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.
Highlights
One essential requirement for the survival of most animals is the ability to move around in a world characterized by complex, unpredictable, and variable environments
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
One would expect that placing model worms in different virtual environments would result in different motor behaviors, but it is not clear a priori what range of motor behaviors can be obtained in this way
Summary
One essential requirement for the survival of most animals is the ability to move around in a world characterized by complex, unpredictable, and variable environments. Adapting to different environments often involves the use of qualitatively distinct patterns of locomotion, called gaits. The animal’s nervous system is responsible for generating the rhythmic neuromuscular activity associated with each of these gaits and must coordinate the task of switching seamlessly between them. The animal must be able to reliably adapt any of these patterns in response to external perturbations. The popular model organism Caenorhabditis elegans is a tiny (≈1 mm long) nematode worm with a largely invariant nervous system, consisting of exactly 302 neurons with known connectivity (White et al, 1986; Chen et al, 2006). Despite its small size and the apparent simplicity of the underlying nervous system, the worm is capable of a surprisingly rich repertoire of behaviors including navigation and foraging, mating, learning, and even rudimentary social behavior (aggregation)
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