Mechanisms of Electrical Coupling Between Pyramidal Cells

• Published in: Journal of neurophysiology 1997-12, Vol.78 (6), p.3107-3116
• Main Authors: Vigmond, Edward J, Velazquez, Jose L. Perez, Valiante, Taufik A, Bardakjian, BERJ L, Carlen, Peter L
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; Computer Simulation; Dendrites - physiology; Electric Conductivity; Gap Junctions - physiology; In Vitro Techniques; Membrane Potentials - physiology; Models, Neurological; Pyramidal Cells - physiology; Rats; Rats, Wistar
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.1997.78.6.3107

Edward J. Vigmond 1 , Jose L. Perez Velazquez 2 , Taufik A. Valiante 2 , BERJ L. Bardakjian 1 , and Peter L. Carlen 2 1   Institute of Biomedical Engineering and Department of Electrical and Computer Engineering, University of Toronto, Toronto M5S 3G9; and 2   Playfair Neuroscience Unit and Bloorview Epilepsy Program, Toronto Hospital Western Division, University of Toronto, Toronto, Ontario M5T 2S8, Canada Vigmond, Edward J., Jose L. Perez Velazquez, Taufik A. Valiante, Berj L. Bardakjian, and Peter L. Carlen. Mechanisms of electrical coupling between pyramidal cells. J. Neurophysiol. 78: 3107-3116, 1997. 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 extra