Voltage- and Calcium-Gated Membrane Currents Tune the Plateau Potential Properties of Multiple Neuron Types

Authors

Curtis L Neveu
Paul Smolen
Douglas A Baxter
John H Byrne

Publication Date

11-8-2023

Journal

The Journal of Neuroscience

Abstract

Many neurons exhibit regular firing that is limited to the duration and intensity of depolarizing stimuli. However, some neurons exhibit all-or-nothing plateau potentials that, once elicited, can lead to prolonged activity that is independent of stimulus intensity or duration. To better understand this diversity of information processing, we compared the voltage-gated and Ca²⁺-gated currents of three identified neurons from hermaphroditic Aplysia californica. Two of these neurons, B51 and B64, generated plateau potentials and a third neuron, B8, exhibited regular firing and was incapable of generating a plateau potential. With the exception of the Ca²⁺-gated potassium current (I_KCa), all three neuron types expressed a similar array of outward and inward currents, but with distinct voltage-dependent properties for each neuron type. Inhibiting voltage-gated Ca²⁺ channels with Ni⁺ prolonged the plateau potential, indicating I_KCa is important for plateau potential termination. In contrast, inhibiting persistent Na⁺ (I_NaP) blocked plateau potentials, empirically and in simulations. Surprisingly, the properties and level of expression of I_NaP were similar in all three neurons, indicating that the presence of I_NaP does not distinguish between regular-firing neurons and neurons capable of generating plateau potentials. Rather, the key distinguishing factor is the relationship between I_NaP and outward currents such as the delayed outward current (I_D), and I_KCa. We then demonstrated a technique for predicting complex physiological properties such as plateau duration, plateau amplitude, and action potential duration as a function of parameter values, by fitting a curve in parameter space and projecting the curve beyond the tested values.

SIGNIFICANCE STATEMENT Plateau potentials are intrinsic properties of neurons that are important for information processing in a wide variety of nervous systems. We examined three identified neurons in Aplysia californica with different propensities to generate a plateau potential. No single conductance was found to distinguish plateau generating neurons. Instead, plateau generation depended on the ratio between persistent Na⁺ current (I_NaP), which favored plateaus, and outward currents such as I_KCa, which facilitated plateau termination. Computational models revealed a relationship between the individual currents that predicted the features of simulated plateau potentials. These results provide a more solid understanding of the conductances that mediate plateau generation.

Keywords

Calcium, Neurons, Action Potentials, Aplysia, KCa, persistent sodium, plateau potential, SNNAP