Action potentials contribute to neuronal signaling in C. elegans

Abstract

Small, high-impedance neurons with short processes, similar to those found in the soil nematode Caenorhabditis elegans, are predicted to transmit electrical signals by passive propagation. However, we have found that certain neurons in C. elegans fire regenerative action potentials. These neurons resembled Schmitt triggers, as their potential state appears to be bistable. Transitions between up and down states could be triggered by application of the neurotransmitter glutamate or brief current pulses.

Figure 1

The RMD neuron fires action potentials and exhibits bistability. (a, b) Current-clamp records from the RMD (a) and AVA (b) neurons. Voltage (top) in response to a ramp of injected current (bottom). (c, d) Voltage responses to small hyperpolarizing and depolarizing current-steps in RMD (c) and AVA (d). (e, f) Voltage when zero holding current in RMD (e) and AVA (f). Transgenic worms that expressed GFP under the regulation of the glr-1 promoter (pDM1286) were used for in vivo electrophysiological experiments. Electrophysiological recordings from the RMD and AVA neurons in vivo were made as previously described .

Figure 2

Action potentials in RMD depend on external Ca²⁺. (a, b) Action potentials measured in RMD in response to steps of depolarizing current in either normal ECF (top), Na⁺-free ECF (a) or Na⁺/Ca²⁺-free ECF (b) (middle), followed by a return to normal ECF (bottom).

Figure 3

Mutations in either voltage-gated or voltage-insensitive cation channels do not eliminate action potentials in RMD. (a, b, d–f) Action potentials measured in RMD in response to steps of depolarizing current in either wild-type (a) or mutant worms (b, d–f). (c) Bistable hyperpolarized and depolarized states in RMD of unc-2(e55) mutants held at 0 pA current. (g) RMD sustained voltage response to brief applications of 1 Mm glutamate. Membrane potential switched back to approximately −75 mV (vertical arrow) following a 4 second step of hyperpolarizing current. (h) RMD current injections (10 ms), simulating inhibitory synaptic currents, switch the membrane potential to a hyperpolarized state. (i) AVA transient voltage response to brief applications of 1 mM glutamate. In (g) and (i) the short, horizontal bars indicate pressure application of glutamate in a continuous flowing bath.