Haverland Benjamin, Timmsen Lena S, Wolf Silke, Stagg Charlotte J, Frontzkowski Lukas, Oostenveld Robert, Schön Gerhard, Feldheim Jan, Higgen Focko L, Gerloff Christian, Schulz Robert, Schneider Till R, Schwab Bettina C, Quandt Fanny
Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
J Physiol. 2025 Feb;603(4):873-893. doi: 10.1113/JP286873. Epub 2025 Jan 9.
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.
运动皮层高频伽马振荡（60 - 90赫兹）在运动开始时出现，且在空间上集中于对侧初级运动皮层。尽管高频伽马振荡因其在人类运动控制中的重要性而被广泛认可，但其在皮层水平上的确切功能仍不清楚。重要的是，它们在人类中风病理生理学中的相关性尚不清楚。由于运动功能障碍是中风后症状负担的基本决定因素，了解运动编码的神经生理过程可能是改善中风康复的重要一步。我们记录了14名慢性中风幸存者、15名年龄匹配的对照参与者和29名健康年轻参与者在拇指运动速率任务期间的脑磁图数据。运动皮层高频伽马振荡与运动速率呈现出强烈的相关性，因为运动速率较高的试验与更大的高频伽马功率相关。尽管中风幸存者表现出皮层高频伽马功率降低，但这种降低主要反映了高频伽马功率随运动速率的缩放，然而在匹配中风幸存者和年龄匹配对照的运动速率后，高频伽马功率的降低超过了仅由其运动速率降低所产生的影响。尽管在所有三组中运动技能的获得都很明显，但它与高频伽马功率并无关联。我们的研究对中风后的高频伽马振荡进行了量化，揭示了与运动相关的高频伽马功率降低。此外，我们为运动皮层高频伽马振荡在编码运动速率中起关键作用提供了有力证据。要点：高频伽马频率范围（60 - 90赫兹）的神经振荡在人类运动过程中出现在运动皮层。这些振荡在运动控制中的精确功能仍不清楚，且从未在中风幸存者中进行过特征描述。在一项脑磁图研究中，我们证明运动皮层区域的高频伽马振荡随运动速率缩放，并且我们进一步探索了它们的时间和空间特征。即使在匹配运动速率后，中风幸存者在运动期间的高频伽马功率仍低于年龄匹配的对照参与者。这些结果有助于理解高频伽马振荡在运动控制中的作用，并对中风康复中的神经调节具有重要意义。
