Chen Xiangdong, Shu Shaofang, Kennedy Dylan P, Willcox Sarah C, Bayliss Douglas A
Department of Pharmacology, University of Virginia, Charlottesville, VA, USA.
J Neurophysiol. 2009 Jan;101(1):129-40. doi: 10.1152/jn.01352.2007. Epub 2008 Oct 29.
The ionic mechanisms that contribute to general anesthetic actions have not been elucidated, although increasing evidence has pointed to roles for subthreshold ion channels, such as the HCN channels underlying the neuronal hyperpolarization-activated cationic current (Ih). Here, we used conventional HCN1 knockout mice to test directly the contributions of specific HCN subunits to effects of isoflurane, an inhalational anesthetic, on membrane and integrative properties of motor and cortical pyramidal neurons in vitro. Compared with wild-type mice, residual Ih from knockout animals was smaller in amplitude and presented with HCN2-like properties. Inhibition of Ih by isoflurane previously attributed to HCN1 subunit-containing channels (i.e., a hyperpolarizing shift in half-activation voltage [V1/2]) was absent in neurons from HCN1 knockout animals; the remaining inhibition of current amplitude could be attributed to effects on residual HCN2 channels. We also found that isoflurane increased temporal summation of excitatory postsynaptic potentials (EPSPs) in cortical neurons from wild-type mice; this effect was predicted by simulation of anesthetic-induced dendritic Ih inhibition, which also revealed more prominent summation accompanying shifts in V1/2 (an HCN1-like effect) than decreased current amplitude (an HCN2-like effect). Accordingly, anesthetic-induced EPSP summation was not observed in cortical cells from HCN1 knockout mice. In wild-type mice, the enhanced synaptic summation observed with low concentrations of isoflurane contributed to a net increase in cortical neuron excitability. In summary, HCN channel subunits account for distinct anesthetic effects on neuronal membrane properties and synaptic integration; inhibition of HCN1 in cortical neurons may contribute to the synaptically mediated slow-wave cortical synchronization that accompanies anesthetic-induced hypnosis.
尽管越来越多的证据表明阈下离子通道发挥了作用,如神经元超极化激活阳离子电流(Ih)背后的超极化激活环核苷酸门控(HCN)通道,但导致全身麻醉作用的离子机制仍未阐明。在此,我们使用传统的HCN1基因敲除小鼠,直接测试特定HCN亚基对异氟烷(一种吸入性麻醉剂)在体外对运动神经元和皮层锥体神经元的膜特性及整合特性影响的作用。与野生型小鼠相比,基因敲除动物的残余Ih幅度较小,并呈现出类似HCN2的特性。在HCN1基因敲除动物的神经元中,异氟烷先前归因于含HCN1亚基通道的Ih抑制作用(即半激活电压[V1/2]的超极化偏移)并不存在;电流幅度的剩余抑制作用可归因于对残余HCN2通道的影响。我们还发现,异氟烷增加了野生型小鼠皮层神经元兴奋性突触后电位(EPSP)的时间总和;麻醉诱导的树突Ih抑制模拟预测了这种效应,该模拟还显示,伴随V1/2的偏移(一种类似HCN1的效应)比电流幅度降低(一种类似HCN2的效应)时的总和更显著。因此,在HCN1基因敲除小鼠的皮层细胞中未观察到麻醉诱导的EPSP总和。在野生型小鼠中,低浓度异氟烷观察到的增强突触总和导致皮层神经元兴奋性净增加。总之,HCN通道亚基解释了对神经元膜特性和突触整合的不同麻醉作用;皮层神经元中HCN1的抑制可能有助于伴随麻醉诱导催眠的突触介导的皮层慢波同步。