The effects of background illumination on the photoresponses of red and green cones

Abstract

1. The photoresponses of light- and dark-adapted red and green cone photoreceptors were recorded intracellularly in the retina of the turtle, Pseduemys scripta elegans. Background illumination produced similar effects on both types of cones. 2. In response to the onset of a prolonged, steady background illumination the cone initially hyperpolarized to a peak which then sagged back to a steady-state polarization that was typically about one half the initial peak amplitude. This sag was observed for all backgrounds studied (dim as well as bright). 3. A resensitization was observed concomitantly with this sag; both the maximum increment and decrement responses grew in amplitude as light-adaptation proceeded. After about 2--3 min of background illumination, the amplitudes of these responses stabilized. 4. The dark-adapted cone produced graded responses to test pulses over a range of intensities spanning about 3.5 log units. The amplitudes of these responses were well fit by the relationship V = I.Vm/(I + sigma). 5. After 2--3 min of background illumination, 500 msec test pulses either brighter or dimmer than the background intensity were substituted for the background. The light-adapted intensity-response curves constructed from this data were similar to the dark-adapted curve but were shifted horizontally and slightly vertically, so that they still spanned about 3.5 log units of intensity. Thus, in the light-adapted cone, graded responses were elicited by a range of bright test pulses which would have produced saturated responses when delivered to the dark-adapted cone. 6. The 'off response' observed at the offset of the background became faster as the background intensity was increased. It also became faster with time following the onset of any particular background intensity. 7. It was concluded that cone sensitivity during any state of light-adaptation is determined by two mechanisms; response compression resulting from the instantaneous non-linearity between 'internal transmitter' concentration and membrane potential and a more active 'cellular adaptation' mechanism which is manifest as a shift in the intensity-response curve. In the steady-state condition of light-adaptation, most of the sensitivity changes are a result of the cellular adaptation mechanism. 8. Photopigment bleaching caused by the backgrounds, negative feed-back from horizontal cells and voltage dependent mechanisms in the cones could not account for this cellular adaptation. These effects of background illumination were interpreted in terms of the 'internal transmitter' hypothesis of phototransduction.