Analog transmission of action potential fine structure in spiral ganglion axons

Action potential waveforms generated at the axon initial segment (AIS) are specialized between and within neuronal classes. But is the fine structure of each electrical event retained when transmitted along myelinated axons or is it rapidly and uniformly transmitted to be modified again at the axon terminal? To address this issue, action potential axonal transmission was evaluated in a class of primary sensory afferents that possess numerous types of voltage-gated ion channels underlying a complex repertoire of endogenous firing patterns. In addition to their signature intrinsic electrophysiological heterogeneity, spiral ganglion neurons are uniquely designed. The bipolar, myelinated somata of type I neurons are located within the conduction pathway, requiring that action potentials generated at the first heminode must be conducted through their electrically excitable membrane. We used this unusual axonal-like morphology to serve as a window into action potential transmission to compare locally evoked action potential profiles to those generated peripherally at their glutamatergic synaptic connections with hair cell receptors. These comparisons showed that the distinctively shaped somatic action potentials were highly correlated with the nodally generated, invading ones for each neuron. This result indicates that the fine structure of the action potential waveform is maintained axonally, thus supporting the concept that analog signaling is incorporated into each digitally transmitted action potential in the specialized primary auditory afferents.NEW & NOTEWORTHY Diverse action potential shapes and kinetics resulting from dynamic heterogeneity in spiral ganglion neurons are axonally transmitted as multiplexed signals that retain the fine structure of each distinctive waveform within a digital code.