Metabolic Energy of Action Potentials Modulated by Spike Frequency Adaptation.

Guo-Sheng Yi,Hui-Yan Li,Bin Deng,Jiang Wang,Xi-Le Wei

doi:10.3389/fnins.2016.00534

Guo-Sheng Yi, Hui-Yan Li + Show 3 more

Open Access

https://doi.org/10.3389/fnins.2016.00534

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Abstract

Spike frequency adaptation (SFA) exists in many types of neurons, which has been demonstrated to improve their abilities to process incoming information by synapses. The major carrier used by a neuron to convey synaptic signals is the sequences of action potentials (APs), which have to consume substantial metabolic energies to initiate and propagate. Here we use conductance-based models to investigate how SFA modulates the AP-related energy of neurons. The SFA is attributed to either calcium-activated K+ (IAHP) or voltage-activated K+ (IM) current. We observe that the activation of IAHP or IM increases the Na+ load used for depolarizing membrane, while produces few effects on the falling phase of AP. Then, the metabolic energy involved in Na+ current significantly increases from one AP to the next, while for K+ current it is less affected. As a consequence, the total energy cost by each AP gets larger as firing rate decays down. It is also shown that the minimum Na+ charge needed for the depolarization of each AP is unaffected during the course of SFA. This indicates that the activation of either adaptation current makes APs become less efficient to use Na+ influx for their depolarization. Further, our simulations demonstrate that the different biophysical properties of IM and IAHP result in distinct modulations of metabolic energy usage for APs. These investigations provide a fundamental link between adaptation currents and neuronal energetics, which could facilitate to interpret how SFA participates in neuronal information processing.

Highlights

By determining the energy cost of each action potentials (APs) in the simulated spike train, we find that the activation of IAHP current results in the increase of total metabolic energy consumed by an AP during the course of Spike frequency adaptation (SFA) (Figure 9D)
The SFA is generated by incorporating an adaptation current, i.e., include M-type current (IM) or IAHP, in the model
Our simulations show that the activation of IM or IAHP both causes the increase in the energy cost of AP as it reduces firing rate

Summary

Introduction

Neurons in the central nervous system (CNS) have powerful ability to encode and conduct afferent information, which requires enormous amounts of metabolic energy to realize this function (Attwell and Laughlin, 2001; Alle et al, 2009; Harris et al, 2012; Bowie and Attwell, 2015). As the activation of IM reduces firing rate, the Na+ influx becomes less efficient in inducing the depolarization of AP since it has to compete with this adaptation current, which is just like it does during the overlap with the repolarizing IK. By determining the energy cost of each AP in the simulated spike train, we find that the activation of IAHP current results in the increase of total metabolic energy consumed by an AP during the course of SFA (Figure 9D).

Results

Conclusion