François Hug, François Dernoncourt, Simon Avrillon, Jacob Thorstensen, Manuela Besomi, Wolbert van den Hoorn, Kylie Tucker
{"title":"Non-homogeneous distribution of inhibitory inputs among motor units in response to nociceptive stimulation at moderate contraction intensity","authors":"François Hug, François Dernoncourt, Simon Avrillon, Jacob Thorstensen, Manuela Besomi, Wolbert van den Hoorn, Kylie Tucker","doi":"10.1113/JP288504","DOIUrl":null,"url":null,"abstract":"<div>\n \n <section>\n \n \n <div>Pain significantly influences movement, yet the neural mechanisms underlying the range of observed motor adaptations remain unclear. This study combined experimental data and <i>in silico</i> models to investigate the contribution of inhibitory and neuromodulatory inputs to motor unit behaviour in response to nociceptive stimulation during contractions at 30% of maximal torque. Specifically, we aimed to unravel the distribution pattern of inhibitory inputs to the motor unit pool. Seventeen participants performed isometric knee extension tasks under three conditions: Control, Pain (induced by injecting hypertonic saline into the infra-patellar fat pad) and Washout. We identified large samples of motor units in the vastus lateralis (up to 53/participant) from high-density electromyographic signals, leading to three key observations. First, while motor unit discharge rates significantly decreased during Pain, a substantial proportion of motor units (14.8–24.8%) did not show this decrease and, in some cases, even exhibited an increase. Second, using complementary approaches, we found that pain did not significantly affect neuromodulation, making it unlikely to be a major contributor to the observed changes in motor unit behaviour. Third, we observed a significant reduction in the proportion of common inputs to motor units during Pain. To explore potential neurophysiological mechanisms underlying these results, we simulated the behaviour of motor unit pools with varying distribution patterns of inhibitory inputs. Our simulations support the hypothesis that a non-homogeneous distribution of inhibitory inputs, not strictly organised according to motor unit size, is a key mechanism underlying the motor response to nociceptive stimulation during moderate contraction intensity.\n\n <figure>\n <div><picture>\n <source></source></picture><p></p>\n </div>\n </figure>\n </div>\n </section>\n \n <section>\n \n <h3> Key points</h3>\n \n <div>\n <ul>\n \n <li>Pain affects movement, but the neural mechanisms underlying these motor adaptations are not well defined.</li>\n \n <li>The traditional view is that pain causes uniform (homogeneous) inhibition among motor units.</li>\n \n <li>Recent research has observed differential motor unit responses to experimental pain – some with decreased discharge rates and others with increased discharge rates.</li>\n \n <li>Combining experimental data with modelling, we provide compelling evidence of increased inhibition that is non-uniformly distributed across motor units, regardless of their size.</li>\n </ul>\n </div>\n </section>\n </div>","PeriodicalId":50088,"journal":{"name":"Journal of Physiology-London","volume":"603 11","pages":"3445-3461"},"PeriodicalIF":4.7000,"publicationDate":"2025-05-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1113/JP288504","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Physiology-London","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1113/JP288504","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Pain significantly influences movement, yet the neural mechanisms underlying the range of observed motor adaptations remain unclear. This study combined experimental data and in silico models to investigate the contribution of inhibitory and neuromodulatory inputs to motor unit behaviour in response to nociceptive stimulation during contractions at 30% of maximal torque. Specifically, we aimed to unravel the distribution pattern of inhibitory inputs to the motor unit pool. Seventeen participants performed isometric knee extension tasks under three conditions: Control, Pain (induced by injecting hypertonic saline into the infra-patellar fat pad) and Washout. We identified large samples of motor units in the vastus lateralis (up to 53/participant) from high-density electromyographic signals, leading to three key observations. First, while motor unit discharge rates significantly decreased during Pain, a substantial proportion of motor units (14.8–24.8%) did not show this decrease and, in some cases, even exhibited an increase. Second, using complementary approaches, we found that pain did not significantly affect neuromodulation, making it unlikely to be a major contributor to the observed changes in motor unit behaviour. Third, we observed a significant reduction in the proportion of common inputs to motor units during Pain. To explore potential neurophysiological mechanisms underlying these results, we simulated the behaviour of motor unit pools with varying distribution patterns of inhibitory inputs. Our simulations support the hypothesis that a non-homogeneous distribution of inhibitory inputs, not strictly organised according to motor unit size, is a key mechanism underlying the motor response to nociceptive stimulation during moderate contraction intensity.
Key points
Pain affects movement, but the neural mechanisms underlying these motor adaptations are not well defined.
The traditional view is that pain causes uniform (homogeneous) inhibition among motor units.
Recent research has observed differential motor unit responses to experimental pain – some with decreased discharge rates and others with increased discharge rates.
Combining experimental data with modelling, we provide compelling evidence of increased inhibition that is non-uniformly distributed across motor units, regardless of their size.
期刊介绍:
The Journal of Physiology publishes full-length original Research Papers and Techniques for Physiology, which are short papers aimed at disseminating new techniques for physiological research. Articles solicited by the Editorial Board include Perspectives, Symposium Reports and Topical Reviews, which highlight areas of special physiological interest. CrossTalk articles are short editorial-style invited articles framing a debate between experts in the field on controversial topics. Letters to the Editor and Journal Club articles are also published. All categories of papers are subjected to peer reivew.
The Journal of Physiology welcomes submitted research papers in all areas of physiology. Authors should present original work that illustrates new physiological principles or mechanisms. Papers on work at the molecular level, at the level of the cell membrane, single cells, tissues or organs and on systems physiology are all acceptable. Theoretical papers and papers that use computational models to further our understanding of physiological processes will be considered if based on experimentally derived data and if the hypothesis advanced is directly amenable to experimental testing. While emphasis is on human and mammalian physiology, work on lower vertebrate or invertebrate preparations may be suitable if it furthers the understanding of the functioning of other organisms including mammals.