Ionic mechanisms of microsecond-scale spike timing in single cells.

Electric fish image their environments and communicate by generating electric organ discharges through the simultaneous action potentials (APs) of electric organ cells (electrocytes) in the periphery. Steatogenys elegans generates a biphasic electrocyte discharge by the precisely regulated timing and waveform of APs generated from two excitable membranes present in each electrocyte. Current-clamp recordings of electrocyte APs reveal that the posterior membrane fires first, followed ∼30 μs later by an AP on the anterior membrane. This delay was maintained even as the onset of the first AP was advanced >5 ms by increasing stimulus intensity and across multiple spikes during bursts of APs elicited by prolonged stimulation. Simultaneous cell-attached loose-patch recordings of Na(+) currents on each membrane revealed that activation voltage for Na(+) channels on the posterior membrane was 10 mV hyperpolarized compared with Na(+) channels on the anterior membrane, with no differences in activation or inactivation kinetics. Computational simulations of electrocyte APs demonstrated that this difference in Na(+) current activation voltage was sufficient to maintain the proper firing order and the interspike delay. A similar difference in activation threshold has been reported for the Na(+) currents of the axon initial segment compared with somatic Na(+) channels of pyramidal neurons, suggesting convergent evolution of spike initiation and timing mechanisms across different systems of excitable cells.