MECHANISMS OF ELECTRICAL COUPLING BETWEEN PYRAMIDAL CELLS

Citation
Ej. Vigmond et al., MECHANISMS OF ELECTRICAL COUPLING BETWEEN PYRAMIDAL CELLS, Journal of neurophysiology, 78(6), 1997, pp. 3107-3116
Citations number
31
Journal title
ISSN journal
00223077
Volume
78
Issue
6
Year of publication
1997
Pages
3107 - 3116
Database
ISI
SICI code
0022-3077(1997)78:6<3107:MOECBP>2.0.ZU;2-F
Abstract
Direct electrical coupling between neurons can be the result of both e lectrotonic current transfer through gap junctions and extracellular f ields. Intracellular recordings from CA1 pyramidal neurons of rat hipp ocampal 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 ce ll was employed to determine the extracellular field produced by a neu ron and its effect on a nearby neuron resulting from both gap junction al and electric field coupling. Computations were performed with a nov el 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. Fiel d effects produced waveforms resembling spikelets although of smaller magnitude than those recorded in vitro. Gap junctional electrotonic co nnections produced waveforms resembling small-amplitude excitatory pos tsynaptic potentials. Intracellular electrode measurements were found inadequate for ascertaining membrane events because of externally appl ied electric fields. The transmembrane voltage induced by the electric field was highly spatially dependent in polarity and wave shape, as w ell as being an order of magnitude larger than activity measured at th e electrode. Membrane voltages because of electrotonic current injecti on across gap junctions were essentially constant over the cell and we re accurately depicted by the electrode. The effects of several parame ters were investigated: I) decreasing the ratio of intra to extracellu lar conductivity reduced the field effects; 2) the tree structure had a major impact on the intracellular potential; 3) placing the gap junc tion in the dendrites introduced a time delay in the gap junctional me diated electrotonic potential, as well as deceasing the potential reco rded by the somatic electrode; and 4) field effects decayed to one-hal f of their maximum strength at a cell separation of similar to 20 mu m . Results indicate that the in vitro measured spikelets are unlikely t o be mediated by gap junctions and that a spikelet produced by the ele ctric field of a single source cell has the same waveshape as the meas ured spikelet but with a much smaller amplitude. It is hypothesized th at spikelets are a manifestation of the simultaneous electric field ef fects from several local cells whose action potential firing is synchr onized.