Department of Psychological and Brain Sciences, University of Iowa, Iowa City, Iowa 52245, and
Department of Neurology, University of Iowa Hospital and Clinics, Iowa City, Iowa 52242.
J Neurosci. 2020 Jan 8;40(2):411-423. doi: 10.1523/JNEUROSCI.1887-19.2019. Epub 2019 Nov 20.
The neurophysiological basis of motor control is of substantial interest to basic researchers and clinicians alike. Motor processes are accompanied by prominent field potential changes in the β-frequency band (15-29 Hz): in trial-averages, movement initiation is accompanied by β-band desynchronization over sensorimotor areas, whereas movement cancellation is accompanied by β-power increases over (pre)frontal areas. However, averaging misrepresents the true nature of the β-signal. Unaveraged β-band activity is characterized by short-lasting, burst-like events, rather than by steady modulations. Therefore, averaging-based quantifications may miss important brain-behavior relationships. To investigate how β-bursts relate to movement in male and female humans ( = 234), we investigated scalp-recorded β-band activity during the stop-signal task, which operationalizes both movement initiation and cancellation. Both processes were indexed by systematic spatiotemporal changes in β-burst rates. Before movement initiation, β-bursting was prominent at bilateral sensorimotor sites. These burst-rates predicted reaction time (a relationship that was absent in trial-average data), suggesting that sensorimotor β-bursting signifies an inhibited motor system, which has to be overcome to initiate movements. Indeed, during movement initiation, sensorimotor burst-rates steadily decreased, lateralizing just before movement execution. In contrast, successful movement cancellation was signified by increased phasic β-bursting over fronto-central sites. Such β-bursts were followed by short-latency increases of bilateral sensorimotor β-burst rates, suggesting that motor inhibition can be rapidly re-instantiated by frontal areas when movements have to be rapidly cancelled. Together, these findings suggest that β-bursting is a fundamental signature of the motor system, used by both sensorimotor and frontal areas involved in the trial-by-trial control of behavior. Movement-related β-frequency (15-29 Hz) changes are among the most prominent features of neural recordings across species, scales, and methods. However, standard averaging-based methods obscure the true dynamics of β-band activity, which is dominated by short-lived, burst-like events. Here, we demonstrate that both movement-initiation and cancellation in humans are characterized by unique trial-to-trial patterns of β-bursting. Movement initiation is characterized by steady reductions of β-bursting over bilateral sensorimotor sites. In contrast, during rapid movement cancellation, β-bursts first emerge over fronto-central sites typically associated with motor control, after which sensorimotor β-bursting re-initiates. These findings suggest a fundamentally novel, non-invasive measure of the neural interaction underlying movement-initiation and -cancellation, opening new avenues for the study of motor control in health and disease.
运动控制的神经生理学基础是基础研究人员和临床医生都非常感兴趣的领域。运动过程伴随着β频带（15-29 Hz）中的突出的场电位变化：在试验平均中，运动起始伴随着感觉运动区域的β频带去同步化，而运动取消则伴随着（额）前区域的β功率增加。然而，平均化会歪曲β信号的真实性质。未平均化的β频带活动以短时间、爆发式的事件为特征，而不是稳定的调制。因此，基于平均化的量化可能会错过重要的脑-行为关系。为了研究β爆发如何与男性和女性人类（= 234）的运动相关，我们在停止信号任务中研究了头皮记录的β频带活动，该任务操作了运动的启动和取消。这两个过程都以β爆发率的系统时空变化为指标。在运动启动之前，双侧感觉运动部位的β爆发明显增加。这些爆发率预测了反应时间（在试验平均数据中不存在这种关系），这表明感觉运动β爆发标志着一个受到抑制的运动系统，必须克服这个系统才能启动运动。事实上，在运动启动期间，感觉运动爆发率稳步下降，在运动执行前偏向于一侧。相比之下，成功的运动取消表现为额-中央部位的β爆发的相位性增加。这种β爆发之后是双侧感觉运动β爆发率的短潜伏期增加，这表明当运动必须迅速取消时，额叶区域可以迅速重新建立运动抑制。总的来说，这些发现表明β爆发是运动系统的基本特征，参与行为的逐次控制的感觉运动和额区都在使用它。与行为相关的β频带（15-29 Hz）变化是跨物种、尺度和方法的神经记录中最突出的特征之一。然而，基于标准平均的方法掩盖了β频带活动的真实动态，该活动主要由短暂的、爆发式的事件主导。在这里，我们证明了人类的运动启动和取消都具有独特的逐次试验β爆发模式。运动启动的特征是双侧感觉运动部位β爆发的稳定减少。相比之下，在快速运动取消期间，β爆发首先出现在通常与运动控制相关的额-中央部位，之后感觉运动β爆发重新开始。这些发现为运动启动和取消的神经相互作用提供了一种全新的、非侵入性的测量方法，为健康和疾病中的运动控制研究开辟了新的途径。
