Vigmond E J, Perez Velazquez J L, Valiante T A, Bardakjian B L, Carlen P L
Institute of Biomedical Engineering and Department of Electrical and Computer Engineering, University of Toronto, Toronto M5S 3G9, Canada.
J Neurophysiol. 1997 Dec;78(6):3107-16. doi: 10.1152/jn.1997.78.6.3107.
Direct electrical coupling between neurons can be the result of both electrotonic current transfer through gap junctions and extracellular fields. Intracellular recordings from CA1 pyramidal neurons of rat hippocampal slices showed two different types of small-amplitude coupling potentials: short-duration (5 ms) biphasic spikelets, which resembled differentiated action potentials and long-duration (>20 ms) monophasic potentials. A three-dimensional morphological model of a pyramidal cell was employed to determine the extracellular field produced by a neuron and its effect on a nearby neuron resulting from both gap junctional and electric field coupling. Computations were performed with a novel formulation of the boundary element method that employs triangular elements to discretize the soma and cylindrical elements to discretize the dendrites. An analytic formula was derived to aid in computations involving cylindrical elements. Simulation results were compared with biological recordings of intracellular potentials and spikelets. Field effects produced waveforms resembling spikelets although of smaller magnitude than those recorded in vitro. Gap junctional electrotonic connections produced waveforms resembling small-amplitude excitatory postsynaptic potentials. Intracellular electrode measurements were found inadequate for ascertaining membrane events because of externally applied electric fields. The transmembrane voltage induced by the electric field was highly spatially dependent in polarity and wave shape, as well as being an order of magnitude larger than activity measured at the electrode. Membrane voltages because of electrotonic current injection across gap junctions were essentially constant over the cell and were accurately depicted by the electrode. The effects of several parameters were investigated: 1) decreasing the ratio of intra to extracellular conductivity reduced the field effects; 2) the tree structure had a major impact on the intracellular potential; 3) placing the gap junction in the dendrites introduced a time delay in the gap junctional mediated electrotonic potential, as well as deceasing the potential recorded by the somatic electrode; and 4) field effects decayed to one-half of their maximum strength at a cell separation of approximately 20 micron. Results indicate that the in vitro measured spikelets are unlikely to be mediated by gap junctions and that a spikelet produced by the electric field of a single source cell has the same waveshape as the measured spikelet but with a much smaller amplitude. It is hypothesized that spikelets are a manifestation of the simultaneous electric field effects from several local cells whose action potential firing is synchronized.
神经元之间的直接电耦合可能是通过缝隙连接的电紧张电流传递和细胞外场共同作用的结果。对大鼠海马切片CA1锥体神经元进行的细胞内记录显示出两种不同类型的小幅度耦合电位：持续时间短（5毫秒）的双相小尖峰，类似于分化的动作电位；以及持续时间长（>20毫秒）的单相电位。利用锥体细胞的三维形态模型来确定神经元产生的细胞外场及其对附近神经元由缝隙连接和电场耦合所产生的影响。计算采用了边界元法的一种新公式，该公式使用三角形单元离散化胞体，使用圆柱形单元离散化树突。推导了一个解析公式以辅助涉及圆柱形单元的计算。将模拟结果与细胞内电位和小尖峰的生物学记录进行了比较。场效应产生的波形类似于小尖峰，尽管其幅度比体外记录的要小。缝隙连接的电紧张连接产生的波形类似于小幅度兴奋性突触后电位。发现细胞内电极测量不足以确定膜电位变化，因为存在外部施加的电场。电场诱导的跨膜电压在极性和波形上高度依赖于空间，并且比电极处测量的活动大一个数量级。通过缝隙连接进行电紧张电流注入所产生的膜电压在整个细胞上基本恒定，并且电极能够准确描绘。研究了几个参数的影响：1）降低细胞内与细胞外电导率的比值会降低场效应；2）树突结构对细胞内电位有重大影响；3）将缝隙连接置于树突中会在缝隙连接介导的电紧张电位中引入时间延迟，同时降低胞体电极记录的电位；以及4）场效应在细胞间距约为20微米时衰减至其最大强度的一半。结果表明，体外测量的小尖峰不太可能由缝隙连接介导，并且单个源细胞电场产生的小尖峰与测量的小尖峰具有相同的波形，但幅度要小得多。据推测，小尖峰是几个局部细胞动作电位发放同步时同时产生的电场效应的一种表现。
