Energy-Efficient Action Potentials in Hippocampal Mossy Fibers

Alle, Henrik; Roth, Arnd; Geiger, Jörg R. P.

doi:10.1126/science.1174331

Cited by 375 publications

(394 citation statements)

References 23 publications

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“…5) it makes a metabolic consumption of about 31 × 10 11 ATP per cm 2 of membrane to generate a single action potential. This result is 10 times greater than the 3.19 × 10 11 ATP per cm 2 reported by Alle et al [4] to generate an action potential in the rat mossy fiber at 37…”

Section: B Energymentioning

confidence: 62%

“…This calculated Na + provides an estimate of the number of pump cycles, or ATP molecules, that the pump will need to reestablish the resting state of the neuron. However, this estimation is the subject of controversy [4]. Inward Na + and outward K + overlap during the action potential generation, introducing an uncertainty in the calculation of sodium ions up to a factor of 4 [1,[5][6][7].…”

Section: Introductionmentioning

confidence: 99%

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Energy and information in Hodgkin-Huxley neurons

2011

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The generation of spikes by neurons is energetically a costly process and the evaluation of the metabolic energy required to maintain the signaling activity of neurons a challenge of practical interest. Neuron models are frequently used to represent the dynamics of real neurons but hardly ever to evaluate the electrochemical energy required to maintain that dynamics. This paper discusses the interpretation of a Hodgkin-Huxley circuit as an energy model for real biological neurons and uses it to evaluate the consumption of metabolic energy in the transmission of information between neurons coupled by electrical synapses, i.e., gap junctions. We show that for a single postsynaptic neuron maximum energy efficiency, measured in bits of mutual information per molecule of adenosine triphosphate (ATP) consumed, requires maximum energy consumption. For groups of parallel postsynaptic neurons we determine values of the synaptic conductance at which the energy efficiency of the transmission presents clear maxima at relatively very low values of metabolic energy consumption. Contrary to what could be expected, the best performance occurs at a low energy cost.

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Section: B Energymentioning

confidence: 62%

Section: Introductionmentioning

confidence: 99%

Energy and information in Hodgkin-Huxley neurons

2011

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“…Importantly, the conduction velocity of fast-spiking interneurons is higher than that of unmyelinated axons of principal cells . This is achieved by a 'supercritical' density of voltagegated Na + -channels all over the unmyelinated axon that results in high Na + -conductance density as well as a larger overlap of depolarizing Na + -entry and repolarizing K + -efflux ('sodium entry ratio' of about 1.98), which differs markedly from cortical principal cells (Alle et al, 2009;Carter and Bean, 2009;. The 'supercritical' density of Na + -channels has been discussed to functionally compensate for the special axonal morphology of fast-spiking interneurons, i.e.…”

Section: Accepted Manuscriptmentioning

confidence: 99%

The interneuron energy hypothesis: Implications for brain disease

Kann

2016

Neurobiology of Disease

205

172

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“…However, the majority of the energy usage seems to occur locally at the level of synapses [47]. On the other hand, the conductance of the action potential through the axons has been found to cause only minimal dissipation of energy [48]. The synaptic compartment may thus represent the major site of mitochondrial respiration within neurons, thereby accommodating its specific expenditure.…”

mentioning

confidence: 99%

Energy metabolism in neuronal/glial induction and in iPSC models of brain disorders

Mlody

Lorenz

Inak

et al. 2016

Seminars in Cell & Developmental Biology

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The metabolic switch associated with the reprogramming of somatic cells to pluripotency has received increasing attention in recent years. However, the impact of mitochondrial and metabolic modulation on stem cell differentiation into neuronal/glial cells and related brain disease modeling still remains to be fully addressed. Here, we seek to focus on this aspect by first addressing brain energy metabolism and its inter-cellular metabolic compartmentalization. We then review the findings related to the mitochondrial and metabolic reconfiguration occurring upon neuronal/glial specification from pluripotent stem cells (PSCs). Finally, we provide an update of the PSC-based models of mitochondria-related brain disorders and discuss the challenges and opportunities that may exist on the road to develop a new era of brain disease modeling and therapy.3 Mitochondrial remodeling in cell fate specificationThe majority of cellular energy in form of ATP is provided through oxidative phosphorylation (OXPHOS) by mitochondria. Mitochondria are also involved in the metabolism of amino acids, fatty acids, and steroids, and contribute to cell signaling through the modulation of reactive oxygen species (ROS), calcium homeostasis, and apoptosis [1].Furthermore, intermediate metabolites can cross-talk to the nucleus acting as epigenetic regulators [2].In low oxygen environments, a typical conversion process of 1 molecule of glucose results into 2 molecules of ATP through glycolysis in the cytosol, which terminates with the secretion of lactate into the extracellular environment. Under normoxic conditions, the 2 molecules of pyruvate, generated through glycolysis, can enter the mitochondria and undergo further oxidation in the tricarboxylic acid (TCA) cycle, leading to the production of additional 34 molecules of ATP [3]. However, under conditions requiring high proliferative rates, this mitochondrial-based energy generation may be shut-down despite the presence of normal oxygen concentration [4]. This situation, known as aerobic glycolysis or Warburg effect, was first described by Otto Warburg in the context of cancer [5]. Recent studies demonstrated that a Warburg-like effect may also represent a defining feature of stem cells [6][7][8].Since distinct cell types have different energy demands, regulation of mitochondria may represent an essential process allowing the cells to meet their biological requirements.The metabolic identity of cells may in fact be influenced not only by changes in the expression of metabolic genes, but also by modulation of mitochondrial dynamics and mitochondrial DNA (mtDNA) copy number [9,10]. In particular, energy metabolism is shifted towards glycolysis in stem cells, whose mitochondria appear round-shaped with poorlydeveloped cristae [11,12]. This is in sharp contrast to cells with high energy demands, like muscle cells and neurons, where mitochondria are abundant in number and exhibit tubularlike morphology and cristae-rich structures [13]. 4As a consequence, acquisition of a distinct metabot...

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Energy-Efficient Action Potentials in Hippocampal Mossy Fibers

Cited by 375 publications

References 23 publications

Energy and information in Hodgkin-Huxley neurons

Energy and information in Hodgkin-Huxley neurons

The interneuron energy hypothesis: Implications for brain disease

Energy metabolism in neuronal/glial induction and in iPSC models of brain disorders

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