ArticleThe Journal of neuroscience : the official journal of the Society for Neuroscience2014
Action potential energetics at the organismal level reveal a trade-off in efficiency at high firing rates.
Article in The Journal of neuroscience : the official journal of the Society for Neuroscience, 2014. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 24 papers.
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24 citing papers in PubMed.
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- Protective down-regulated states in the human brain: A possible lesson from COVID-19.Proceedings of the National Academy of Sciences of the United States of America · 2022Article
- Morphology and receptive field organization of a temporal processing region in Apteronotus albifrons.Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology · 2022Article
- Reintegrating Biology Through the Nexus of Energy, Information, and Matter.Integrative and comparative biology · 2022Article
- Derived loss of signal complexity and plasticity in a genus of weakly electric fish.The Journal of experimental biology · 2021Article
- Studying convergent evolution to relate genotype to behavioral phenotype.The Journal of experimental biology · 2020Review
- Convergent patterns of evolution of mitochondrial oxidative phosphorylation (OXPHOS) genes in electric fishes.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2020Article
- Function and energy consumption constrain neuronal biophysics in a canonical computation: Coincidence detection.PLoS computational biology · 2018Article
- Rapid evolution of a voltage-gated sodium channel gene in a lineage of electric fish leads to a persistent sodium current.PLoS biology · 2018Article
- The complexity of high-frequency electric fields degrades electrosensory inputs: implications for the jamming avoidance response in weakly electric fish.Journal of the Royal Society, Interface · 2018Article
- Article
- Massive increase in visual range preceded the origin of terrestrial vertebrates.Proceedings of the National Academy of Sciences of the United States of America · 2017Article
- Cable energy function of cortical axons.Scientific reports · 2016Article
- Leaping eels electrify threats, supporting Humboldt's account of a battle with horses.Proceedings of the National Academy of Sciences of the United States of America · 2016Article
- Individual Neuronal Subtypes Exhibit Diversity in CNS Myelination Mediated by Synaptic Vesicle Release.Current biology : CB · 2016Article
- Energy-efficient population coding constrains network size of a neuronal array system.Scientific reports · 2016Article
- Metabolic Energy of Action Potentials Modulated by Spike Frequency Adaptation.Frontiers in neuroscience · 2016Article
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5 authors.
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Abstract
The energetic costs of action potential (AP) production constrain the evolution of neural codes and brain networks. Cellular-level estimates of AP-related costs are typically based on voltage-dependent Na(+) currents that drive active transport by the Na(+)/K(+) ATPase to maintain the Na(+) and K(+) ion concentration gradients necessary for AP production. However, these estimates of AP cost have not been verified at the organismal level. Electric signaling in the weakly electric fish Eigenmannia virescens requires that specialized cells in an electric organ generate APs with large Na(+) currents at high rates (200-600 Hz). We measured these currents using a voltage-clamp protocol and then estimated the energetic cost at the cellular level using standard methods. We then used this energy-intensive signaling behavior to measure changes in whole-animal energetics for small changes in electric discharge rate. At low rates, the whole-animal measure of AP cost was similar to our cellular-level estimates. However, AP cost increased nonlinearly with increasing firing rates. We show, with a biophysical model, that this nonlinearity can arise from the increasing cost of maintaining AP amplitude at high rates. Our results confirm that estimates of energetic costs based on Na(+) influx are appropriate for low baseline firing rates, but that extrapolating to high firing rates may underestimate true costs in cases in which AP amplitude does not decrease. Moreover, the trade-off between energetic cost and firing rate suggests an additional constraint on the evolution of high-frequency signaling in neuronal systems.
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