An animal adapts its motor behavior to navigate through the external environment. This adaptation depends on proprioception, which provides feedback on an animal’s body postures. How proprioception mechanisms interact with motor circuits and contribute to locomotor adaptation remains unclear. Here we describe and characterize proprioception-mediated homeostatic control of undulatory movement in the roundworm Caenorhabditis elegans. We found the worm responds to optogenetically or mechanically induced decreases in mid-body bending amplitude by increasing its anterior amplitude. Conversely, it responds to increased mid-body amplitude by decreasing the anterior amplitude. Using genetics, microfluidic and optogenetic perturbation response analyses, and optical neurophysiology, we elucidated the neural circuit underlying this compensatory postural response. The dopaminergic PDE neurons sense mid-body bending and signal to AVK interneurons via the D2-like dopamine receptor DOP-3. The FMRFamide-like neuropeptide FLP-1, released by AVK, regulates SMB head motor neurons to modulate anterior bending. We propose that this homeostatic behavioral control optimizes the efficiency of locomotion. Our findings demonstrate a mechanism in which proprioception works with dopamine and neuropeptide signaling to mediate motor control, a motif that may be conserved in other animals.

ImageJ or other image/video softwares are required to open the image/video files. Intermediate files contained in the 'Optogenetic experiments' folder can be opened by MATLAB (2020b).