Light-induced changes of extra- and intracellular potassium concentration in photoreceptors of the leech,Hirudo medicinalis

Summary

The potassium concentration was measured in the cytoplasm, perimicrovillar extracellular space (=‘vacuole’) and intercellular space of leech photoreceptors with double-barrelled potassium-sensitive microelectrodes in darkness and upon photostimulation. The mean intracellular potassium concentration in cells with membrane potentials >50 mV was 100±34 mmol/l. Photostimulation with 90 saturating 20 ms light flashes (1/s) evoked a potassium loss of 10.6±7.6 mmol/l. In the dark, there was no potassium concentration gradient between vacuole and intercellular space (K ⁺_VAC =4.5±0.9 mmol/l, K ⁺_ECS =4.5±0.5 mmol/l). In both compartments the potassium concentration increased upon repetitive photostimulation. Thus, the potassium loss from the cell is due to potassium movements across both the receptive and the non-receptive membrane domains.

The time courses of K⁺ accumulation and clearance differed in the two extracellular compartments: In the vacuole, potassium increased by 2.8±2.5 mmol/l to a ceiling level which was maintained during the standard train of light flashes. Potassium clearing in the dark was exponential with a half time of 60±26 s. In the intercellular space, repetitive photostimulation produced an initial rapid increase (half time <1 s) of the K⁺ concentration (mean† K ⁺_max =1.5±0.6 mmol/l). K⁺ clearing showed two superimposed components. A rapid one clears intercellular K⁺ after each light flash. The resultant K⁺ pulses ride on a slowly decreasing intercellular K+ level, and, following the last flash, K⁺ transiently undershoots the dark concentration.

Ouabain or a decrease in specimen temperature affect only the slow component and abolish the poststimulation K⁺ undershoot. Thus, the rapid component is interpreted as due to passive K⁺ dispersal by diffusion through the intercellular spaces, and the slow component and the poststimulation undershoot to K⁺ clearing by active reuptake of K⁺ into the photoreceptor cells.

K⁺ disappearance from the vacuole was not affected by ouabain, but a decrease in specimen temperature decreased the rate constant of K⁺ clearing, which has a Q₁₀ of 1.48. It is concluded that K⁺ clearing from the vacuole is dominated by passive processes, and that the Na⁺/K⁺-pump is possibly localized only in the non-receptive membrane domain.