne M</creatorcontrib><creatorcontrib>Grill, Stephen</creatorcontrib><creatorcontrib>Jeka, John J</creatorcontrib><creatorcontrib>Carter, Michael J</creatorcontrib><creatorcontrib>Cashaback, Joshua G A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Roth, Adam M</au><au>Buggeln, John H</au><au>Hoh, Joanna E</au><au>Wood, Jonathan M</au><au>Sullivan, Seth R</au><au>Ngo, Truc T</au><au>Calalo, Jan A</au><au>Lokesh, Rakshith</au><au>Morton, Susanne M</au><au>Grill, Stephen</au><au>Jeka, John J</au><au>Carter, Michael J</au><au>Cashaback, Joshua G A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Roles and interplay of reinforcement-based and error-based processes during reaching and gait in neurotypical adults and individuals with Parkinson's disease</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2024-10-14</date><risdate>2024</risdate><volume>20</volume><issue>10</issue><spage>e1012474</spage><pages>e1012474-</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39401183</pmid><doi>10.1371/journal.pcbi.1012474</doi><tpages>e1012474</tpages><orcidid>https://orcid.org/0000-0002-9154-9503</orcidid><orcidid>https://orcid.org/0000-0002-0675-4271</orcidid><orcidid>https://orcid.org/0009-0000-2890-6312</orcidid><orcidid>https://orcid.org/0000-0002-8642-6648</orcidid><orcidid>https://orcid.org/0000-0002-7347-275X</orcidid><orcidid>https://orcid.org/0000-0002-8835-9696</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Aged Basal Ganglia - physiopathology Biology and Life Sciences Care and treatment Cerebellum - physiopathology Computational Biology Engineering and Technology Female Gait Gait - physiology Health aspects Humans Male Medicine and Health Sciences Middle Aged Parkinson Disease - physiopathology Parkinson Disease - rehabilitation Parkinson's disease Physical Sciences Psychomotor Performance - physiology Reinforcement, Psychology Research and Analysis Methods Reward Social Sciences |
title | Roles and interplay of reinforcement-based and error-based processes during reaching and gait in neurotypical adults and individuals with Parkinson's disease |
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