Department of Animal Physiology, Institute of Zoology, Biocenter Cologne, University of Cologne, Cologne, Germany.
J Neurophysiol. 2021 May 1;125(5):1800-1813. doi: 10.1152/jn.00090.2021. Epub 2021 Mar 31.
In legged animals, integration of information from various proprioceptors in and on the appendages by local premotor networks in the central nervous system is crucial for controlling motor output. To ensure posture maintenance and precise active movements, information about limb loading and movement is required. In insects, various groups of campaniform sensilla (CS) measure forces and loads acting in different directions on the leg, and the femoral chordotonal organ (fCO) provides information about movement of the femur-tibia (FTi) joint. In this study, we used extra- and intracellular recordings of extensor tibiae (ExtTi) and retractor coxae (RetCx) motor neurons (MNs) and identified local premotor nonspiking interneurons (NSIs) and mechanical stimulation of the fCO and tibial or trochanterofemoral CS (tiCS, tr/fCS), to investigate the premotor network architecture underlying multimodal proprioceptive integration. We found that load feedback from tiCS altered the strength of movement-elicited resistance reflexes and determined the specificity of ExtTi and RetCx MN responses to various load and movement stimuli. These responses were mediated by a common population of identified NSIs into which synaptic inputs from the fCO, tiCS, and tr/fCS are distributed, and whose effects onto ExtTi MNs can be antagonistic for both stimulus modalities. Multimodal sensory signal interaction was found at the level of single NSIs and MNs. The results provide evidence that load and movement feedback are integrated in a multimodal, distributed local premotor network consisting of antagonistic elements controlling movements of the FTi joint, thus substantially extending current knowledge on how legged motor systems achieve fine-tuned motor control. Proprioception is crucial for motor control in legged animals. We show the extent to which processing of movement (fCO) and load (CS) signals overlaps in the local premotor network of an insect leg. Multimodal signals converge onto the same set of interneurons, and our knowledge about distributed, antagonistic processing is extended to incorporate multiple modalities within one perceptual neuronal framework.
在有腿的动物中，中枢神经系统中附肢内和附肢上的各种本体感受器的信息通过局部运动前网络进行整合，对于控制运动输出至关重要。为了确保姿势维持和精确的主动运动，需要有关肢体负荷和运动的信息。在昆虫中，各种类型的钟形感觉器（CS）测量作用在腿部不同方向上的力和负荷，股索感觉器（fCO）提供关于股骨-胫骨（FTi）关节运动的信息。在这项研究中，我们使用了伸肌胫骨（ExtTi）和伸肌股骨（RetCx）运动神经元（MN）的细胞外和细胞内记录，并鉴定了局部运动前无峰神经元（NSI）和对 fCO 和胫骨或转节股 CS（tiCS，tr/fCS）的机械刺激，以研究多模态本体感受整合的运动前网络结构。我们发现，tiCS 的负载反馈改变了运动引发的阻力反射的强度，并确定了 ExtTi 和 RetCx MN 对各种负载和运动刺激的特异性反应。这些反应是由一个共同的鉴定 NSI 种群介导的，该种群接受来自 fCO、tiCS 和 tr/fCS 的突触输入，并且其对 ExtTi MN 的影响可以对两种刺激模式产生拮抗作用。在单个 NSI 和 MN 水平上发现了多模态感觉信号相互作用。研究结果提供了证据，表明负载和运动反馈在一个由拮抗元件组成的多模态、分布式局部运动前网络中进行整合，该网络控制 FTi 关节的运动，从而大大扩展了关于腿部运动系统如何实现精细运动控制的现有知识。本体感受对于有腿动物的运动控制至关重要。我们展示了运动（fCO）和负荷（CS）信号在昆虫腿部的局部运动前网络中处理的程度。多模态信号汇聚到同一组神经元上，并且我们对分布式拮抗处理的了解扩展到在一个感知神经元框架内包含多个模态。
