C. elegans AWA Olfactory Neurons Fire Calcium-Mediated All-or-None Action Potentials

Neurons in Caenorhabditis elegans and other nematodes have been thought to lack classical action potentials. Unexpectedly, we observe membrane potential spikes with defining characteristics of action potentials in C. elegans AWA olfactory neurons recorded under current-clamp conditions. Ion substitution experiments, mutant analysis, pharmacology, and modeling indicate that AWA fires calcium spikes, which are initiated by EGL-19 voltage-gated CaV1 calcium channels and terminated by SHK-1 Shaker-type potassium channels. AWA action potentials result in characteristic signals in calcium imaging experiments. These calcium signals are also observed when intact animals are exposed to odors, suggesting that natural odor stimuli induce AWA spiking. The stimuli that elicit action potentials match AWA’s specialized function in climbing odor gradients. Our results provide evidence that C. elegans neurons can encode information through regenerative all-or-none action potentials, expand the computational repertoire of its nervous system, and inform future modeling of its neural coding and network dynamics. [Display omitted] •Certain olfactory neurons in C. elegans fire action potentials, contrary to dogma•Voltage-gated calcium and potassium channels shape action potential dynamics•The stimuli that induce spiking have a minimum duration and defined amplitudes•Spikes may encode natural odor stimuli to support gradient climbing behavior Although all-or-none action potentials are crucial for information processing in many animals, identifying them in the C. elegans nervous system, where they had not previously been observed, will allow them to be studied in concert with other models.