TY - JOUR
T1 - Roll maneuvers are essential for active reorientation of Caenorhabditis elegans in 3D media
AU - Bilbao, Alejandro
AU - Patel, Amar K.
AU - Rahman, Mizanur
AU - Vanapalli, Siva A.
AU - Blawzdziewicz, Jerzy
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank Dr. N. J. Szewczyk and Dr. M. Driscoll for useful discussions. A.B. acknowledges financial support from NSF Grant CBET 1059745 and a Texas Tech University Doctoral Dissertation Completion Fellowship. J.B. was partially supported by NSF Grant CBET 1603627. S.A.V. and M.R. acknowledge partial support from Grants NIH 1R21AG050503-01 and NASA NNX15AL16G.
Funding Information:
We thank Dr. N. J. Szewczyk and Dr. M. Driscoll for useful discussions. A.B. acknowledges financial support from NSF Grant CBET 1059745 and a Texas Tech University Doctoral Dissertation Completion Fellowship. J.B. was partially supported by NSF Grant CBET 1603627. S.A.V. and M.R. acknowledge partial support from Grants NIH 1R21AG050503-01 and NASA NNX15AL16G.
Publisher Copyright:
© 2018 National Academy of Sciences. All rights reserved.
PY - 2018
Y1 - 2018
N2 - 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.
AB - 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.
KW - 3D gait
KW - Behavior
KW - Caenorhabdtis elegans
KW - Maneuverability
KW - Undulatory locomotion
UR - http://www.scopus.com/inward/record.url?scp=85045668042&partnerID=8YFLogxK
U2 - 10.1073/pnas.1706754115
DO - 10.1073/pnas.1706754115
M3 - Article
C2 - 29618610
AN - SCOPUS:85045668042
VL - 115
SP - E3616-E3625
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 16
ER -