Journal of Neuroscience ( IF 5.3 ) Pub Date : 2021-02-17 , DOI: 10.1523/jneurosci.1589-20.2020 Steve A. Edgley , Elizabeth R. Williams , Stuart N. Baker
Renshaw cells mediate recurrent inhibition between motoneurons within the spinal cord. The function of this circuit is not clear; we previously suggested based on computational modeling that it may cancel oscillations in muscle activity around 10 Hz, thereby reducing physiological tremor. Such tremor is especially problematic for dexterous hand movements, yet knowledge of recurrent inhibitory function is sparse for the control of the primate upper limb, where no direct measurements have been made to date. In this study, we made intracellular penetrations into 89 motoneurons in the cervical enlargement of four terminally anesthetized female macaque monkeys, and recorded recurrent IPSPs in response to antidromic stimulation of motor axons. Recurrent inhibition was strongest to motoneurons innervating shoulder muscles and elbow extensors, weak to wrist and digit extensors, and almost absent to the intrinsic muscles of the hand. Recurrent inhibitory connections often spanned joints, for example from motoneurons innervating wrist and digit muscles to those controlling the shoulder and elbow. Wrist and digit flexor motoneurons sometimes inhibited the corresponding extensors, and vice versa. This complex connectivity presumably reflects the flexible usage of the primate upper limb. Using trains of stimuli to motor nerves timed as a Poisson process and coherence analysis, we also examined the temporal properties of recurrent inhibition. The recurrent feedback loop effectively carried frequencies up to 100 Hz, with a coherence peak around 20 Hz. The coherence phase validated predictions from our previous computational model, supporting the idea that recurrent inhibition may function to reduce tremor.
SIGNIFICANCE STATEMENT We present the first direct measurements of recurrent inhibition in primate upper limb motoneurons, revealing that it is more flexibly organized than previous observations in cat. Recurrent inhibitory connections were relatively common between motoneurons controlling muscles that act at different joints, and between flexors and extensors. As in the cat, connections were minimal for motoneurons innervating the most distal intrinsic hand muscles. Empirical data are consistent with previous modeling: temporal properties of the recurrent inhibitory feedback loop are compatible with a role in reducing physiological tremor by suppressing oscillations around 10 Hz.
中文翻译:
灵长类上肢反复抑制的时空安排
Renshaw细胞介导脊髓内运动神经元之间的反复抑制。该电路的功能不清楚。我们先前根据计算模型提出,它可以消除10 Hz附近的肌肉活动振荡,从而减少生理震颤。这样的震颤对于灵巧的手运动尤其成问题,但是对于抑制灵长类上肢的复发抑制功能的知识很少,迄今尚未进行直接测量。在这项研究中,我们使四只末端麻醉的雌性猕猴的宫颈增大进入了89个运动神经元的细胞内穿入,并记录了对运动轴突的反刺激刺激后的复发IPSP。反复抑制对支配肩部肌肉和肘伸肌的运动神经元最强,对腕部和指伸肌无力,而手的固有肌肉几乎不存在。反复出现的抑制性连接经常跨越关节,例如从支配腕部和趾部肌肉的运动神经元到控制肩膀和肘部的神经元。腕关节和指屈运动神经元有时会抑制相应的伸肌,反之亦然。这种复杂的连接性大概反映了灵长类上肢的灵活使用。使用以Poisson过程和相干分析为定时的运动神经刺激序列,我们还检查了反复抑制的时间特性。循环反馈环路有效地承载了高达100 Hz的频率,并且相干峰约为20 Hz。相干阶段验证了我们先前计算模型的预测,
重要性声明我们首次对灵长类上肢运动神经元中的复发抑制进行了直接测量,揭示了它比猫中先前的观察更为灵活。反复抑制连接在控制作用于不同关节的运动神经元之间以及屈肌和伸肌之间相对普遍。就像在猫中一样,运动神经元支配最远端固有手部肌肉的连接极少。经验数据与以前的模型一致:周期性抑制性反馈回路的时间特性与通过抑制10 Hz左右的振荡来减轻生理性震颤的作用兼容。