A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue

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Abstract
Proprioception, the sense of self, is essential for our daily life. For example, we count on proprioception to ‘feel’ our body position in space and guide how much to extend our arms and legs. A study of the roundworm C. elegans shows that it uses proprioception to control its body posture and position during locomotion. This requires a single proprioceptor neuron and a mechanosensitive ion channel functioning in this neuron. Interestingly, this C. elegans neuron is functionally analogous to human muscle spindles and Golgi tendon organs that are important for controlling arm and leg movements. These results suggest that the basic principles of proprioception are evolutionarily conserved between C. elegans and humans, and indicate that C. elegans can be a valuable model organism for studying proprioception and its related human diseases. The nematode Caenorhabditis elegans is commonly used as a genetic model organism for dissecting integration of the sensory and motor systems1. Despite extensive genetic and behavioural analyses that have led to the identification of many genes and neural circuits involved in regulating C. elegans locomotion behaviour1, it remains unclear whether and how somatosensory feedback modulates motor output during locomotion. In particular, no stretch receptors have been identified in C. elegans, raising the issue of whether stretch-receptor-mediated proprioception is used by C. elegans to regulate its locomotion behaviour. Here we have characterized TRP-4, the C. elegans homologue of the mechanosensitive TRPN channel. We show that trp-4 mutant worms bend their body abnormally, exhibiting a body posture distinct from that of wild-type worms during locomotion, suggesting that TRP-4 is involved in stretch-receptor-mediated proprioception. We show that TRP-4 acts in a single neuron, DVA, to mediate its function in proprioception, and that the activity of DVA can be stimulated by body stretch. DVA both positively and negatively modulates locomotion, providing a unique mechanism whereby a single neuron can fine-tune motor activity. Thus, DVA represents a stretch receptor neuron that regulates sensory–motor integration during C. elegans locomotion.