Biomechanical analysis of gait adaptation in the nematode Caenorhabditis elegans

Abstract

To navigate different environments, an animal must be able to adapt its locomotory gait to its physical surroundings. The nematode Caenorhabditis elegans, between swimming in water and crawling on surfaces, adapts its locomotory gait to surroundings that impose approximately 10,000-fold differences in mechanical resistance. Here we investigate this feat by studying the undulatory movements of C. elegans in Newtonian fluids spanning nearly five orders of magnitude in viscosity. In these fluids, the worm undulatory gait varies continuously with changes in external load: As load increases, both wavelength and frequency of undulation decrease. We also quantify the internal viscoelastic properties of the worm's body and their role in locomotory dynamics. We incorporate muscle activity, internal load, and external load into a biomechanical model of locomotion and show that (i) muscle power is nearly constant across changes in locomotory gait, and (ii) the onset of gait adaptation occurs as external load becomes comparable to internal load. During the swimming gait, which is evoked by small external loads, muscle power is primarily devoted to bending the worm's elastic body. During the crawling gait, evoked by large external loads, comparable muscle power is used to drive the external load and the elastic body. Our results suggest that C. elegans locomotory gait continuously adapts to external mechanical load in order to maintain propulsive thrust.H ow do neural circuits produce and regulate the rhythmic patterns of muscle activity that drive animal locomotion? The nematode Caenorhabditis elegans-with its well-mapped nervous system (1), relatively simple anatomy (2), and rhythmic undulatory movements (3)-is a promising model for exploring the neural basis of locomotion. To fully understand motor behavior we also need to understand C. elegans locomotory biomechanics: how muscle activity produces movement within the mechanical framework of the worm's body and its physical environment.C. elegans moves forward by propagating undulatory waves in a dorsal-ventral plane from head to tail (3). Bending is generated by alternating contraction and relaxation of two dorsal and two ventral muscle groups running along the length of the worm's body (2). Both the shape and speed of these undulations change in response to the physical environment (3, 4). When moving on moist surfaces such as agarose gels, C. elegans exhibits a crawling gait characterized by undulations with low frequency and short wavelength (5). By contrast, when moving through water, C. elegans exhibits a swimming gait characterized by undulations with higher frequency and longer wavelength ( Table 1). The differences in the size and speed of undulations are modest in comparison with the difference in the scales of physical force during swimming and crawling. At the size and speed of C. elegans, forces due to surface tension (surface tension holds the crawling animal to the agar surface) are approximately 10,000-fold larger than forces due to viscosity when swimming ...

Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans

“…A wild-type C. elegans worm exhibits a rapid backward movement when its nose encounters water-soluble repellents in a dry drop test 24 . To quantify the kinematics of worm undulatory locomotion during a CuSO 4 -evoked reversal, we calculated the normalized curvature (NC) of the worm body 25,26 . In brief, the worm body was divided into ten equal segments from head to tail (head ¼ 0 and tail ¼ 1).…”

“…CuSO 4 was dissolved in M13 buffer consisting of 30 mM Tris, 100 mM NaCl and 10 mM KCl. To examine a single worm response to Cu 2 þ stimulation, the 'dry drop test' was used 25 . Briefly, a micro-drop (approximately a few hundreds of nanolitres) of Cu 2 þ solution was delivered via a glass micropipette in front of an animal exhibiting forward sinusoidal locomotion, and the rapid backward movement was observed and recorded when the animals encountered the repellent, of which the solution drop had been absorbed into the agar, under a Zeiss Discovery V8 stereomicroscope (Carl Zeiss MicroImaging GmbH, Göttingen, Germany).…”

“…The body bend was defined as the change in the direction of propagation of the part corresponding to the posterior bulb of the pharynx along the y axis of the worm, assuming the worm was travelling along the x axis. NC was used to quantify the undulatory kinematics of the reversal over time 25,26 . First, the total length of the worm body from head to tail (head ¼ 0; tail ¼ 1) was divided into ten equal segments.…”

Worms under Pressure: Bulk Mechanical Properties of C. elegans Are Independent of the Cuticle

“…A bulk modulus~1 atm would lead to observable strains (~10% if the worm moves downwards a distance of 1 m in the water column), suggesting that a soft, hydraulically reinforced body plan may allow the worm to inhabit a greater range of environments. Similarly, a soft, isotropically deformable body may allow the worm to optimize its swimming mechanism for heterogenous or pressurized environments, as there is known mechanical feedback between the worm's environment and its ability to swim (13,53).…”

Characterizations of kinetic power and propulsion of the nematode Caenorhabditis elegans based on a micro-particle image velocimetry system

“…[1][2][3] For studies regarding motor neurons, 4 neuromuscular damage, 5 and muscular disorder, 6 the properties provide quantitative clues of the worm's physiological changes. However, direct measurements of motility for such a small-sized organism remain challenging due to lack of proper tools.…”