Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans

Abstract

C. elegans locomotes in an undulatory fashion, generating thrust by propagating dorsoventral bends along its body. Although central pattern generators (CPGs) are typically involved in animal locomotion, their presence in C. elegans has been questioned, mainly because there has been no evident circuit that supports intrinsic network oscillations. With a fully reconstructed connectome, the question of whether it is possible to have a CPG in the ventral nerve cord (VNC) of C. elegans can be answered through computational models. We modeled a repeating neural unit based on segmentation analysis of the connectome. We then used an evolutionary algorithm to determine the unknown physiological parameters of each neuron so as to match the features of the neural traces of the worm during forward and backward locomotion. We performed 1,000 evolutionary runs and consistently found configurations of the neural circuit that produced oscillations matching the main characteristic observed in experimental recordings. In addition to providing an existence proof for the possibility of a CPG in the VNC, we suggest a series of testable hypotheses about its operation. More generally, we show the feasibility and fruitfulness of a methodology to study behavior based on a connectome, in the absence of complete neurophysiological details. Despite the relative simplicity of C. elegans, its locomotion machinery is not yet well understood. We focus on the generation of dorsoventral body bends. Although network central pattern generators are commonly involved in animal locomotion, their presence in C. elegans has been questioned due to a lack of an evident neural circuit to support it. We developed a computational model grounded in the available neuroanatomy and neurophysiology, and we used an evolutionary algorithm to explore the space of possible configurations of the circuit that matched the neural traces observed during forward and backward locomotion in the worm. Our results demonstrate that it is possible for the rhythmic contraction to be produced by a circuit present in the ventral nerve cord.

Keywords

• Behavioral connectomics
• Network dynamics
• Central pattern generator
• Locomotion