A small fraction of strongly cooperative sodium channels boosts neuronal encoding of high frequencies.

A small fraction of strongly cooperative sodium channels boosts neuronal encoding of high frequencies.
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DOI:
10.1371/journal.pone.0037629
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发表时间:
2012
期刊:
影响因子:
3.7
通讯作者:
Wolf F
Wolf F
中科院分区:
综合性期刊3区
文献类型:
--
作者:
Huang M;Volgushev M;Wolf F

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动作电位(AP)的产生是神经元信息处理的关键步骤。现有的AP产生的生物物理模型几乎普遍假设单个电压门控钠通道在统计上是独立运行的,并且它们在AP产生下的雪崩样开口仅通过跨膜电位来协调。然而,各种类型的生物离子通道在聚集时可以表现出强烈的协作门控。钠通道的协同门控被认为可以解释大脑皮层神经元AP的快速起效动力学和大的阈值变异性。然而,目前尚不清楚如果只有一小部分通道表现出协作性,大脑皮层AP的这些特征属性是否可以复制,以及合作通道的存在是否会影响神经元群体的编码属性。为了解决这些问题,我们构建了一个基于电导的神经元模型,在该模型中,我们连续改变部分钠通道的大小,以表达协作性和合作通道之间的耦合强度。我们发现,从一个耦合强度的临界值开始,钠通道的激活曲线发展成一个间断,在这个不连续处,所有耦合通道的开放变成一个全有或全无事件,导致非常快的AP起始。具有一小部分强合作信道的模型产生具有最快发作动力学的AP。在这一机制中,AP由协作通道部分的同时开放而触发,并呈现出明显的双相波形,通常在皮质神经元中观察到。我们进一步表明,一小部分合作的Na+通道的存在显著提高了神经元群体对高频输入波动的放电进行锁相的能力。我们的结论是,一小部分强耦合钠通道的存在可以解释皮层AP的特征,并具有增强快速变化信号的棘波编码的功能影响。
Generation of action potentials (APs) is a crucial step in neuronal information processing. Existing biophysical models for AP generation almost universally assume that individual voltage-gated sodium channels operate statistically independently, and their avalanche-like opening that underlies AP generation is coordinated only through the transmembrane potential. However, biological ion channels of various types can exhibit strongly cooperative gating when clustered. Cooperative gating of sodium channels has been suggested to explain rapid onset dynamics and large threshold variability of APs in cortical neurons. It remains however unknown whether these characteristic properties of cortical APs can be reproduced if only a fraction of channels express cooperativity, and whether the presence of cooperative channels has an impact on encoding properties of neuronal populations. To address these questions we have constructed a conductance-based neuron model in which we continuously varied the size of a fraction of sodium channels expressing cooperativity and the strength of coupling between cooperative channels . We show that starting at a critical value of the coupling strength , the activation curve of sodium channels develops a discontinuity at which opening of all coupled channels becomes an all-or-none event, leading to very rapid AP onsets. Models with a small fraction, , of strongly cooperative channels generate APs with the most rapid onset dynamics. In this regime APs are triggered by simultaneous opening of the cooperative channel fraction and exhibit a pronounced biphasic waveform often observed in cortical neurons. We further show that presence of a small fraction of cooperative Na+ channels significantly improves the ability of neuronal populations to phase-lock their firing to high frequency input fluctuation. We conclude that presence of a small fraction of strongly coupled sodium channels can explain characteristic features of cortical APs and has a functional impact of enhancing the spike encoding of rapidly varying signals.
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期刊: Science (New York, N.Y.)
影响因子: --
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