Abstract

Neurons utilize bursts of action potentials as an efficient and reliable way to encode information. It is likely that the intrinsic membrane properties of neurons involved in burst generation may also participate in preserving its temporal features. Here we examined the contribution of the persistent and resurgent components of voltage-gated Na+ currents in modulating the burst discharge in sensory neurons. Using mathematical modeling, theory and dynamic-clamp electrophysiology, we show that, distinct from the persistent Na+ component which is important for membrane resonance and burst generation, the resurgent Na+ can help stabilize burst timing features including the duration and intervals. Moreover, such a physiological role for the resurgent Na+ offered noise tolerance and preserved the regularity of burst patterns. Model analysis further predicted a negative feedback loop between the persistent and resurgent gating variables which mediate such gain in burst stability. These results highlight a novel role for the voltage-gated resurgent Na+ component in moderating the entropy of burst-encoded neural information.

Highlights

  • Real-time signal detection in uncertain settings is a fundamental problem for information and communication systems

  • Ion channels important for spike generation can serve as noise modulators in sensory neurons

  • Mathematical models of bursting have helped explain the basic structure of an underlying dynamical system as one in which a slow process dynamically modulates a faster action potential/spike-generating process, leading to stereotypical alternating phases of spiking and quiescence[2, 3]

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Summary

Author Summary

The nervous system extracts meaningful information from natural environments to guide precise behaviors. Ion channels important for spike generation can serve as noise modulators in sensory neurons. We developed and utilized mathematical models for the different experimentally inseparable components of a complex Na+ channel current. This enabled phenomenological simplification and examination of the individual roles of Na+ components in spike timing control. We further utilized real-time closed-loop experiments to validate model predictions, and theoretical analysis to explain experimental outcomes. Using such multifaceted approach, we uncovered a novel role for a resurgent Na + component in enhancing the reliability of spike timing and in noise modulation.

Introduction
Figures and Legends
Methods
Findings
Potassium and leak currents

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