Saar Lanir-Azaria, Rakefet Chishinski, Riva Tauman, Yuval Nir, Nir Giladi
{"title":"睡眠能提高年轻人、老年人和帕金森病患者的泛化运动学习的准确性,但不能提高速度。","authors":"Saar Lanir-Azaria, Rakefet Chishinski, Riva Tauman, Yuval Nir, Nir Giladi","doi":"10.3389/fnbeh.2024.1466696","DOIUrl":null,"url":null,"abstract":"<p><p>An essential aspect of motor learning is generalizing procedural knowledge to facilitate skill acquisition across diverse conditions. Here, we examined the development of generalized motor learning during initial practice-dependent learning, and how distinct components of learning are consolidated over longer timescales during wakefulness or sleep. In the first experiment, a group of young healthy volunteers engaged in a novel motor sequence task over 36 h in a two-arm experimental design (either morning-evening-morning, or evening-morning-evening) aimed at controlling for circadian confounders. The findings unveiled an immediate, rapid generalization of sequential learning, accompanied by an additional long-timescale performance gain. Sleep modulated accuracy, but not speed, above and beyond equivalent wake intervals. To further elucidate the role of sleep across ages and under neurodegenerative disorders, a second experiment utilized the same task in a group of early-stage, drug-naïve individuals with Parkinson's disease and in healthy individuals of comparable age. Participants with Parkinson's disease exhibited comparable performance to their healthy age-matched group with the exception of reduced performance in recalling motor sequences, revealing a disease-related cognitive shortfall. In line with the results found in young subjects, both groups exhibited improved accuracy, but not speed, following a night of sleep. This result emphasizes the role of sleep in skill acquisition and provides a potential framework for deeper investigation of the intricate relationship between sleep, aging, Parkinson's disease, and motor learning.</p>","PeriodicalId":12368,"journal":{"name":"Frontiers in Behavioral Neuroscience","volume":null,"pages":null},"PeriodicalIF":2.6000,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11464313/pdf/","citationCount":"0","resultStr":"{\"title\":\"Sleep improves accuracy, but not speed, of generalized motor learning in young and older adults and in individuals with Parkinson's disease.\",\"authors\":\"Saar Lanir-Azaria, Rakefet Chishinski, Riva Tauman, Yuval Nir, Nir Giladi\",\"doi\":\"10.3389/fnbeh.2024.1466696\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>An essential aspect of motor learning is generalizing procedural knowledge to facilitate skill acquisition across diverse conditions. Here, we examined the development of generalized motor learning during initial practice-dependent learning, and how distinct components of learning are consolidated over longer timescales during wakefulness or sleep. In the first experiment, a group of young healthy volunteers engaged in a novel motor sequence task over 36 h in a two-arm experimental design (either morning-evening-morning, or evening-morning-evening) aimed at controlling for circadian confounders. The findings unveiled an immediate, rapid generalization of sequential learning, accompanied by an additional long-timescale performance gain. Sleep modulated accuracy, but not speed, above and beyond equivalent wake intervals. To further elucidate the role of sleep across ages and under neurodegenerative disorders, a second experiment utilized the same task in a group of early-stage, drug-naïve individuals with Parkinson's disease and in healthy individuals of comparable age. Participants with Parkinson's disease exhibited comparable performance to their healthy age-matched group with the exception of reduced performance in recalling motor sequences, revealing a disease-related cognitive shortfall. In line with the results found in young subjects, both groups exhibited improved accuracy, but not speed, following a night of sleep. This result emphasizes the role of sleep in skill acquisition and provides a potential framework for deeper investigation of the intricate relationship between sleep, aging, Parkinson's disease, and motor learning.</p>\",\"PeriodicalId\":12368,\"journal\":{\"name\":\"Frontiers in Behavioral Neuroscience\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":2.6000,\"publicationDate\":\"2024-09-26\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11464313/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Frontiers in Behavioral Neuroscience\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.3389/fnbeh.2024.1466696\",\"RegionNum\":3,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/1/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q2\",\"JCRName\":\"BEHAVIORAL SCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Behavioral Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.3389/fnbeh.2024.1466696","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/1/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"BEHAVIORAL SCIENCES","Score":null,"Total":0}
Sleep improves accuracy, but not speed, of generalized motor learning in young and older adults and in individuals with Parkinson's disease.
An essential aspect of motor learning is generalizing procedural knowledge to facilitate skill acquisition across diverse conditions. Here, we examined the development of generalized motor learning during initial practice-dependent learning, and how distinct components of learning are consolidated over longer timescales during wakefulness or sleep. In the first experiment, a group of young healthy volunteers engaged in a novel motor sequence task over 36 h in a two-arm experimental design (either morning-evening-morning, or evening-morning-evening) aimed at controlling for circadian confounders. The findings unveiled an immediate, rapid generalization of sequential learning, accompanied by an additional long-timescale performance gain. Sleep modulated accuracy, but not speed, above and beyond equivalent wake intervals. To further elucidate the role of sleep across ages and under neurodegenerative disorders, a second experiment utilized the same task in a group of early-stage, drug-naïve individuals with Parkinson's disease and in healthy individuals of comparable age. Participants with Parkinson's disease exhibited comparable performance to their healthy age-matched group with the exception of reduced performance in recalling motor sequences, revealing a disease-related cognitive shortfall. In line with the results found in young subjects, both groups exhibited improved accuracy, but not speed, following a night of sleep. This result emphasizes the role of sleep in skill acquisition and provides a potential framework for deeper investigation of the intricate relationship between sleep, aging, Parkinson's disease, and motor learning.
期刊介绍:
Frontiers in Behavioral Neuroscience is a leading journal in its field, publishing rigorously peer-reviewed research that advances our understanding of the neural mechanisms underlying behavior. Field Chief Editor Nuno Sousa at the Instituto de Pesquisa em Ciências da Vida e da Saúde (ICVS) is supported by an outstanding Editorial Board of international experts. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics, clinicians and the public worldwide.
This journal publishes major insights into the neural mechanisms of animal and human behavior, and welcomes articles studying the interplay between behavior and its neurobiological basis at all levels: from molecular biology and genetics, to morphological, biochemical, neurochemical, electrophysiological, neuroendocrine, pharmacological, and neuroimaging studies.