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

1. The spread of electrical signals between rods in the salamander retina was examined by passing current into one rod and recording the voltage responses in nearby rods. Rod network behaviour, measured in this way, was simulated from data on rod membrane properties gathered in voltage-clamp experiments on single isolated rods.2. 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.3. Neighbouring rods and cones were coupled less strongly than neighbouring rods.4. The response of the rod network to current injection was unaffected by 2 mm-aspartate(-), which eliminates transmission from receptors to horizontal cells.5. The input resistance of single isolated rods, measured at the resting potential, varied between 100 and 680 MOmega. The lower values were probably due to damage by the micro-electrodes. Electrical coupling was found to be very strong between the rod inner and outer segments.6. A strong ;instantaneous' outward rectification seen in isolated rods at potentials positive to -35 mV was reduced, but not abolished, by 15 mm-TEA.7. In normal solution, isolated rods exhibited a voltage- and time-dependent current, I(A), whose kinetics were approximated by a single first-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 msec between -140 and -40 mV.8. A reversal potential for I(A) could not be found between -140 and -40 mV in normal solution, and the fully activated current, I(A), was approximately voltage-independent, with a magnitude of approximately 0.1 nA over this potential range.9. By several criteria, I(A) behaved as a single inward current activated by hyperpolarization. Pharmacological studies suggest, however, that it is the sum of at least two currents with very similar kinetics.10. Most isolated rods exhibited a very slow (tau approximately 3 sec) increase in net outward current on depolarizing beyond -35 mV. The magnitude of this current varied considerably between cells.11. Assuming that the rod network can be approximated by a square lattice of individual rods, resistively coupled together, the voltage-clamp data on isolated rods were used to predict the response of the network to current injection at one cell. The theoretical and observed network behaviour were in good agreement. The resistance coupling neighbouring rods was estimated to be approximately 300 MOmega. The current I(A) plays a major role in determining the behaviour of the rod network.12. The time-dependent current, I(A), is responsible for the peak-plateau wave form of the response to a bright flash. A current similar to I(A) could also 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 & McNaughton (1978).