Simon Thibault, John B Yates, Laurel J Buxbaum, Aaron L Wong
{"title":"工具运动与手部运动的竞争损害肢体失用症患者的运动计划。","authors":"Simon Thibault, John B Yates, Laurel J Buxbaum, Aaron L Wong","doi":"10.1523/JNEUROSCI.0692-25.2025","DOIUrl":null,"url":null,"abstract":"<p><p>Tool use is a complex motor planning problem. Prior research suggests that planning to use tools involves resolving competition between different tool-related action representations. We therefore reasoned that competition may also be exacerbated with tools for which the motions of the tool and the hand are incongruent (e.g., pinching the fingers to open a clothespin). If this hypothesis is correct, we should observe marked deficits in planning the use of incongruent as compared to congruent tools in individuals with limb apraxia following left-hemisphere stroke (LCVA), a disorder associated with abnormal action competition. We asked 34 individuals with chronic LCVA (14 females) and 16 matched neurotypical controls (8 females) to use novel tools in which the correspondence between the motions of the hand and tool-tip were either congruent or incongruent. Individuals with LCVA also completed background assessments to quantify apraxia severity. We observed increased planning time for incongruent as compared to congruent tools as a function of apraxia severity. Further analysis revealed that this impairment predominantly occurred early in the task when the tools were first introduced. Lesion-symptom mapping analyses revealed that lesions to posterior temporal and inferior parietal areas were associated with impaired planning for incongruent tools. A second experiment on the same individuals with LCVA revealed that the ability to gesture the use of conventional tools was impaired for tools rated as more incongruent by a normative sample. These findings suggest that tool-hand incongruence evokes action competition and influences the tool-use difficulties experienced by people with apraxia.<b>Significance Statement</b> Prior research indicates that competition between different representations associated with moving or using tools must be resolved to enable tool use. We demonstrated that competition may be exacerbated when tool and hand motions are incongruent (e.g., pinching the hand opens a clothespin), resulting in tool-use impairments particularly for individuals with greater severity of limb apraxia, a disorder known to be associated with action competition abnormalities. Lesions in posterior portions of the brain's tool use network were associated with impairments in planning incongruent tool actions. This study thus demonstrates that tool-hand incongruence may invoke competition between motions of the hand and tool-tip, which individuals with limb apraxia have difficulty resolving to properly use tools.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0000,"publicationDate":"2025-09-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Competition between tool and hand motion impairs movement planning in limb apraxia.\",\"authors\":\"Simon Thibault, John B Yates, Laurel J Buxbaum, Aaron L Wong\",\"doi\":\"10.1523/JNEUROSCI.0692-25.2025\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Tool use is a complex motor planning problem. Prior research suggests that planning to use tools involves resolving competition between different tool-related action representations. We therefore reasoned that competition may also be exacerbated with tools for which the motions of the tool and the hand are incongruent (e.g., pinching the fingers to open a clothespin). If this hypothesis is correct, we should observe marked deficits in planning the use of incongruent as compared to congruent tools in individuals with limb apraxia following left-hemisphere stroke (LCVA), a disorder associated with abnormal action competition. We asked 34 individuals with chronic LCVA (14 females) and 16 matched neurotypical controls (8 females) to use novel tools in which the correspondence between the motions of the hand and tool-tip were either congruent or incongruent. Individuals with LCVA also completed background assessments to quantify apraxia severity. We observed increased planning time for incongruent as compared to congruent tools as a function of apraxia severity. Further analysis revealed that this impairment predominantly occurred early in the task when the tools were first introduced. Lesion-symptom mapping analyses revealed that lesions to posterior temporal and inferior parietal areas were associated with impaired planning for incongruent tools. A second experiment on the same individuals with LCVA revealed that the ability to gesture the use of conventional tools was impaired for tools rated as more incongruent by a normative sample. These findings suggest that tool-hand incongruence evokes action competition and influences the tool-use difficulties experienced by people with apraxia.<b>Significance Statement</b> Prior research indicates that competition between different representations associated with moving or using tools must be resolved to enable tool use. We demonstrated that competition may be exacerbated when tool and hand motions are incongruent (e.g., pinching the hand opens a clothespin), resulting in tool-use impairments particularly for individuals with greater severity of limb apraxia, a disorder known to be associated with action competition abnormalities. Lesions in posterior portions of the brain's tool use network were associated with impairments in planning incongruent tool actions. This study thus demonstrates that tool-hand incongruence may invoke competition between motions of the hand and tool-tip, which individuals with limb apraxia have difficulty resolving to properly use tools.</p>\",\"PeriodicalId\":50114,\"journal\":{\"name\":\"Journal of Neuroscience\",\"volume\":\" \",\"pages\":\"\"},\"PeriodicalIF\":4.0000,\"publicationDate\":\"2025-09-09\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of Neuroscience\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1523/JNEUROSCI.0692-25.2025\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"NEUROSCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/JNEUROSCI.0692-25.2025","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
Competition between tool and hand motion impairs movement planning in limb apraxia.
Tool use is a complex motor planning problem. Prior research suggests that planning to use tools involves resolving competition between different tool-related action representations. We therefore reasoned that competition may also be exacerbated with tools for which the motions of the tool and the hand are incongruent (e.g., pinching the fingers to open a clothespin). If this hypothesis is correct, we should observe marked deficits in planning the use of incongruent as compared to congruent tools in individuals with limb apraxia following left-hemisphere stroke (LCVA), a disorder associated with abnormal action competition. We asked 34 individuals with chronic LCVA (14 females) and 16 matched neurotypical controls (8 females) to use novel tools in which the correspondence between the motions of the hand and tool-tip were either congruent or incongruent. Individuals with LCVA also completed background assessments to quantify apraxia severity. We observed increased planning time for incongruent as compared to congruent tools as a function of apraxia severity. Further analysis revealed that this impairment predominantly occurred early in the task when the tools were first introduced. Lesion-symptom mapping analyses revealed that lesions to posterior temporal and inferior parietal areas were associated with impaired planning for incongruent tools. A second experiment on the same individuals with LCVA revealed that the ability to gesture the use of conventional tools was impaired for tools rated as more incongruent by a normative sample. These findings suggest that tool-hand incongruence evokes action competition and influences the tool-use difficulties experienced by people with apraxia.Significance Statement Prior research indicates that competition between different representations associated with moving or using tools must be resolved to enable tool use. We demonstrated that competition may be exacerbated when tool and hand motions are incongruent (e.g., pinching the hand opens a clothespin), resulting in tool-use impairments particularly for individuals with greater severity of limb apraxia, a disorder known to be associated with action competition abnormalities. Lesions in posterior portions of the brain's tool use network were associated with impairments in planning incongruent tool actions. This study thus demonstrates that tool-hand incongruence may invoke competition between motions of the hand and tool-tip, which individuals with limb apraxia have difficulty resolving to properly use tools.
期刊介绍:
JNeurosci (ISSN 0270-6474) is an official journal of the Society for Neuroscience. It is published weekly by the Society, fifty weeks a year, one volume a year. JNeurosci publishes papers on a broad range of topics of general interest to those working on the nervous system. Authors now have an Open Choice option for their published articles