Metabolic efficiency with fast spiking in the squid axon

Abdelmalik Moujahid,Alicia D'Anjou

doi:10.3389/fncom.2012.00095

Abstract

Fundamentally, action potentials in the squid axon are consequence of the entrance of sodium ions during the depolarization of the rising phase of the spike mediated by the outflow of potassium ions during the hyperpolarization of the falling phase. Perfect metabolic efficiency with a minimum charge needed for the change in voltage during the action potential would confine sodium entry to the rising phase and potassium efflux to the falling phase. However, because sodium channels remain open to a significant extent during the falling phase, a certain overlap of inward and outward currents is observed. In this work we investigate the impact of ion overlap on the number of the adenosine triphosphate (ATP) molecules and energy cost required per action potential as a function of the temperature in a Hodgkin–Huxley model. Based on a recent approach to computing the energy cost of neuronal action potential generation not based on ion counting, we show that increased firing frequencies induced by higher temperatures imply more efficient use of sodium entry, and then a decrease in the metabolic energy cost required to restore the concentration gradients after an action potential. Also, we determine values of sodium conductance at which the hydrolysis efficiency presents a clear minimum.

Highlights

The generation of action potentials in mammalian neurons involves the flux of different ions such as sodium, potassium, and calcium across the cell membrane
Based on biophysical considerations about the nature of the Hodgkin–Huxley model, we have recently found an analytical expression of the electrochemical energy involved in the dynamics of the model, which provides a new approach for estimating the energy consumption during the resting and active states of neurons (Moujahid et al, 2011)
In this work we investigate the impact of ion currents overlapping on the number of adenosine triphosphate (ATP) molecules required to restore the concentration gradients after an action potential in the Hodgkin–Huxley model

Summary

INTRODUCTION

The generation of action potentials in mammalian neurons involves the flux of different ions such as sodium, potassium, and calcium across the cell membrane. Because the observed overlap is temperature-dependent, we have computed the number of ATP molecules per action potential and its corresponding energy cost at different values of temperature Both the classic study by Hodgkin and Huxley of the squid axon (Hodgkin, 1975), and other recent works (Attwell and Laughlin, 2001; Lennie, 2003) assume that the action potential requires four times Na+ charge compared to the charge needed for the change in voltage.

MATERIALS AND METHODS

ION CURRENTS OVERLAPPING

ENERGY EFFICIENCY

DISCUSSIONS