Navigation of C. elegans in three-dimensional media: roll maneuvers and planar turns

TL;DR

This study provides the first quantitative analysis of C. elegans' 3D locomotion, revealing how roll maneuvers and planar turns enable effective exploration and chemotaxis in complex environments.

Contribution

It introduces a novel model describing C. elegans' 3D movement combining torsion and undulations, expanding understanding beyond previous 2D analyses.

Findings

C. elegans uses roll maneuvers to rotate undulation planes in 3D.

The nematode can perform efficient chemotaxis without sensory-motor adjustments.

3D locomotion strategies are applicable in both gel and water environments.

Abstract

Free-living nematode Caenorhabditis elegans is a powerful genetic model, essential for investigations ranging from behavior to neuroscience to aging, and locomotion is a key observable used in these studies. However, despite the fact that in its natural environment C. elegans moves in three-dimensional (3D) complex media (decomposing organic matter and water), quantitative in vestigations of its locomotion have been limited to two-dimensional (2D) motion. Based on our recent quantitative analysis of 2D turning maneuvers [Phys. Fluids 25, 081902 (2013)] we follow with the first quantitative description of how C. elegans moves in 3D environments. We show that by superposing body torsion and 2D undulations, a burrowing or swimming nematode can rotate the undulation plane. A combination of these roll maneuvers and 2D turns associated with variation of undulation-wave parameters allows the nematode to explore 3D space. We apply our model to analyze 3D chemotaxis of nematodes burrowing in a gel and swimming in water; we conclude that the nematode can achieve efficient chemotaxis in different environments without adjusting its sensory-motor response to chemical signals. Implications of our findings for understanding of 3D neuromuscular control of nematode body are discussed.