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. 2008 Dec 30;105(52):20982-7.
doi: 10.1073/pnas.0810359105. Epub 2008 Dec 12.

Genetic analysis of crawling and swimming locomotory patterns in C. elegans

Jonathan T Pierce-Shimomura  1 , Beth L Chen, James J Mun, Raymond Ho, Raman Sarkis, Steven L McIntire
Affiliations

Genetic analysis of crawling and swimming locomotory patterns in C. elegans

Jonathan T Pierce-Shimomura et al. Proc Natl Acad Sci U S A. .

Abstract

Alternative patterns of neural activity drive different rhythmic locomotory patterns in both invertebrates and mammals. The neuro-molecular mechanisms responsible for the expression of rhythmic behavioral patterns are poorly understood. Here we show that Caenorhabditis elegans switches between distinct forms of locomotion, or crawling versus swimming, when transitioning between solid and liquid environments. These forms of locomotion are distinguished by distinct kinematics and different underlying patterns of neuromuscular activity, as determined by in vivo calcium imaging. The expression of swimming versus crawling rhythms is regulated by sensory input. In a screen for mutants that are defective in transitioning between crawl and swim behavior, we identified unc-79 and unc-80, two mutants known to be defective in NCA ion channel stabilization. Genetic and behavioral analyses suggest that the NCA channels enable the transition to rapid rhythmic behaviors in C. elegans. unc-79, unc-80, and the NCA channels represent a conserved set of genes critical for behavioral pattern generation.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Crawling and swimming are characterized by distinct kinematics. (A) Video frames of the same WT animal crawling and swimming. Time and phase of the DV head-bend cycle are indicated below each frame. DV cycle start is defined as the moment the head turns dorsal. Note that the body always forms a C-like shape immediately before this turn. Curvature columns (Right) represent curvature for each of the 11 angles along the example midlines aligned anterior to posterior (A, P). Example angles are matched by arrows. (B) Crawl and swim curvature matrices for a WT individual. Average curvature matrix for DV head-bend cycles are shown (Right) with number of averaged cycles indicated above. (C) Plots of neck curvature versus time for the same individual. Plots of average power versus frequency of neck curvature across individuals (D). Individual traces are indicated by gray lines. Bars represent SEM.
Fig. 2.
Fig. 2.
Swimming as a directed form of locomotion for C. elegans. Photos of groups of WT animals swimming in a puddle dropped over agar containing either a salt gradient (A) or no gradient (B). Cross-section layout of the agar assay plates and liquid drops below. (C) Average percent of individuals on attractive side versus time for animals in gradient or control assays. Bars represent SEM.
Fig. 3.
Fig. 3.
Crawling and swimming are generated by distinct patterns of muscle activity. (A and B) Muscle activity of opposing dorsal and ventral muscle quadrants in a crawling (A) and swimming (B) animals. Plots of intensity ratio (YFP/CFP) for cameleon in body-wall muscle along anterior-posterior axis versus time shown above. Corresponding curvature matrices for dorsal and ventral body sides shown below. Note that areas of peak muscle activity (contour lines) for dorsal side generally coincide with or slightly precede corresponding areas of dorsal curvature (green/blue) whereas areas of peak muscle activity for ventral side coincide with or slightly precede corresponding areas of ventral curvature (yellow/red). Positions on anteroposterior axis with no observed ratio change are a result of absence of expression of cameleon extra-chromosomal array. Color key for intensity ratio is shown (Right). Vertical black lines distinguish head bend cycles. Slanted/dashed lines correspond to end of one cycle of ventral muscle activity and highlight the rapid propagation of ventral muscle activity for swimming versus crawling with respect to DV head bending. Color key for body-side curvature matrices uses blue-green-yellow-red color scheme to contrast with body-midline curvature matrices, which use blue-white-red color scheme in other figures.
Fig. 4.
Fig. 4.
Sensory regulation of the expression of crawling and swimming. (A) Crawl and swim curvature matrices for a che-3 mutant. Two panels are shown for “Swim” to demonstrate switch between nearly normal swimming (Left) and crawl-like motion (Right). Average curvature matrix for DV head-bend cycles are shown (Right). (B) Plots of neck curvature versus time for the same individual. Example of swim curvature demonstrates a switch from normal swim to crawl-like motion even though the animal remains in liquid. (C) Plots of average power versus frequency of neck curvature across individuals. *P < 0.05 with Tukey test of multiple comparison. Arrowhead indicates extra peak in the che-3 mutant distribution. Bars represent SEM.
Fig. 5.
Fig. 5.
Comparison of WT and mutant patterns of locomotion. (A) On crawling curvature matrices, vertical lines distinguish DV head-bend cycles. Corresponding average DV cycle curvature matrix is shown (Right). Number of averaged cycles indicated above. (B) Swimming curvature matrices: dotted vertical lines indicates when animals entered liquid. (C) Crawl escape curvature matrices: dotted vertical lines indicates stimulation time. (D) Average propagation speed of first DV bend for swimming (s; gray) and crawl escape (ce; orange) relative to WT (s, 0.85 sec−1; ce, 1.75 sec−1). Speed not calculated for cca-1 double mutants (N. D.) because of incomplete bend propagation. (E) Average number of DV bends propagated for initial swimming and crawl escape motion before omega bend (Ω) or faint episode (F). Rescue strain unc-80;Punc-80(+) indicated by unc-80(R). Symbols show differences (*) from WT, ($) from unc-80, or (&) from nca-1;nca-2; P < 0.05. n = 15 for each bar. Bars represent SEM with Tukey test of multiple comparison.
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References

    1. Feldman JL, Mitchell GS, Nattie EE. Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci. 2003;26:239–266. - PMC - PubMed
    1. Jing J, et al. From hunger to satiety: reconfiguration of a feeding network by Aplysia neuropeptide Y. J Neurosci. 2007;27:3490–3502. - PMC - PubMed
    1. Nusbaum MP, Beenhakker MP. A small-systems approach to motor pattern generation. Nature. 2002;417:343–350. - PMC - PubMed
    1. Marder E, Bucher D. Central pattern generators and the control of rhythmic movements. Curr Biol. 2001;11:R986–R996. - PubMed
    1. Marder E, Calabrese RL. Principles of rhythmic motor pattern generation. Physiol Rev. 1996;76:687–717. - PubMed

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