Conductance and dye permeability of a rectifying electrical synapse

Abstract

Electrical synapses provide a basis for efficient signal transmission in a wide variety of nervous systems¹. These synapses are composed of specialized cell-to-cell contacts known as nexuses² or gap junctions³ which mediate the direct transfer of ions and small molecules between adjacent cell interiors^1,4 by way of intercellular channels embedded in the junctional membrane⁵. The crayfish giant motor synapse (CMS) was the first cell-to-cell junction clearly demonstrated to operate by an electrical mechanism⁶. Current applied to the presynaptic lateral giant (LG) axon or to the neurite of the postsynaptic giant flexor motoneurone (MoG) spreads passively through the synapse into the adjacent neurone^6,7. Each GMS behaves like an electrical rectifier: its conductance is high when LG is positive with respect to MoG, and decreases dramatically when the sign of the trans-synaptic voltage is reversed^6,7. We have now examined GMS conductance and dye permeability at thoracic and abdominal levels of the crayfish nerve cord. At both levels, values of GMS chord conductance fit a simple Boltzmann model in which the conductance of individual synaptic channels is assumed to be voltage dependent. Moreover, thoracic synapses display higher limiting conductances than do those at an abdominal level, apparently as a result of their larger size. We also find that synapses at both locations are permeable to the fluorescent dye Lucifer yellow, even in conditions where electrical conductance is low. These results provide a framework for understanding the operation and functional limits of rectifying electrical synapses, and illustrate that dye permeability can be associated even with their relatively low conductance condition.