RESPONSE PROPERTIES OF CONES FROM THE RETINA OF THE TIGER SALAMANDER

1. Spectral sensitivity measurements using the suction electrode technique reveal three types of cone in the retina of the tiger salamander, showing maximum sensitivity at wavelengths 610 nm (red-sensitive cone), 444 nm (blue-sensitive cone) and below 400 nm (UV-sensitive cone). 2. The absolute sensitivities of red- and blue-sensitive cones to flashes of optimal wavelength are 0.022 and 0.33 pA photon-1 mu-m2 respectively. 3. The time-to-peak of the dim flash response and the recovery of membrane current after a flash of any intensity are fastest in red-sensitive and slowest in blue-sensitive cones. 4. In blue- and UV-sensitive cones the flash response peaks progressively earlier as the flash strength is increased, as in rods. In red-sensitive cones, however, bright flash responses take longer to peak than dim flash responses. 5. In all three cone types, voltage clamping at -40 mV reduces the time-to-peak of the response to a bright flash, showing that the rising phase of the bright flash response is normally limited by the time constant of the cell. Under voltage clamp, all cones show a decrease in time-to-peak with increasing flash intensity. 6. Voltage clamping red-sensitive cones reveals two components of the rising phase of the response to a bright flash. Most of the current is rapidly suppressed by a bright flash, and represents the closure of light-sensitive channels. The residual current decays with a mean time constant of 20 ms, and is probably attributable to the decline of electrogenic Na+ -Ca2+, K+ exchange. The amplitude of this exchange current suggests that the proportion of the dark currents carried by calcium ions is greater in red-sensitive cones than in rods of the same species. 7. In UV-sensitive cones, a prominent oscillation of light-sensitive current is observed during the recovery from flashes of intermediate intensity. A similar, but slower and less prominent oscillation is usually seen in blue-sensitive cones. 8. When a red-sensitive cone is voltage clamped an oscillation similar to those in the other two cone type is revealed. An underswing of up to 2 pA is also observed after recovery from intermediate or bright flashes in the majority of red-sensitive cones, and voltage clamping increases the amplitude of this underswing. These observations demonstrate that the oscillations and underswing are not caused by changes in membrane potential and must therefore reflect oscillations in the cytosolic concentration of cyclic GMP. 9. Rapid solution change experiments indicate that the selectivity of the light-sensitive channel for monovalent cations is different in the rod and the red-sensitive cone. 10. About 60 % of the membrane current remains after replacement of external sodium ions with an important cation, and this residual current is abolished by removal of calcium ions.