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The effect of light on outer segment calcium in salamander rods

Hugh R. Matthews and Gordon L. Fain*

Calcium acts as a second messenger in vertebrate rods, regulating the recovery phase of the light response and modulating sensitivity during light-adaptation. Since light not only decreases the outer segment calcium concentration ([Ca²⁺]_i) by closing cyclic nucleotide-gated channels but can also increase [Ca²⁺]_i by releasing Ca²⁺ from buffer sites or intracellular stores, we examined in detail the effect of light and circulating current on [Ca²⁺]_i by making simultaneous measurements of suction pipette current and [Ca²⁺]_i from isolated rods of the salamander Ambystoma tigrinum after incorporation of the fluorescent dye fluo-5F. When the release of Ca²⁺ is measured in 0 Ca²⁺-0 Na⁺ solution, minimising fluxes of Ca²⁺ across the plasma membrane, it is substantial only for light bright enough to bleach a significant fraction of the photopigment and is restricted to the part of the outer segment in which the bleach occurred. It is unlikely, therefore, to make a large contribution to [Ca²⁺]_i for most of the physiological operating range of the rod. Nevertheless, since release is half-maximal for a bleach of less than 10 %, it cannot be produced by a simple mechanism such as a change in the affinity of a binding site on rhodopsin itself but must instead require some more complex interaction. In Ringer solution, the Ca²⁺ in the light-releasable pool can be discharged merely by the decrease in [Ca²⁺]_i that occurs as the outer segment channels close. In steady background light or after exposure to saturating illumination, the fraction of Ca²⁺ in the pool decreases essentially in proportion to [Ca²⁺]_i as if Ca²⁺ were being removed from a buffer site within the cytoplasm. Furthermore, [Ca²⁺]_i itself changes in proportion to the circulating current, with little evidence for a contribution from Ca²⁺ release or other mechanisms of Ca²⁺ homeostasis. This indicates that flux of Ca²⁺ across the plasma membrane is the major determinant of outer segment Ca²⁺ concentration within the rod's normal operating light intensity range. Once Ca²⁺ has been discharged from the releasable pool, it is restored following dim illumination apparently as the simple result of the subsequent restoration of dark [Ca²⁺]_i and the rebinding of Ca²⁺ to its release site, but after brighter light perhaps also as a consequence of regeneration of the photopigment.

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