Benjamin Haverland, Lena S Timmsen, Silke Wolf, Charlotte J Stagg, Lukas Frontzkowski, Robert Oostenveld, Gerhard Schön, Jan Feldheim, Focko L Higgen, Christian Gerloff, Robert Schulz, Till R Schneider, Bettina C Schwab, Fanny Quandt
{"title":"Human cortical high-gamma power scales with movement rate in healthy participants and stroke survivors.","authors":"Benjamin Haverland, Lena S Timmsen, Silke Wolf, Charlotte J Stagg, Lukas Frontzkowski, Robert Oostenveld, Gerhard Schön, Jan Feldheim, Focko L Higgen, Christian Gerloff, Robert Schulz, Till R Schneider, Bettina C Schwab, Fanny Quandt","doi":"10.1113/JP286873","DOIUrl":null,"url":null,"abstract":"<p><p>Motor cortical high-gamma oscillations (60-90 Hz) occur at movement onset and are spatially focused over the contralateral primary motor cortex. Although high-gamma oscillations are widely recognized for their significance in human motor control, their precise function on a cortical level remains elusive. Importantly, their relevance in human stroke pathophysiology is unknown. Because motor deficits are fundamental determinants of symptom burden after stroke, understanding the neurophysiological processes of motor coding could be an important step in improving stroke rehabilitation. We recorded magnetoencephalography data during a thumb movement rate task in 14 chronic stroke survivors, 15 age-matched control participants and 29 healthy young participants. Motor cortical high-gamma oscillations showed a strong relation with movement rate as trials with higher movement rate were associated with greater high-gamma power. Although stroke survivors showed reduced cortical high-gamma power, this reduction primarily reflected the scaling of high-gamma power with movement rate, yet after matching movement rate in stroke survivors and age-matched controls, the reduction of high-gamma power exceeded the effect of their decreased movement rate alone. Even though motor skill acquisition was evident in all three groups, it was not linked to high-gamma power. Our study quantifies high-gamma oscillations after stroke, revealing a reduction in movement-related high-gamma power. Moreover, we provide strong evidence for a pivotal role of motor cortical high-gamma oscillations in encoding movement rate. KEY POINTS: Neural oscillations in the high-gamma frequency range (60-90 Hz) emerge in the human motor cortex during movement. The precise function of these oscillations in motor control remains unclear, and they have never been characterized in stroke survivors. In a magnetoencephalography study, we demonstrate that high-gamma oscillations in motor cortical areas scale with movement rate, and we further explore their temporal and spatial characteristics. Stroke survivors exhibit lower high-gamma power during movement than age-matched control participants, even after matching for movement rate. The results contribute to the understanding of the role of high-gamma oscillations in motor control and have important implications for neuromodulation in stroke rehabilitation.</p>","PeriodicalId":50088,"journal":{"name":"Journal of Physiology-London","volume":" ","pages":""},"PeriodicalIF":4.7000,"publicationDate":"2025-01-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Physiology-London","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1113/JP286873","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
Motor cortical high-gamma oscillations (60-90 Hz) occur at movement onset and are spatially focused over the contralateral primary motor cortex. Although high-gamma oscillations are widely recognized for their significance in human motor control, their precise function on a cortical level remains elusive. Importantly, their relevance in human stroke pathophysiology is unknown. Because motor deficits are fundamental determinants of symptom burden after stroke, understanding the neurophysiological processes of motor coding could be an important step in improving stroke rehabilitation. We recorded magnetoencephalography data during a thumb movement rate task in 14 chronic stroke survivors, 15 age-matched control participants and 29 healthy young participants. Motor cortical high-gamma oscillations showed a strong relation with movement rate as trials with higher movement rate were associated with greater high-gamma power. Although stroke survivors showed reduced cortical high-gamma power, this reduction primarily reflected the scaling of high-gamma power with movement rate, yet after matching movement rate in stroke survivors and age-matched controls, the reduction of high-gamma power exceeded the effect of their decreased movement rate alone. Even though motor skill acquisition was evident in all three groups, it was not linked to high-gamma power. Our study quantifies high-gamma oscillations after stroke, revealing a reduction in movement-related high-gamma power. Moreover, we provide strong evidence for a pivotal role of motor cortical high-gamma oscillations in encoding movement rate. KEY POINTS: Neural oscillations in the high-gamma frequency range (60-90 Hz) emerge in the human motor cortex during movement. The precise function of these oscillations in motor control remains unclear, and they have never been characterized in stroke survivors. In a magnetoencephalography study, we demonstrate that high-gamma oscillations in motor cortical areas scale with movement rate, and we further explore their temporal and spatial characteristics. Stroke survivors exhibit lower high-gamma power during movement than age-matched control participants, even after matching for movement rate. The results contribute to the understanding of the role of high-gamma oscillations in motor control and have important implications for neuromodulation in stroke rehabilitation.
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.