Cited by 248Ion channel regulation and functionNeural dynamics and brain functionNeuroscience and Neuropharmacology Research

Metabolic cost as a unifying principle governing neuronal biophysics.

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Hasenstaub, Andrea, Otte, Stephani, Callaway, Edward, Sejnowski, Terrence J.·2010·Proceedings of the National Academy of Sciences

Abstract

The brain contains an astonishing diversity of neurons, each expressing only one set of ion channels out of the billions of potential channel combinations. Simple organizing principles are required for us to make sense of this abundance of possibilities and wealth of related data. We suggest that energy minimization subject to functional constraints may be one such unifying principle. We compared the energy needed to produce action potentials singly and in trains for a wide range of channel densities and kinetic parameters and examined which combinations of parameters maximized spiking function while minimizing energetic cost. We confirmed these results for sodium channels using a dynamic current clamp in neocortical fast spiking interneurons. We find further evidence supporting this hypothesis in a wide range of other neurons from several species and conclude that the ion channels in these neurons minimize energy expenditure in their normal range of spiking.

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Crossref · 10.1073/pnas.0914886107

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  • PV cells are particularly susceptible to oxidative stress given their fast cellular metabolism and increased mitochondrial function.

    “PV cells are particularly susceptible to oxidative stress given their fast cellular metabolism and increased mitochondrial function (Hasenstaub et al., 2010; Kann et al., 2014; Inan et al., 2016).”

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Authors
Hasenstaub, A., Otte, S., Callaway, E., & Sejnowski, T. J.
Affiliations
  • Salk Institute for Biological Studies (US)
  • Crick–Jacobs Center for Theoretical and Computational Biology, Salk Institute for Biological Studies, La Jolla, CA 92037; and
Venue
Proceedings of the National Academy of Sciences
Published
2010-06-23
Volume
107
Issue
27
Pages
12329-12334
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2164189343
Cited by
246
References
72
Citations by year
2026: 11 · 2025: 13 · 2024: 11 · 2023: 19 · 2022: 21 · 2021: 22 · 2020: 25 · 2019: 14 · 2018: 13 · 2017: 15 · 2016: 16 · 2015: 17 · 2014: 9 · 2013: 11 · 2012: 22
FWCI
5.21
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Howard Hughes Medical Institute
  • Francis Crick Institute
  • National Institutes of Health
  • National Institute of Mental Health (MH063912, R01MH063912)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
metabolic cost, energy minimization, ion channel density, sodium channels, action potential trains, fast-spiking interneurons, neocortex, channel kinetics, energy expenditure
MeSH terms
Action Potentials, Sodium-Potassium-Exchanging ATPase, Algorithms, Animals, Brain, Computer Simulation, Energy Metabolism, Ion Channels, Kinetics, Membrane Potentials, Mice, Inbred C57BL, Models, Neurological, Neurons, Potassium, Sodium, Potassium Channels, Sodium Channels, Patch-Clamp Techniques, Mice

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