Ion fluxes in photoreception in Limulus polyphemus ventral eye. I. The response of potassium efflux to light

Abstract

1. 1. Radioactive tracers were used to study the effect of light on the efflux of K + from Limulus polyphemus ventral eye. Eyes were labeled in artificial sea water containing 42KCl and then perfused with non-radioactive artificial sea water. 2. 2. After the first 2 min of perfusion, 42K in the eye decreased with time as the sum of two exponential terms of half-times 0.3 and 2 h. 3. 3. Illumination of an eye labeled with 42K caused an abrupt increase in the rate of release of 42K. The additional 42K released in response to light comes from the photoreceptor cell bodies rather than from the axons. 4. 4. The proportional increase in efflux rate upon illumination did not vary with the length of time that an eye was perfused. This suggests that the two exponential terms above reflect two classes of photoreceptor cells rather than photoreceptor cells and glial cells. 5. 5. By collection of perfusate at intervals of less than one second, it was shown that the instantaneous rate of 42K release increases up to 20-fold at the onset of illumination. With continuous illumination, the rate remains above the dark rate, but by less than a factor of 2. Thus, the response of potassium efflux to light has transient and steady phases like the receptor potential. The increased driving force on internal potassium resulting from the receptor potential is not sufficient to explain the flux changes, if one makes the constant field assumption for the photoreceptor membrane. 6. 6. A double label method with 42K and 42K was used to show that the average rate of influx over a 10-min period is not affected by illumination. 7. 7. In eyes cooled in the dark to 2–3 °C, light still elicited an increase in the rate of 42K release and large, prolonged receptor potentials. Thus, the photoreception mechanism of the ventral eye is not, as has been previously suggested, inactive at low temperatures.