State and location dependence of action potential metabolic cost in cortical pyramidal neurons

Stefan Hallermann, Christiaan P.J. De Kock, Greg J. Stuart, Maarten H.P. Kole*

*Corresponding author for this work

    Research output: Contribution to journalArticlepeer-review

    110 Citations (Scopus)

    Abstract

    Action potential generation and conduction requires large quantities of energy to restore Na + and K + ion gradients. We investigated the subcellular location and voltage dependence of this metabolic cost in rat neocortical pyramidal neurons. Using Na +K + charge overlap as a measure of action potential energy efficiency, we found that action potential initiation in the axon initial segment (AIS) and forward propagation into the axon were energetically inefficient, depending on the resting membrane potential. In contrast, action potential backpropagation into dendrites was efficient. Computer simulations predicted that, although the AIS and nodes of Ranvier had the highest metabolic cost per membrane area, action potential backpropagation into the dendrites and forward propagation into axon collaterals dominated energy consumption in cortical pyramidal neurons. Finally, we found that the high metabolic cost of action potential initiation and propagation down the axon is a trade-off between energy minimization and maximization of the conduction reliability of high-frequency action potentials.

    Original languageEnglish
    Pages (from-to)1007-1014
    Number of pages8
    JournalNature Neuroscience
    Volume15
    Issue number7
    DOIs
    Publication statusPublished - Jul 2012

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