Zhao Peng, Wang Boyang, Rong Yi, Yuan Ye, Liu Jian, Huo Hong, Liu Zhuyong, Li Zhaoyu, Fang Tao
Department of Automation, Shanghai Jiao Tong University, Shanghai, China.
School of Naval Architecture, Ocean and Civil Engineering, Shanghai Jiao Tong University, Shanghai, China.
PLoS Comput Biol. 2025 Jun 25;21(6):e1013171. doi: 10.1371/journal.pcbi.1013171. eCollection 2025 Jun.
Rhythmic behaviors are essential in biological systems, particularly in animal locomotion. The central pattern generator and sensory feedback loop mechanism have been instrumental in explaining many rhythmic locomotion patterns, however, it is insufficient to account for the tunability and robustness of frequency and amplitude in certain oscillatory movements. This suggests the involvement of additional, less understood circuit mechanisms. This study employs calcium imaging and neuromechanical modelling to investigate the circuit mechanism responsible for sinusoidal forward locomotion in Caenorhabditis elegans. We demonstrate that the feedback loop circuit, consisting of motoneurons and muscles, could govern the generation of oscillations and regulate rhythmic forward movement. This circuit is composed of both negative and positive feedback loops, which together regulate the turnability and robustness of oscillations. The oscillatory behavior of C. elegans typically involves a rhythmic alternation of dorsoventral muscles. Our neuromechanical model of the functional oscillatory unit reveals that asymmetric inputs from interneurons to motoneurons, and asymmetric connections from motoneurons to muscles, are essential for this switching mechanism. Our findings suggest that, besides the established roles of existed oscillator mechanisms, circuits formed by both negative and positive feedback loops contribute to the generation and robust modulation of rhythmic behaviors.
节律性行为在生物系统中至关重要,尤其是在动物运动方面。中枢模式发生器和感觉反馈回路机制对于解释许多节律性运动模式起到了重要作用,然而,对于某些振荡运动中频率和幅度的可调性及稳健性,这一机制并不足以做出解释。这表明还存在其他尚未完全理解的电路机制在发挥作用。本研究采用钙成像和神经力学建模方法,来探究秀丽隐杆线虫正弦波式向前运动背后的电路机制。我们证明,由运动神经元和肌肉组成的反馈回路电路能够控制振荡的产生,并调节有节奏的向前运动。该电路由负反馈回路和正反馈回路组成,二者共同调节振荡的可调性和稳健性。秀丽隐杆线虫的振荡行为通常涉及背腹侧肌肉的有节奏交替。我们对功能性振荡单元的神经力学模型表明,中间神经元到运动神经元的不对称输入,以及运动神经元到肌肉的不对称连接,对于这种切换机制至关重要。我们的研究结果表明,除了现有振荡机制已明确的作用外,由负反馈回路和正反馈回路共同构成的电路,也有助于节律性行为的产生和稳健调节。