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Roll maneuvers are essential for active reorientation of Caenorhabditis elegans in 3D media

A. Bilbao,Amar K Patel,Mizanur Rahman,S. Vanapalli,J. Blawzdziewicz

Published 2016 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance Investigations of the free-living nematode Caenorhabditis elegans give powerful insights into fundamental biological processes that are conserved across species. Locomotion of this model organism is used to assess muscular and neural defects and score impacts of genetic mutations and pharmacological interventions. Existing analyses of the nematode gait have been focused on 2D locomotion, and 3D motion remains largely unexplored. We identify and mathematically describe a unique 3D behavioral pattern in burrowing and swimming—a roll maneuver—which, in combination with 2D turns, allows the nematode to explore bulk media. Our results provide important insights into 3D neuromuscular actuation and may be used to develop better assays for locomotion phenotype analysis. Locomotion of the nematode Caenorhabditis elegans is a key observable used in investigations ranging from behavior to neuroscience to aging. However, while the natural environment of this model organism is 3D, quantitative investigations of its locomotion have been mostly limited to 2D motion. Here, we present a quantitative analysis of how the nematode reorients itself in 3D media. We identify a unique behavioral state of C. elegans—a roll maneuver—which is an essential component of 3D locomotion in burrowing and swimming. The rolls, associated with nonzero torsion of the nematode body, result in rotation of the plane of dorsoventral body undulations about the symmetry axis of the trajectory. When combined with planar turns in a new undulation plane, the rolls allow the nematode to reorient its body in any direction, thus enabling complete exploration of 3D space. The rolls observed in swimming are much faster than the ones in burrowing; we show that this difference stems from a purely hydrodynamic enhancement mechanism and not from a gait change or an increase in the body torsion. This result demonstrates that hydrodynamic viscous forces can enhance 3D reorientation in undulatory locomotion, in contrast to known hydrodynamic hindrance of both forward motion and planar turns.

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