Summation of excitatory postsynaptic potentials in electrically-coupled neurones

Abstract

Dendritic electrical coupling increases the number of effective synaptic inputs onto neurones by allowing the direct spread of synaptic potentials from one neurone to another. Here we studied the summation of excitatory postsynaptic potentials (EPSPs) produced locally and arriving from the coupled neurone (transjunctional) in pairs of electrically-coupled Retzius neurones of the leech. We combined paired recordings of EPSPs, the production of artificial excitatory postsynaptic potentials (APSPs) in neurone pairs with different coupling coefficients and simulations of EPSPs produced in the coupled dendrites. Summation of the EPSPs produced in the dendrites was always linear, suggesting that synchronous EPSPs are produced at two or more different pairs of coupled dendrites and not in both sides of any one gap junction. The different spatio-temporal relationships explored between pairs of EPSPs or APSPs produced three main effects. (1) Synchronous pairs of EPSPs or APSPs exhibited an elongation of their decay phase compared to singe EPSPs. (2) Asymmetries in the amplitudes between the pair of EPSPs added a “hump” to the smallest EPSP. (3) Modelling the inputs near the electrical synapse or anticipating the production of the transjunctional APSP increased the amplitude of the compound EPSP. The magnitude of all these changes depended on the coupling coefficient of the neurones. We also show that the hump improves the passive conduction of EPSPs by adding low frequency components. The diverse effects of summation of local and alien EPSPs shown here endow electrically-coupled neurones with a wider repertoire of adjustable integrative possibilities.