State and location dependence of action potential metabolic cost in cortical pyramidal neurons

State and location dependence of action potential metabolic cost in cortical pyramidal neurons
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DOI:
10.1038/nn.3132
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发表时间:
2012-07-01
影响因子:
25
通讯作者:
Kole, Maarten H. P.
Kole, Maarten H. P.
中科院分区:
医学1区
文献类型:
--
作者:
Hallermann, Stefan;de Kock, Christiaan P. J.;Kole, Maarten H. P.

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动作电位的产生和传导需要大量的能量来恢复Na+和K+离子的梯度。我们研究了这种代谢成本在大鼠新皮质锥体神经元中的亚细胞位置和电压依赖性。用Na+/K+电荷重叠作为衡量动作电位能量效率的指标,我们发现动作电位在轴突起始段(AIS)的启动和向轴突的正向传播在能量上是无效的,这依赖于静息膜电位。相反,动作电位反向传播到树突是有效的。计算机模拟预测,尽管AIS和Ranvier结节的每膜面积的代谢成本最高,但动作电位向树突的反向传播和向轴突侧支的正向传播主导了皮质锥体神经元的能量消耗。最后,我们发现,动作电位的启动和沿轴突传播的高代谢成本是高频动作电位传导可靠性的能量最小化和最大化之间的权衡。
Action potential generation and conduction requires large quantities of energy to restore Na+ and K+ ion gradients. We investigated the subcellular location and voltage dependence of this metabolic cost in rat neocortical pyramidal neurons. Using Na+/K+ charge overlap as a measure of action potential energy efficiency, we found that action potential initiation in the axon initial segment (AIS) and forward propagation into the axon were energetically inefficient, depending on the resting membrane potential. In contrast, action potential backpropagation into dendrites was efficient. Computer simulations predicted that, although the AIS and nodes of Ranvier had the highest metabolic cost per membrane area, action potential backpropagation into the dendrites and forward propagation into axon collaterals dominated energy consumption in cortical pyramidal neurons. Finally, we found that the high metabolic cost of action potential initiation and propagation down the axon is a trade-off between energy minimization and maximization of the conduction reliability of high-frequency action potentials.