Behaviour of the rod network in the tiger salamander retina mediated by membrane properties of individual rods

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Abstract
The spread of electrical signals between rods in the salamander retina was examined by passing current into 1 rod and recording the voltage responses in nearby rods. Rod network behavior, measured in this way, was simulated from rod membrane properties gathered with voltage-clamps from single isolated rods. The network voltage responses to square current pulses became smaller, more transient and had a longer time-to-peak for rods further away from the site of current injection. Depolarizing currents produced smaller responses than hyperpolarizing currents of the same magnitude. Neighboring rods and cones were coupled less strongly than neighboring rods. The response of the rod network to current injection was unaffected by 2 mM-aspartate-, which eliminates transmission from receptors to horizontal cells. The input resistance of single isolated rods, measured at the resting potential, varied between 100-680 M.OMEGA.. The lower values were probably due to damage by the micro-electrodes. Electrical coupling was very strong between the rod inner and outer segments. A strong instantaneous outward rectification in isolated rods at potentials positive to -35 mV was reduced, but not abolished, by 15 mM-TEA [tetraethyl ammonium chloride]. In normal solution, isolated rods exhibited a voltage- and time-dependent current, IA, whose kinetics were approximated by a single 1st-order gating variable, and whose activation curve spanned the range between -40 and -80 mV. The time constant for the current varied with voltage and was 60-200 ms between -140 and -40 mV. A reversal potential for IA was not found between -140 and -40 mV in normal solution and the fully activated current, .hivin.IA, was approximately voltage-independent with a magnitude of .apprx. 0.1 nA over this potential range. By several criteria IA behaved as a single inward current activated by hyperpolarization. Pharmacologically IA appeared as the sum of at least 2 currents with very similar kinetics. Most isolated rods exhibited a very slow (.tau. .apprx. 3 s) increase in net outward current on depolarizing beyond -35 mV. The magnitude of this current varied considerably between cells. Assuming the rod network was approximated by a square lattice of individual rods resistively coupled together, the voltage-clamp data on isolated rods predicted the response of the network to current injection at 1 cell. The theoretical and observed network behavior were in good agreement. The resistance coupling neighboring rods was .apprx. 300 M.OMEGA.. The current IA played a major role in determining the behavior of the rod network. The time-dependent current, IA, is responsible for the peak-plateau wave form of the response to a bright flash. A current similar to IA could account for the negative propagation velocity of the peak of the dim flash response, through the rod network of the turtle, observed by Detwiler, Hodgkin and McNaughton.