Madison Weinrich, Osmar P Neto, Yiyu Wang, Brock Balthazor, Deanna M Kennedy
{"title":"帕金森病和健康成人的双手协调和神经肌肉同步。","authors":"Madison Weinrich, Osmar P Neto, Yiyu Wang, Brock Balthazor, Deanna M Kennedy","doi":"10.1007/s00221-025-07061-4","DOIUrl":null,"url":null,"abstract":"<p><p>Parkinson's disease (PD) is a progressive neurodegenerative disorder that significantly impairs motor function, affecting over 1.5 million people in the U.S. PD is characterized by deficits in movement speed, force timing, and force modulation, particularly during coordinated upper limb actions. These impairments contribute to reduced functional independence and a diminished quality of life in individuals with PD. This study investigated the impact of PD on bimanual coordination, focusing on temporal accuracy, force production, and neuromuscular synchronization. The goal was to compare these parameters across individuals with PD, healthy older adults (HOA), and healthy young adults (HYA) during a stable force coordination task. Thirteen individuals with PD (median age [min-max] = 73 [60-83] years; 6 males), 13 HOAs median age [min-max] = 74 [60-84] years; 7 males), and 15 HYAs (median age [min-max] = 21 [18-23] years; 7 males) performed a 1:1 in-phase (0°) bimanual coordination task, requiring participants to rhythmically produce isometric forces with their left and right index fingers. Muscle activity from the First Dorsal Interosseus (FDI) muscles were recorded using electromyography (EMG). Each participant completed 21, 30-second trials. Temporal accuracy and stability were assessed using frequency ratio, absolute error (AE), and variability (VE) of relative phase. Force production was evaluated in terms of force harmonicity, force asymmetry, and peak force. Neuromuscular synchronization was analyzed using force-force and EMG-EMG coherence across different frequency bands. All groups achieved the target frequency ratio of 1.0, with no significant differences in AE or VE, suggesting comparable temporal accuracy and stability across groups. However, the PD group demonstrated significantly lower harmonicity, indicating less smooth force production, and greater force asymmetry compared to HOA and HYA groups. Reduced force-force coherence, especially in the 1-4 Hz and 4-8 Hz frequency bands, further highlighted challenges in bilateral force synchronization for the PD group. EMG-EMG coherence analysis revealed that the HYA group exhibited higher muscle activation synchronization, particularly in the alpha band, compared to the PD group. These findings suggest that while basic temporal coordination remains intact in PD, the disease impairs the smoothness and symmetry of force production, likely due to disrupted neural synchronization. The observed correlations between higher force coherence, greater harmonicity, and lower force asymmetry underscore the critical role of neural drive coherence in achieving smooth and symmetrical force production. However, it is important to consider the impact of medication state, since all participants were tested around their \"ON\" medication state. Understanding these impairments can inform the development of targeted interventions and rehabilitation strategies aimed at improving motor function and quality of life in individuals with PD.</p>","PeriodicalId":12268,"journal":{"name":"Experimental Brain Research","volume":"243 4","pages":"104"},"PeriodicalIF":1.7000,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Bimanual coordination and neuromuscular synchronization in Parkinson's disease and healthy adults.\",\"authors\":\"Madison Weinrich, Osmar P Neto, Yiyu Wang, Brock Balthazor, Deanna M Kennedy\",\"doi\":\"10.1007/s00221-025-07061-4\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Parkinson's disease (PD) is a progressive neurodegenerative disorder that significantly impairs motor function, affecting over 1.5 million people in the U.S. PD is characterized by deficits in movement speed, force timing, and force modulation, particularly during coordinated upper limb actions. These impairments contribute to reduced functional independence and a diminished quality of life in individuals with PD. This study investigated the impact of PD on bimanual coordination, focusing on temporal accuracy, force production, and neuromuscular synchronization. The goal was to compare these parameters across individuals with PD, healthy older adults (HOA), and healthy young adults (HYA) during a stable force coordination task. Thirteen individuals with PD (median age [min-max] = 73 [60-83] years; 6 males), 13 HOAs median age [min-max] = 74 [60-84] years; 7 males), and 15 HYAs (median age [min-max] = 21 [18-23] years; 7 males) performed a 1:1 in-phase (0°) bimanual coordination task, requiring participants to rhythmically produce isometric forces with their left and right index fingers. Muscle activity from the First Dorsal Interosseus (FDI) muscles were recorded using electromyography (EMG). Each participant completed 21, 30-second trials. Temporal accuracy and stability were assessed using frequency ratio, absolute error (AE), and variability (VE) of relative phase. Force production was evaluated in terms of force harmonicity, force asymmetry, and peak force. Neuromuscular synchronization was analyzed using force-force and EMG-EMG coherence across different frequency bands. All groups achieved the target frequency ratio of 1.0, with no significant differences in AE or VE, suggesting comparable temporal accuracy and stability across groups. However, the PD group demonstrated significantly lower harmonicity, indicating less smooth force production, and greater force asymmetry compared to HOA and HYA groups. Reduced force-force coherence, especially in the 1-4 Hz and 4-8 Hz frequency bands, further highlighted challenges in bilateral force synchronization for the PD group. EMG-EMG coherence analysis revealed that the HYA group exhibited higher muscle activation synchronization, particularly in the alpha band, compared to the PD group. These findings suggest that while basic temporal coordination remains intact in PD, the disease impairs the smoothness and symmetry of force production, likely due to disrupted neural synchronization. The observed correlations between higher force coherence, greater harmonicity, and lower force asymmetry underscore the critical role of neural drive coherence in achieving smooth and symmetrical force production. However, it is important to consider the impact of medication state, since all participants were tested around their \\\"ON\\\" medication state. Understanding these impairments can inform the development of targeted interventions and rehabilitation strategies aimed at improving motor function and quality of life in individuals with PD.</p>\",\"PeriodicalId\":12268,\"journal\":{\"name\":\"Experimental Brain Research\",\"volume\":\"243 4\",\"pages\":\"104\"},\"PeriodicalIF\":1.7000,\"publicationDate\":\"2025-04-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Experimental Brain Research\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1007/s00221-025-07061-4\",\"RegionNum\":4,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q4\",\"JCRName\":\"NEUROSCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Experimental Brain Research","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1007/s00221-025-07061-4","RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q4","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
Bimanual coordination and neuromuscular synchronization in Parkinson's disease and healthy adults.
Parkinson's disease (PD) is a progressive neurodegenerative disorder that significantly impairs motor function, affecting over 1.5 million people in the U.S. PD is characterized by deficits in movement speed, force timing, and force modulation, particularly during coordinated upper limb actions. These impairments contribute to reduced functional independence and a diminished quality of life in individuals with PD. This study investigated the impact of PD on bimanual coordination, focusing on temporal accuracy, force production, and neuromuscular synchronization. The goal was to compare these parameters across individuals with PD, healthy older adults (HOA), and healthy young adults (HYA) during a stable force coordination task. Thirteen individuals with PD (median age [min-max] = 73 [60-83] years; 6 males), 13 HOAs median age [min-max] = 74 [60-84] years; 7 males), and 15 HYAs (median age [min-max] = 21 [18-23] years; 7 males) performed a 1:1 in-phase (0°) bimanual coordination task, requiring participants to rhythmically produce isometric forces with their left and right index fingers. Muscle activity from the First Dorsal Interosseus (FDI) muscles were recorded using electromyography (EMG). Each participant completed 21, 30-second trials. Temporal accuracy and stability were assessed using frequency ratio, absolute error (AE), and variability (VE) of relative phase. Force production was evaluated in terms of force harmonicity, force asymmetry, and peak force. Neuromuscular synchronization was analyzed using force-force and EMG-EMG coherence across different frequency bands. All groups achieved the target frequency ratio of 1.0, with no significant differences in AE or VE, suggesting comparable temporal accuracy and stability across groups. However, the PD group demonstrated significantly lower harmonicity, indicating less smooth force production, and greater force asymmetry compared to HOA and HYA groups. Reduced force-force coherence, especially in the 1-4 Hz and 4-8 Hz frequency bands, further highlighted challenges in bilateral force synchronization for the PD group. EMG-EMG coherence analysis revealed that the HYA group exhibited higher muscle activation synchronization, particularly in the alpha band, compared to the PD group. These findings suggest that while basic temporal coordination remains intact in PD, the disease impairs the smoothness and symmetry of force production, likely due to disrupted neural synchronization. The observed correlations between higher force coherence, greater harmonicity, and lower force asymmetry underscore the critical role of neural drive coherence in achieving smooth and symmetrical force production. However, it is important to consider the impact of medication state, since all participants were tested around their "ON" medication state. Understanding these impairments can inform the development of targeted interventions and rehabilitation strategies aimed at improving motor function and quality of life in individuals with PD.
期刊介绍:
Founded in 1966, Experimental Brain Research publishes original contributions on many aspects of experimental research of the central and peripheral nervous system. The focus is on molecular, physiology, behavior, neurochemistry, developmental, cellular and molecular neurobiology, and experimental pathology relevant to general problems of cerebral function. The journal publishes original papers, reviews, and mini-reviews.