Action potential energy efficiency varies among neuron types in vertebrates and invertebrates.
Action potential energy efficiency varies among neuron types in vertebrates and invertebrates.
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DOI：
10.1371/journal.pcbi.1000840
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发表时间：
2010-07-01
影响因子：
4.3
通讯作者：
Niven JE
中科院分区：
文献类型：
--
作者：
Sengupta B;Stemmler M;Laughlin SB;Niven JE
动作电位（AP）的启动和传播对神经组织的能量资源提出了很高的要求。每个AP迫使ATP驱动的离子泵更努力地工作以恢复离子浓度梯度，从而消耗更多的能量。在这里，我们问是否可以从理论上预测的最低能耗的原则，离子电流的AP。一个长期持有的假设，即AP是能量浪费，根据鱿鱼巨大的轴突AP的理论分析，最近被推翻的研究，测量电流有助于AP在几种哺乳动物神经元。在这里研究的单室模型中，AP能量消耗在脊椎动物和无脊椎动物神经元之间变化很大，几种哺乳动物神经元模型使用接近所需能量的电容最小值。引人注目的是，能量消耗可以增加超过十倍，只要改变重叠的Na+和K+电流在AP不改变AP的形状。因此，AP的高度和宽度是能量消耗的不良预测因子。在鱿鱼轴突的Hodgkin-Huxley模型中，优化Na+和K+通道的动力学或数量可以将每个AP所需的ATP分子数量减少四倍。相反，鱿鱼AP，一些哺乳动物神经元的电流基础AP的时间分布几乎完全匹配的优化性能的离子电导，以尽量减少ATP的成本。神经元产生无数具有不同形状和不同高度和宽度的动作电位;这些动作电位的基础是具有不同生物物理性质的高度非线性、电压依赖性离子电导。每个动作电位都是有代价的：大脑使用其总能量预算的很大一部分来产生和传播动作电位。最近的研究结果表明，一些哺乳动物的动作电位具有生物物理特性，使他们的能源效率。然而，能量有效的动作电位有多普遍？通过数学分析和建模，我们发现单个动作电位的高度、宽度和能量消耗之间没有直接的关系。此外，我们确定，许多哺乳动物的动作电位的生物物理特性，减少其内向和外向电流之间的重叠，以尽量减少能量消耗。这种重叠的减少是由于为每个特定神经元类型唯一定制的离子通道特性和该神经元中动作电位的功能目的的组合。通过比较测得的生物物理参数的数值优化最大的能源效率的参数，我们认为，能源效率的自然选择可以帮助解释的动作电位和离子电流的基本生物物理的形状。
The initiation and propagation of action potentials (APs) places high demands on the energetic resources of neural tissue. Each AP forces ATP-driven ion pumps to work harder to restore the ionic concentration gradients, thus consuming more energy. Here, we ask whether the ionic currents underlying the AP can be predicted theoretically from the principle of minimum energy consumption. A long-held supposition that APs are energetically wasteful, based on theoretical analysis of the squid giant axon AP, has recently been overturned by studies that measured the currents contributing to the AP in several mammalian neurons. In the single compartment models studied here, AP energy consumption varies greatly among vertebrate and invertebrate neurons, with several mammalian neuron models using close to the capacitive minimum of energy needed. Strikingly, energy consumption can increase by more than ten-fold simply by changing the overlap of the Na+ and K+ currents during the AP without changing the APs shape. As a consequence, the height and width of the AP are poor predictors of energy consumption. In the Hodgkin–Huxley model of the squid axon, optimizing the kinetics or number of Na+ and K+ channels can whittle down the number of ATP molecules needed for each AP by a factor of four. In contrast to the squid AP, the temporal profile of the currents underlying APs of some mammalian neurons are nearly perfectly matched to the optimized properties of ionic conductances so as to minimize the ATP cost. Neurons produce a myriad of action potentials with different shapes and varying heights and widths; underlying these action potentials are highly nonlinear, voltage-dependent ionic conductances with varying biophysical properties. Each action potential comes at a cost: the brain uses a substantial portion of its total energy budget to generate and propagate action potentials. Recent results show that some mammalian action potentials have biophysical properties that make them energy efficient. Yet, how widespread are energy efficient action potentials? Using mathematical analysis and modeling, we show that there is no direct relationship between the height, width, and the energy consumption of a single action potential. Furthermore, we establish that many mammalian action potentials have biophysical properties that reduce the overlap between their inward and outward currents so as to minimize energy consumption. This reduction in overlap results from a combination of ion channel properties uniquely tailored for each particular neuron type and the functional purpose of the action potential in that neuron. By comparing the measured biophysical parameters to the parameters produced by numerical optimization for maximal energy-efficiency, we argue that natural selection for energy-efficiency could help explain both the shape of the action potential and the underlying biophysics of ionic currents.
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影响因子：
4.3
作者：
Angelino, Elaine;Brenner, Michael P.
通讯作者：
Brenner, Michael P.
影响因子：
56.9
作者：
Alle, Henrik;Roth, Arnd;Geiger, Joerg R. P.
通讯作者：
Geiger, Joerg R. P.
影响因子：
64.8
作者：
Niven, JE;Vähäsöyrinki, M;Weckström, M
通讯作者：
Weckström, M
哺乳动物神经元动作电位期间的钠进入：快速刺激神经元的灭活不完全失活和代谢效率降低。
影响因子：
16.2
作者：
Carter, Brett C.;Bean, Bruce P.
通讯作者：
Bean, Bruce P.
影响因子：
5.5
作者：
KIMURA, J;MIYAMAE, S;NOMA, A
通讯作者：
NOMA, A