Current-voltage relations in the rod photoreceptor network of the turtle retina

Abstract

1. Electrical coupling between rod photoreceptors was studied in the eyecup preparation of the snapping turtle, Chelydra serpentina, using intracellular micro-electrodes.2. The spatial profiles of rod responses to a long narrow slit of light were determined. The peak response amplitudes were found to decline exponentially as the slit was moved from the most sensitive position in the receptive field of each rod. The mean length constant was 55.7 mum.3. Rods were simultaneously impaled in pairs and electrical coupling was demonstrated between the rods in seventeen of these pairs. No coupling was observed between rods separated by more than 110 mum. The transfer resistance, defined as the ratio of potential in the second rod (coupled potential) to the current injected into the first rod, varied from 0.2 to 13.2 MOmega.4. The waveform of the coupled potential was time varying, exhibiting a peak and subsequent relaxation phase. The time course of the relaxation phase was voltage-dependent. At the cessation of current, the coupled potential rebounded beyond the resting potential and then decayed to the dark potential.5. Plots of input current versus coupled potential showed strong outward-going rectification, chord transfer resistances being as much as 3.5 times lower for depolarizing currents.6. Simultaneous impalements were made of pairs of neighbouring red-sensitive cones, of horizontal cells and rods, and of red-sensitive cones and rods. No evidence of coupling between cones and rods were found, nor could feed-back from horizontal cells onto rods be demonstrated; however, coupling between red-sensitive cones was found. This coupling exhibited neither the marked time-varying nor voltage-dependent properties that characterize the rod-rod coupling.7. Individual rods were impaled with independent current passing and voltage sensing micro-electrodes. Pulses of current produced time-varying potentials having relaxation and rebound phases. Current-voltage measurements showed a strong outward-going rectification. Input resistances at the resting potential ranged up to 96 MOmega.8. Square grid and hexagonal lattice models of ohmic electrical coupling were applied to the results. Using the measured values for the length constants and input resistances of single rods, we calculate that the plasma membrane resistance of each rod is approximately 1000 MOmega at the resting potential and that the coupling resistances are 272 and 444 MOmega for the square grid and hexagonal models, respectively.9. The time-varying and voltage-dependent properties observed at the input and in the coupling between rods appear to reflect characteristics of the rod's plasma membrane and not of the coupling pathways between the rods. Both the outward-going rectification and relaxation phase of the response appear to involve voltage-dependent conductance increases in the rod's plasma membrane.