Laboratorio de Neurofisiología Celular, Departamento de Fisiología, Facultad de Medicina, Universidad de la República, Montevideo 11800, Uruguay.
J Neurosci. 2012 Mar 28;32(13):4341-59. doi: 10.1523/JNEUROSCI.6216-11.2012.
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. 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.
电突触已知在哺乳动物大脑的各个区域形成广泛偶联神经元的网络。由起源于下颌闭合肌肉的初级传入体形成的中脑三叉神经(MesV)核是支持哺乳动物中枢神经系统中存在电突触的最早实例之一;然而,该结构内电耦联的特性、功能组织和发育出现仍不清楚。通过在大鼠和小鼠脑切片中结合电生理、示踪剂偶联和免疫化学分析,我们发现偶联主要局限于 MesV 神经元的对或小簇。电传递由位于体-体细胞接触处的包含连接蛋白 36(Cx36)的缝隙连接支持,其中只有一小部分通道似乎是开放的(约 0.1%)。与大多数脑结构形成鲜明对比的是,MesV 神经元之间的偶联随着年龄的增长而增加,因此在早期发育过程中不存在,并且在出生后第 8 天出现。有趣的是,偶联的发育与负责这些神经元重复放电的内在膜特性的发育相平行。我们发现,钠和钾电导共同作用增强了具有高频内容的信号通过电突触的传递,导致偶联神经元的强烈同步放电。总之,我们的数据表明,MesV 核内的偶联主要局限于大多数体之间,其中电传递由估计存在的通道的一小部分支持,并且偶联协同作用于特定的膜电导,以促进这些神经元的同步。