Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration

Abstract

The vertebrate visual system can operate over a large range of light intensities. This is possible in part because the sensitivity of photoreceptors decreases approximately in inverse proportion to the background light intensity. This process, called photoreceptor light adaptation, is known to be mediated by a diffusible intracellular messenger, but the identity of the messenger is still unclear. There has been considerable speculation that decreased cytoplasmic Ca2+ concentration (Cai2+) may play a role in light adaptation, and recent experiments in which Ca2+ buffer was incorporated into rod-cells have supported this notion. The extent of the contribution of calcium, however, remains unresolved. We now show that light-dependent changes in sensitivity in amphibian photoreceptors can be abolished by preventing movements of Ca2+ across the outer-segment plasma membrane. These experiments demonstrate that light adaptation in photoreceptors is mediated in cones primarily, and in rods perhaps exclusively, by changes in Cai2+.

Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

“…Interestingly, the two mathematical relationships intersect at a background concentration, revealing that adaptation selectively reduces sensitivity at a low background but increases sensitivity at a high background. This dynamic adjustment of sensitivity during adaptation is in great contrast to the long-held view that adaptation always increases sensitivity as has been established for vertebrate photoreceptors (40,48).…”

“…Odor sensitivity in Drosophila Or-expressing OSNs adapts to the odor background in accordance with the Weber-Fechner relation, which is well known for describing the adaptation of retinal photoreceptors (40,48). In the absence of extracellular Ca 2+ , the Weber-Fechner relation no longer held and was replaced by a saturating exponential relationship with a concomitant reduction in the operating range.…”

“…As shown above, Ca 2+ entry during an odor response attenuated odor sensitivity, enabling OSNs to avoid saturation. Next, we quantified the changes in sensitivity and operating range during adaptation by adopting a standard protocol used for retinal photoreceptors (29,40). Specifically, we measured the incremental sensitivity of OSNs to a brief stimulation superimposed on a background stimulus.…”

Interactions between divalent cations and the gating machinery of cyclic GMP-activated channels in salamander retinal rods.

“…Ca ~+ entry in the dark provides negative feedback control of cGMP synthesis (LoUey and Racz, 1982;Pepe, Panfoli, and Cugnoli, 1986;Hodgkin and Nunn, 1988;Koch and Stryer, 1988;Dizhoor, Ray, Kumar, Niemi, Spencer, Brolley, Walsh, Philipov, Hurley, and Stryer, 1991). A light-induced drop in internal Ca 2+ concentration (Yau and Nakatani, 1985;McNaughton, Cervetto, and Nunn, 1986) is important for the recovery of the light response and for light adaptation (Matthews, Murphy, Fain, and Lamb, 1988;Nakatani and Yau, 1988b).…”

Calcium‐bound recoverin targets rhodopsin kinase to membranes to inhibit rhodopsin phosphorylation

“…Light-induced cGMP hydrolysis disrupts Ca 2+ influx through the cGMP-gated channel and lowers the intracellular Ca 2+ concentration through the continued extrusion of cytosolic Ca 2+ by the Na+-Ca2+/K + exchanger [1]. The light-induced decrease in Ca 2+ concentration plays an important role in light adaptation of photoreceptor cells [2,3]. Frog S-modulin and bovine recoverin, new members of the EF-hand superfamily, mediate this role of Ca 2+ [4] by inhibiting rhodopsin phosphorylation at high Ca 2+ concentration [5,6].…”