Light Adaptation in Salamander L-Cone Photoreceptors

Abstract

The responses of individual salamander L-cones to light steps of moderate intensity (bleaching 0.3-3% of the total photopigment) and duration (between 5 and 90 s) were recorded using suction electrodes. Light initially suppressed the circulating current, which partially recovered or "sagged" over several seconds. The sensitivity of the cone to dim flashes decreased rapidly after light onset and approached a minimum within 500 ms. Background light did not affect the rising phase of the dim flash response, a measure of the initial gain of phototransduction. When the light was extinguished, the circulating current transiently exceeded or "overshot" its level in darkness. During the overshoot, the sensitivity of the cone required several seconds to recover. The sag and overshoot remained in voltage-clamped cones. Comparison with theory suggests that three mechanisms cause the sag, overshoot, and slow recovery of sensitivity after the light step: a gradual increase in the rate of inactivation of the phototransduction cascade during the light step, residual activity of the transduction cascade after the step is extinguished, and an increase in guanylate cyclase activity during the light step that persists after the light is extinguished.Key words: photoreceptor; phototransduction; cone adaptation; retina adaptation; light; vision IntroductionA common feature of sensory systems is their ability to function under widely varying stimulus conditions. Cone photoreceptors, which provide the dominant input to daylight vision, operate over a range of more than one million in mean light intensity. Even within a single visual scene, cones encounter light intensities that vary as much as 10,000-fold (Xiao et al., 2002). To encode these visual inputs effectively, cones must adjust their sensitivity, or adapt, to large changes in illumination.Visual information is encoded in photoreceptors by a G-protein-coupled signal transduction cascade (for review, see Yau, 1994;Arshavsky et al., 2002) (see Fig. 7). Light absorption by the photopigment ( R) triggers the serial activation of multiple G-proteins, causing the amplified stimulation of the enzyme phosphodiesterase (PDE). The activated phosphodiesterase (PDE*) hydrolyzes the second messenger cGMP, causing cGMPgated channels in the cone outer segment to close, suppressing the circulating current and causing a fall in intracellular Ca 2ϩ . The decrease in Ca 2ϩ activates guanylate cyclase, accelerating its rate of cGMP synthesis. This negative feedback counters the light-induced increase in hydrolytic activity, partially restoring the cGMP concentration. Light-activated photopigment (R*) and PDE* are inactivated through a separate series of biochemical reactions. The decrease in circulating current hyperpolarizes the cell and modulates the release of neurotransmitter at the cone output synapse, sending a signal to the rest of the retina.In rods, many of these biochemical steps appear to be modulated during adaptation (for review, see Fain et al., 2001). Adaptation in cones is less wel...

Light-Driven Calcium Signals in Mouse Cone Photoreceptors

“…4 E 1 ), reminiscent of the current undershoot reported for primate cones (Baylor et al, 1987). This undershoot was proposed to be related to delayed activation of GCs (Soo et al, 2008) by GC activating protein 2 (GCAP2), which, during light adaptation, regulates GC activity to restore high resting [Ca 2ϩ ] levels (Mendez et al, 2001). An alternative explanation is VGCC-dependent spiking, which has been reported for human rods (Kawai et al, 2001) and cones (Schnapf et al, 1990).…”

Adaptation of Mammalian Photoreceptors to Background Light: Putative Role for Direct Modulation of Phosphodiesterase

“…Tranchina showed that both WT and GCAPs−/− mouse rod response waveform and sensitivity could be modeled by assuming that light directly regulates the decay of PDE6. Unlike Soo et al [46], however, Tranchina found that modulation of only light-activated PDE6 could not explain the responses of WT and GCAPs−/− rods; the decay of both spontaneous and light-activated PDE6 had to be accelerated to produce model calculations that replicated actual recordings.…”

“…We can tell that this is so by comparing the open circles to the curve of large dashes, which is the prediction of a simple expression that assumes that all of adaptation has been eliminated and that the rod is simply summing responses of single photons with no active mechanism of sensitivity regulation [12]. The open circles should also be compared to the dotted curve of Chen et al [14], from a model developed by Dan Tranchina based on earlier models of Hamer and collaborators [44] and of Soo et al [46]. The Tranchina model successfully predicts Weber-Fechner-like adaptation for WT rods [14], but the dotted curve in Fig.…”

“…The experiments of Soo et al [46] were most successfully modeled if light was hypothesized to produce a slow increase in the decay of light-activated PDE, though no distinction could be made between modulation of Rh* decay and direct modulation of the PDE itself. A model like the one Soo et al used was also exploited by Daniel Tranchina in the study of Chen et al [14].…”

Rod Phototransduction Determines the Trade-Off of Temporal Integration and Speed of Vision in Dark-Adapted Toads

“…. The initial rise of the photoreceptor response remains rather constant under moderate adaptation (Thomas and Lamb, 1999;Friedburg et al, 2001;Nymark et al, 2005) and is similar in cones as well (Soo et al, 2008). Because visual latency (or reaction time) is basically determined by the rising edge of responses (Donner, 1989b), delaying recovery kinetics alone need not slow down reactions to moving contrast borders.…”