Synergy between electrical coupling and membrane properties promotes strong synchronization of neurons of the mesencephalic trigeminal nucleus.

Synergy between electrical coupling and membrane properties promotes strong synchronization of neurons of the mesencephalic trigeminal nucleus.
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DOI:
10.1523/jneurosci.6216-11.2012
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发表时间:
2012-03-28
期刊:
The Journal of neuroscience : the official journal of the Society for Neuroscience
影响因子:
--
通讯作者:
Pereda AE
Pereda AE
中科院分区:
其他
文献类型:
--
作者:
Curti S;Hoge G;Nagy JI;Pereda AE

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已知电突触在哺乳动物大脑的各个区域中形成广泛耦合的神经元网络。三叉神经中脑核(MesV)是哺乳动物中枢神经系统(CNS)中最早发现的一个电突触,但其电耦合的性质、功能组织和发育过程尚不清楚。结合大鼠和小鼠脑片的电生理、示踪剂偶联和免疫化学分析,我们发现偶联主要限于成对或小簇的MesV神经元。电传输由在躯体-躯体接触处的含有连接蛋白36(Cx 36)的间隙连接支持,其中只有一小部分通道似乎是开放的(~0.1%)。与大多数大脑结构形成鲜明对比的是,MesV神经元之间的耦合随着年龄的增长而增加,因此在早期发育期间不存在,并在出生后第8天出现。有趣的是,耦合的发展与负责这些神经元重复放电的内在膜特性的发展平行。我们发现,钠和钾电导共同作用,通过电突触增强具有高频内容的信号的传递,导致耦合神经元的强尖峰同步。两者合计,我们的数据表明,在MesV核耦合被限制到大多数对的胞体之间的电传输是支持一个令人惊讶的小部分的通道估计是存在的,耦合协同相互作用与特定的膜电导,以促进这些神经元的同步。
Electrical synapses are known to form networks of extensively coupled neurons in various regions of the mammalian brain. The mesencephalic trigeminal (MesV) nucleus, formed by the somata of primary afferents originating in jaw-closing muscles, constitutes one of the first examples supporting the presence of electrical synapses in the mammalian CNS, however, the properties, functional organization and developmental emergence of electrical coupling within this structure remain unknown. By combining electrophysiological, tracer coupling and immunochemical analysis in brain slices of rat and mouse, we found that coupling is mostly restricted to pairs or small clusters of MesV neurons. Electrical transmission is supported by connexin36 (Cx36)-containing gap junctions at somato-somatic contacts where only a small proportion of channels appear to be open (~0.1%). In marked contrast with most brain structures, coupling among MesV neurons increases with age, such that it is absent during early development and appears at postnatal day 8. Interestingly, the development of coupling parallels the development of intrinsic membrane properties responsible for repetitive firing in these neurons. We found that, acting together, sodium and potassium conductances enhance the transfer of signals with high frequency content via electrical synapses, leading to strong spiking synchronization of the coupled neurons. Taken together, our data indicate that coupling in the MesV nucleus is restricted to mostly pairs of somata between which electrical transmission is supported by a surprisingly small fraction of the channels estimated to be present, and that coupling synergically interacts with specific membrane conductances to promote synchronization of these neurons.