Determinants of single photon response variability

The responses to single photon absorptions (quantum bumps) vary randomly in size in Limulus photoreceptors. This variability is a natural consequence of simple chemical reactions involving a small number of molecules. The measured size distributions differ significantly from the exponential distribution predicted by the simplest transduction cascade models, one feature of which is that light-activated rhodopsin (R*) is turned off in a single step process. As shown in the companion paper, the nonexponential size distributions can be accounted for if R* is turned off in a multi-step process. This would lead to a nonexponential (peaked) distribution in the number of G-protein molecules activated during a quantum bump and to a nonexponential distribution in the size of bumps. To test this possibility we measured the distribution of quantum bump size under two conditions in which the variability in the number of activated G-proteins was eliminated. In one method, bumps were produced by direct activation of single G-proteins using GTP-γ-.S; in the second GDP-β-S reduced the R* gain to the point where most quantal events were due to activation of a single G-protein. In both cases the size distribution of bumps became much closer to an exponential distribution than that of normal light-induced bumps. These results support the idea that the size distribution of light-induced bumps is dependent on events at the R* level and reflects to the multi-step deactivation of R*.