Gait Modulation in C. elegans: An Integrated Neuromechanical Model

Abstract

Equipped with its 302-cell nervous system, the nematode Caenorhabditis elegans adapts its locomotion in different environments, exhibiting so-called swimming in liquids and crawling on dense gels. Recent experiments have demonstrated that the worm displays the full range of intermediate behaviors when placed in intermediate environments. The continuous nature of this transition strongly suggests that these behaviors all stem from modulation of a single underlying mechanism. We present a model of C. elegans forward locomotion that includes a neuromuscular control system that relies on a sensory feedback mechanism to generate undulations and is integrated with a physical model of the body and environment. We find that the model reproduces the entire swim-crawl transition, as well as locomotion in complex and heterogeneous environments. This is achieved with no modulatory mechanism, except via the proprioceptive response to the physical environment. Manipulations of the model are used to dissect the proposed pattern generation mechanism and its modulation. The model suggests a possible role for GABAergic D-class neurons in forward locomotion and makes a number of experimental predictions, in particular with respect to non-linearities in the model and to symmetry breaking between the neuromuscular systems on the ventral and dorsal sides of the body.

A Model of Larval Biomechanics Reveals Exploitable Passive Properties for Efficient Locomotion

“…A general practice in modelling soft tissues is to use idealized mass-springdamper systems [11][12][13][14].…”

The whole worm: brain–body–environment models of C. elegans

“…Despite large variations in the neural parameters of individual circuits, the information flow of the circuits was consistent across the ensemble [67 ]. The same minimal circuit was recently combined with the Boyle et al [42] model of forward locomotion to produce the first integrated neuromechanical model of spatial orientation in the worm [68 ] (Figure 2c). The model predicted how the worm's directional bearing changes as a function of the undulatory phase in which sensory stimuli is applied.…”

“…The only downside of biomechanical models that do not take into consideration environmental forces is that thrust production is not modeled, and thus forward motion is described only kinematically. Most recently, Boyle, Berri and Cohen [42] developed a neuromechanical model of locomotion using realistic environmental forces (Figure 2a,b). The model was designed to produce and propagate the waves using proprioceptive feedback.…”

“…(a) Model of forward locomotion adapted from[42]. The forward locomotion neural units affect all muscles along the body (blue).…”

Si elegans: A Computational Model of C. elegans Muscle Response to Light

“…The force calculated in the body wall muscles can be translated into muscle contraction and, furthermore, into movement. Many investigators have provided different models to achieved this (Boyle et al, 2012;Bryden and Cohen, 2008;Bryden, 2004), however, in this particular piece of work, the translation has not been performed.…”