Nematode locomotion: dissecting the neuronal–environmental loop

Abstract

With a fully reconstructed and extensively characterized neural circuit, the nematode Caenorhabditis elegans is a promising model system for integrating our understanding of neuronal, circuit and whole-animal dynamics. Fundamental to addressing this challenge is the need to consider the tight neuronal-environmental coupling that allows the animal to survive and adapt to changing conditions. Locomotion behaviors are affected by environmental variables both at the biomechanical level and via adaptive sensory responses that drive and modulate premotor and motor circuits. Here we review significant advances in our understanding of proprioceptive control of locomotion, and more abstract models of spatial orientation and navigation. The growing evidence of the complexity of the underlying circuits suggests that the intuition gained is but the first step in elucidating the secrets of neural computation in this relatively simple system. http://dx.doi.org/10. 1016/j.conb.2013.12.003 Introduction To survive, animals process sensory information to drive motor behaviors and to move about their environment. Among locomotion strategies, undulations are remarkably effective across scales and in a variety of environments [1][2][3]. Common to most locomotion and to undulationbased strategies, in particular, is the tight neuronalenvironmental loop, in which the shape of the body and the way in which the sensory organs sample the environment are integral to the neural dynamics. The nematode Caenorhabditis elegans (C. elegans) is a powerful system in which to study this loop, due to its small nervous system and experimental tractability. Indeed, with a largely specified neural circuit and rapidly advancing technologies for recording and manipulating neuronal activity [4 ,5], significant progress is being made in deciphering the dynamics this neural circuit supports.Here we review recent progress in understanding the motor programs underpinning undulatory locomotion as well as higher level command of locomotion primitives and sensorimotor programs in C. elegans. We discuss how progress in understanding the neuronal-environmental loop is contributing to the ongoing effort and fundamental challenges in assembling a whole animal model of C. elegans behavior. The ventral nerve cordC. elegans is a small (1 mm long) unsegmented worm with 302 nerve cells [6][7][8]. The animal's undulations are controlled by head and ventral nerve cord (VNC) circuits. Extensive characterization of defects (through ablation of individual classes of neurons) [9][10][11] has provided a strong basis for an intuitive understanding of the operation of this otherwise irregular circuit architecture [12 ,13]. Indeed, evidence suggests that semi-independent VNC subcircuits control forward and backward locomotion [6,14,15,16 ,17 ,18 ,19 ] and are gated by distinct premotor (so-called command) interneurons. The forward locomotion circuit in the ventral nerve cordIn forward locomotion, cholinergic motor neurons excite muscles on either side of the body while ...

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