C. elegans relies on sensory cues to find food. In the absence of such cues, the worm might display defined search patterns or other stereotyped behavior. We sought to characterize the motion of C. elegans in the absence of stimuli, over time scales comparable to that of starvation. To this end, we devised an imaging setup employing several flatbed scanners, which enables us to collect animals' paths over large (24 cm x 24 cm) surfaces. Wild-type worms display striking behavior in the absence of food. ~60% of the animals' paths display persistence in the direction of motion over length scales that are 50-100 times the body-length of C. elegans. The direction of movement differs from animal to animal, suggesting that the bias we observe might not represent a taxis towards an external cue. We confirmed these results with a camera imaging setup, in a more stringently homogeneous environment. Interestingly, directionality does not appear to arise from local correlation in the direction of motion. Furthermore, synthetic trajectories generated from the same angle and step distributions of individual trajectories indicate that the observed persistence in direction cannot be accounted for by simple random walk models. To determine whether sensory input is required for directionality, we analyzed the paths of sensory mutants.
che-2 animals, which display cilia defects, exhibit non-directional behavior. Surprisingly, however, ~20% of
daf-19 mutants, which lack cilia, display directionality. Mutations in
osm-9, a TRPV channel required in several sensory neurons, do not affect behavior. By contrast, mutations in the cGMP-gated channel
tax-4 result in loss of directionality, indicating a requirement for the activity of sensory neurons. To further investigate the role of sensory perception we performed rescue experiments of TAX-4 function. No rescue is observed when driving TAX-4 in the thermosensory neuron AFD or in the olfactory neurons AWB and AWC. Moreover, mutants defective in signal transduction for thermotaxis, odortaxis, phototaxis, and aerotaxis do not display loss of directionality. We observe partial rescue of directionality when driving TAX-4 in a set of five cells: the oxygen-sensing AQR, PQR and URX neurons and the ASJ and ASK neurons. In conclusion, our results suggest that the motion of C. elegans in the absence of apparent sensory cues cannot be assimilated to a random walk, and raise the intriguing speculative possibility that C. elegans might achieve directional motion by relying solely on self-based information.