On the molecular origins of thermal noise in vertebrate and invertebrate photoreceptors

Abstract

Retinal photoreceptors generate discrete electrical events in the dark indistinguishable from those evoked by light and the resulting dark signals limit visual sensitivity at low levels of illumination. The random spontaneous events are strongly temperature dependent and in both vertebrate and invertebrate photoreceptors require activation energies usually in the range of 23 to 28 kcal mol −1. Recent molecular orbital studies and pH experiments on horseshoe crabs ( Limulus) suggest that the thermal isomerization of a relatively unstable form of rhodopsin, one in which the Schiff-base linkage between the chromophore and protein is unprotonated, is responsible for thermal noise. This mechanism is examined in detail and compared to other literature models for photoreceptor noise. We conclude that this two-step process is likely to be the principal source of noise in all vertebrate and invertebrate photoreceptors. This model predicts that the rate of photoreceptor noise will scale in proportion to 10 −ξ, where ξ is the p K a of the Schiff base proton on the retinyl chromophore. Nature minimizes photoreceptor noise by selecting a binding site geometry which shifts the p K a of the Schiff base proton to > 16, a value significantly larger than the p K a of the chromophore in bacteriorhodopsin (p K a ≈ 13) or model protonated Schiff bases in solution (p K a ≈ 7).