C. elegansenteric motor neurons fire synchronized action potentials underlying the defecation motor program

Abstract

The C. elegans nervous system was thought to be strictly analog, constituted solely by graded neurons. We recently discovered neuronal action potentials in the sensory neuron AWA; however, the extent to which the C. elegans nervous system relies on analog or digital neural signaling and coding is unclear. Here we report that the enteric motor neurons AVL and DVB fire all-or-none calcium-mediated action potentials that play essential roles in the rhythmic defecation behavior in C. elegans. Both AVL and DVB synchronously fire giant action potentials to faithfully execute all-or-none expulsion following the intestinal pacemaker. AVL fires unusual compound action potentials with each positive calcium-mediated spike followed by a potassium-mediated negative spike. The depolarizing calcium spikes in AVL are mediated by a CaV2 calcium channel UNC-2, while the negative potassium spikes are mediated by a repolarization-activated potassium channel EXP-2. Whole-body behavior tracking and simultaneous neural imaging in free-moving animals suggest that action potentials initiated in AVL in the head propagate along its axon to the tail and activate DVB through the INX-1 gap junction. Synchronized action potential spikes between AVL and DVB, as well as the negative spike and long-lasting afterhyperpolarization in AVL, play an important function in executing expulsion behavior. This work provides the first evidence that in addition to sensory coding, C. elegans motor neurons also use digital coding scheme to perform specific functions including long-distance communication and temporal synchronization, suggesting further, unforeseen electrophysiological diversity remains to be discovered in the C. elegans nervous system.

A Leak K+Channel TWK-40 Regulates Rhythmic Motor Program inC. elegans

“…The recent descriptions of synchronized giant action potentials between AVL and DVB, and of unusual compound action potentials in AVL, provide insights into how the rhythmic expulsion behaviour is generated at the cellular level. In particular, the negative potassium spikes in AVL are mediated by a repolarization-activated potassium channel EXP-2 (Jiang et al, 2021). Yet, no ion channel had been associated so far with the rhythmic activity of DVB.…”

“…To directly investigate the functional effect of twk-40, we dissected and recorded GFP-labeled DVB neurons in vivo in the whole-cell patch clamp configuration (Methods, Figure 5A). In wild-type animals, stable outward K + currents were recorded at stepwise holding voltages from -60 mV to +80 mV (Xie et al, 2013;Jiang et al, 2021). These currents were significantly diminished in twk-40(hp834) loss-of-function mutants (Figure 5B, C).…”