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Sensitivity and Adaptation in Vertebrate Photoreceptors: Evolution and Mechanism

Abstract

Lamprey are cyclostomes, which diverged from jawed vertebrates (fishes, amphibians, mammals) in the Cambrian perhaps 500 Mya. Using single-cell measurements with suction recording from the photoreceptors of adult�Petromyzon marinus�we first show that this primitive vertebrate has a duplex retina: rods respond to single photons, have a longer integration time, and are 80 times more sensitive than cones, much as in other vertebrates. We then demonstrate that responses to maintained steps of light decay as in other vertebrates and flash responses superimposed on steady backgrounds show decreases in sensitivity and changes in waveform in both rods and cones, also typical of other vertebrates. Backgrounds produce a decrease in maximum flash-response amplitude and an increase in the flash intensity necessary to produce a detectable response, with characteristic shifts of response-intensity curves along the intensity axis. Increasing background light had little effect on response onset but monotonically increased the rate of response decay. Sensitivity as a function of background intensity decreased by Weber’s Law in both rods and cones; rods show incremental saturation, and cones begin to adapt near the intensity at which rod saturation occurs. Bright bleaching light produces an equivalent background, with opsin in rods 7.5 x 10-6�times as effective in stimulating the cascade as Rh* (2 x 10-5�in mouse rods). The decreases in sensitivity and acceleration of response decay in stably bleached photoreceptors can be nearly completely reversed with exogenous 11-cis�retinal.

We then used mice to demonstrate that in wild-type animals background lights decrease the sensitivity of the rod and accelerate the kinetics of the response, and these processes occur rapidly within 250ms after presentation of the background. We also recorded the dark current from recoverin-knockout photoreceptors and did not detect any changes in flash sensitivity. However, responses to steps of light were significantly desensitized and the rate of reduction in sensitivity is much faster when recoverin is eliminated compared to wild-type rods. The waveform of the response however, appears to be independent of the background intensity in recoverin-knock out animals.

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