Metabolic cost as a unifying principle governing neuronal biophysics
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 en...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 107; no. 27; pp. 12329 - 12334 |
|---|---|
| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
06.07.2010
National Acad Sciences |
| Subjects | |
| Online Access | Get full text |
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| 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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| AbstractList | 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. 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.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. 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. [PUBLICATION ABSTRACT] |
| Author | Sejnowski, Terrence J. Marder, Eve Otte, Stephani Callaway, Edward Hasenstaub, Andrea |
| Author_xml | – sequence: 1 givenname: Andrea surname: Hasenstaub fullname: Hasenstaub, Andrea – sequence: 2 givenname: Stephani surname: Otte fullname: Otte, Stephani – sequence: 3 givenname: Edward surname: Callaway fullname: Callaway, Edward – sequence: 4 givenname: Terrence J. surname: Sejnowski fullname: Sejnowski, Terrence J. – sequence: 5 givenname: Eve surname: Marder fullname: Marder, Eve |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20616090$$D View this record in MEDLINE/PubMed |
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| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 Author contributions: A.H. and S.O. designed research; A.H. and S.O. performed research; A.H. contributed new reagents/analytic tools; A.H. analyzed data; and A.H., S.O., E.C., and T.J.S. wrote the paper. Edited by Eve Marder, Brandeis University, Waltham, MA, and approved May 17, 2010 (received for review December 24, 2009) |
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| SubjectTerms | Action potentials Action Potentials - physiology Algorithms Animals Biological Sciences Biophysics Brain Brain - cytology Computer Simulation Cost functions Energy energy expenditure Energy Metabolism interneurons Ion channels Ion Channels - physiology Kinetics Membrane Potentials - physiology Metabolism Mice Mice, Inbred C57BL Minimization of cost Models, Neurological Neurons Neurons - metabolism Neurons - physiology Patch-Clamp Techniques Potassium - metabolism Potassium channels Potassium Channels - physiology Sodium Sodium - metabolism Sodium channels Sodium Channels - physiology Sodium-Potassium-Exchanging ATPase - metabolism |
| Title | Metabolic cost as a unifying principle governing neuronal biophysics |
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