Inactivation of voltage-activated Na⁺ currents contributes to different adaptation properties of paired mechanosensory neurons

Voltage-activated sodium current (I_Na) is primarily responsible for the leading edge of the action potential in many neurons. While I_Na generally activates rapidly when a neuron is depolarized, its inactivation properties differ significantly between different neurons and even within one neuron, where I_Na often has slowly and rapidly inactivating components. I_Na inactivation has been suggested to regulate action potential firing frequency in some cells, but no clear picture of this relationship has emerged. We studied I_Na in both members of the paired mechanosensory neurons of a spider slit-sense organ, where one neuron adapts rapidly (type A) and the other slowly (type B) in response to a step depolarization. In both neuron types I_Na activated and inactivated with single time constants of 2-3 ms and 5-10 ms, respectively, varying with the stimulus intensity. However, there was a clear difference in the steady-state inactivation properties of the two neuron types, with the half-maximal inactivation (V₅₀) being -40.1 mV in type A neurons and -58.1 mV in type B neurons. Therefore I_Na inactivated closer to the resting potential in the more slowly adapting neurons. I_Na also recovered from inactivation significantly faster in type B than type A neurons, and the recovery was dependent on conditioning voltage. These results suggest that while the rate of I_Na inactivation is not responsible for the difference in the adaptation behavior of these two neuron types, the rate of recovery from inactivation may play a major role. Inactivation at lower potentials could therefore be crucial for more rapid recovery.