Plasma membrane calcium fluxes in intact rods are inconsistent with the "calcium hypothesis"

The temporal relationship between the extracellular rod photovoltage and light-induced net Ca fluxes across the rod plasma membrane is investigated. The net Ca flux measurements are derived from extracellular Ca concentration measurements at the receptor surface of the isolated bullfrog retina. As reported previously, illumination leads to a net Ca efflux, which is followed by a net influx, during which the released Ca is taken back up. However, the net Ca flux has two characteristics that are inconsistent with the hypothesis that intracellular free Ca is the intracellular messenger for phototransduction in rods. First, during maintained photovoltage saturation, the net Ca efflux is transient, declining with a stereotypic time course that is independent of stimulus intensity and duration. Second, the significant rate of net influx during Ca uptake has no correlate in the photovoltage waveform. These observations are not consistent with the "Ca hypothesis." Rather, these data corroborate recent findings suggesting that light causes a decrease rather than an increase in intracellular free Ca concentration.