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Chloride enters glial cells and photoreceptors in response to light stimulation in the retina of the honey bee drone

Double‐barrelled ion‐selective microelectrodes were used to measure free [Cl−] in photoreceptors, extracellular space, and glial cells in superfused slices of drone retina. Tests indicated that with normal superfusate the intracellular electrode signal was due essentially to Cl− and not to some other interfering anion. The results indicate that Cl− is more concentrated in both photoreceptors and glial cells than would be predicted for a passive electrochemical distribution. When the photoreceptors were stimulated by a standard train of 20 ms flashes, 1/s for 90 s, their intracellular free [Cl−] (Cli) rose by 8 ± 1 mM. At the end of stimulation Cli usually continued to rise for up to a further 2 min and then returned toward the baseline over about 10 min. During light stimulation Cli in the glia rose. The magnitude of the increase was 5.1 ± 0.4 mM, about half the increase in Ki. In some extracellular recording sites, light stimulation caused [Cl−] to increase and in others to decrease. The mean change was –0.7 mM, SD 6.5 mM. The Cl− that entered the photoreceptors and the glia was presumably made available by the shrinking of the extracellular space. When the cells were depolarized by increasing [K+] in the superfusate from 7.5 mM to 18 mM, Cli increased. The half‐time of the change in Cli was longer than the half‐time of the depolarization by 10–30 s in the glia and 50–250s in the photoreceptors. During superfusion with 0 Cl− Ringer's solution, the light‐induced rise in extracellular [K+] was greater by a factor of 1.4–2.7, and the clearance after the end of the stimulation was slower. The rate of increase in glial Ki during light stimulation fell; the rate of increase of glial Ki caused by superfusion with raised [K+] (in the absence of Cl−) fell more. We conclude that when extracellular [K+] is increased, entry of Cl− into the glia is necessary for part, but not all, of the net uptake of K+. During light stimulation, the observed movement of Cl− into glia contributes to homeostasis of extracellular [K+], and the cell swelling associated with movement of Cl− into both glia and photoreceptors contributes to homeostasis of extracellular [Na+].