β-Bursts Reveal the Trial-to-Trial Dynamics of Movement Initiation and Cancellation

β-Bursts Reveal the Trial-to-Trial Dynamics of Movement Initiation and Cancellation
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DOI:
10.1101/644682
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发表时间:
2019-05
期刊:
The Journal of Neuroscience
影响因子:
--
通讯作者:
J. Wessel
J. Wessel
中科院分区:
其他
文献类型:
--
作者:
J. Wessel

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基础研究人员和临床医生都对运动控制的神经生理学基础非常感兴趣。运动过程伴随着β频段(15-29赫兹)的显著场电位变化:在试验平均值中,运动启动伴随着感觉运动区的β频段去同步,而运动取消伴随着额叶(前)区的β功率增加。然而,平均化错误地反映了β信号的真实性质。非平均β频段活动的特点是持续时间短、类似突发的事件,而不是稳定的调制。因此,基于平均值的量化可能会错过重要的大脑-行为关系。为了研究β-Burst如何与男性和女性(N=234)的运动有关,我们研究了停止信号任务中头皮记录的β频段活动,该任务同时操作了运动的启动和取消。这两个过程都通过系统的β-Burst速率的时空变化来索引。在运动开始前,β爆发在双侧感觉运动部位显著。这些爆发率预测了反应时间(这种关系在试验平均数据中是不存在的),这表明感觉运动β-猝发意味着运动系统受到抑制,必须克服该系统才能启动运动。事实上,在动作启动过程中,感觉运动爆发率稳步下降,在动作执行前呈偏侧化。相反,成功的运动取消标志着额叶到中央部位的时相β爆发增加。在这种β爆发之后,双侧感觉运动β爆发频率的短潜伏期增加,这表明当运动必须迅速取消时,运动抑制可以通过额区迅速重新激活。综上所述,这些发现表明,β爆发是运动系统的一个基本标志,感觉运动和额叶区域都使用,参与对行为的逐次尝试控制。意义陈述与运动相关的β频率(15-29赫兹)变化是跨物种、不同尺度和不同方法的神经记录的最显著特征之一。然而,基于标准平均的方法掩盖了β频段活动的真实动态,该频段活动由短暂的、类似突发的事件主导。在这里,我们证明了人类运动的启动和取消都具有独特的β爆发的试验到试验模式。运动起始的特点是双侧感觉运动部位的β爆发持续减少。相比之下,在快速运动消除过程中,β爆发首先出现在通常与运动控制相关的额中枢部位,之后感觉运动β爆发重新启动。这些发现表明了一种全新的、非侵入性的测量运动启动和取消的神经相互作用的方法,为研究健康和疾病中的运动控制开辟了新的途径。
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 (N = 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. SIGNIFICANCE STATEMENT 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.