Biophysical Insights into How Spike Threshold Depends on the Rate of Membrane Potential Depolarization in Type I and Type II Neurons

PLoS One. 2015 Jun 17;10(6):e0130250. doi: 10.1371/journal.pone.0130250. eCollection 2015.

Abstract

Dynamic spike threshold plays a critical role in neuronal input-output relations. In many neurons, the threshold potential depends on the rate of membrane potential depolarization (dV/dt) preceding a spike. There are two basic classes of neural excitability, i.e., Type I and Type II, according to input-output properties. Although the dynamical and biophysical basis of their spike initiation has been established, the spike threshold dynamic for each cell type has not been well described. Here, we use a biophysical model to investigate how spike threshold depends on dV/dt in two types of neuron. It is observed that Type II spike threshold is more depolarized and more sensitive to dV/dt than Type I. With phase plane analysis, we show that each threshold dynamic arises from the different separatrix and K+ current kinetics. By analyzing subthreshold properties of membrane currents, we find the activation of hyperpolarizing current prior to spike initiation is a major factor that regulates the threshold dynamics. The outward K+ current in Type I neuron does not activate at the perithresholds, which makes its spike threshold insensitive to dV/dt. The Type II K+ current activates prior to spike initiation and there is a large net hyperpolarizing current at the perithresholds, which results in a depolarized threshold as well as a pronounced threshold dynamic. These predictions are further attested in several other functionally equivalent cases of neural excitability. Our study provides a fundamental description about how intrinsic biophysical properties contribute to the threshold dynamics in Type I and Type II neurons, which could decipher their significant functions in neural coding.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Kinetics
  • Membrane Potentials*
  • Models, Neurological*
  • Neurons / cytology*
  • Neurons / metabolism
  • Sodium / metabolism

Substances

  • Sodium

Grants and funding

This work is supported by the National Natural Science Foundation of China under Grants 61172009 and 61372010, and Tianjin Municipal Natural Science Foundation under Grants 12JCZDJC21100 and 13JCZDJC27900. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.