Synergistic Organization of Neural Inputs from Spinal Motor Neurons to Extrinsic and Intrinsic Hand Muscles
Synergistic Organization of Neural Inputs from Spinal Motor Neurons to Extrinsic and Intrinsic Hand Muscles
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DOI：
10.1523/jneurosci.0419-21.2021
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发表时间：
2021-06
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通讯作者：
Simone Tanzarella;S. Muceli;M. Santello;D. Farina
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作者：
Simone Tanzarella;S. Muceli;M. Santello;D. Farina
我们目前对协同肌肉控制的理解是基于对肌肉活动的分析。肌肉协调中的模块（协同作用）是从肌电图（EMG）信号包络中提取的。每个包膜间接反映了肌肉接收的神经驱动;因此，它携带了支配运动神经元的整体活动信息。然而，目前尚不清楚脊髓运动神经元的输出，其数量比它们所支配的肌肉大几个数量级，在执行复杂任务时是否以低维方式组织。在这里，我们假设运动神经元活动在复杂任务中表现出协同组织，因此运动神经元的共同输入导致运动神经元输出的大维数降低。为了验证这一假设，我们分解了支配14个内在和外在手部肌肉的运动神经元的输出尖峰序列，并分析了健康个体使用7种抓握类型施加等长力时的控制维度。我们确定了四个运动神经元协同作用，占54.1 ± 12.9个运动神经元活动方差的70%以上，我们确定了四个功能相似的肌肉协同作用。然而，运动神经元的协同作用更好地区分个别手指的力量比肌肉协同作用，更符合预期的作用，肌肉驱动每个手指。此外，在少数情况下，支配同一肌肉的运动神经元在单独的协同作用中是活跃的。我们的研究结果表明，一个高度分散的净神经输入脊髓运动神经元从脊髓和脊髓上的结构，有助于减少肌肉协同作用所捕获的维度。我们讨论了支配多个手部肌肉的脊髓运动神经元的输出是否可以通过模块化组织来解释，即，协同作用，先前描述为多个肌肉的协调。我们发现，运动神经元协同作用呈现出与肌肉协同作用相似的维度（意味着维度减少>10倍）和结构。尽管如此，也观察到肌肉内运动神经元子集的协同行为。这些结果推进了我们对神经肌肉控制如何从映射下行输入到肌肉激活信号的理解。我们提供了，第一次，深入了解脊髓运动神经元的神经输入的组织，迄今为止，已推断通过肌肉协同作用的分析。
Our current understanding of synergistic muscle control is based on the analysis of muscle activities. Modules (synergies) in muscle coordination are extracted from electromyographic (EMG) signal envelopes. Each envelope indirectly reflects the neural drive received by a muscle; therefore, it carries information on the overall activity of the innervating motor neurons. However, it is not known whether the output of spinal motor neurons, whose number is orders of magnitude greater than the muscles they innervate, is organized in a low-dimensional fashion when performing complex tasks. Here, we hypothesized that motor neuron activities exhibit a synergistic organization in complex tasks and therefore that the common input to motor neurons results in a large dimensionality reduction in motor neuron outputs. To test this hypothesis, we factorized the output spike trains of motor neurons innervating 14 intrinsic and extrinsic hand muscles and analyzed the dimensionality of control when healthy individuals exerted isometric forces using seven grip types. We identified four motor neuron synergies, accounting for >70% of the variance of the activity of 54.1 ± 12.9 motor neurons, and we identified four functionally similar muscle synergies. However, motor neuron synergies better discriminated individual finger forces than muscle synergies and were more consistent with the expected role of muscles actuating each finger. Moreover, in a few cases, motor neurons innervating the same muscle were active in separate synergies. Our findings suggest a highly divergent net neural inputs to spinal motor neurons from spinal and supraspinal structures, contributing to the dimensionality reduction captured by muscle synergies. SIGNIFICANCE STATEMENT We addressed whether the output of spinal motor neurons innervating multiple hand muscles could be accounted for by a modular organization, i.e., synergies, previously described to account for the coordination of multiple muscles. We found that motor neuron synergies presented similar dimensionality (implying a >10-fold reduction in dimensionality) and structure as muscle synergies. Nonetheless, the synergistic behavior of subsets of motor neurons within a muscle was also observed. These results advance our understanding of how neuromuscular control arises from mapping descending inputs to muscle activation signals. We provide, for the first time, insights into the organization of neural inputs to spinal motor neurons which, to date, has been inferred through analysis of muscle synergies.