Quantifying the relationship between optical anatomy and retinal physiological sensitivity: A comparative approach

Abstract

Light intensity varies 1 million-fold between night and day, driving the evolution of eye morphology and retinal physiology. Despite extensive research across taxa showing anatomical adaptations to light niches, surprisingly few empirical studies have quantified the relationship between such traits and the physiological sensitivity to light. In this study, we employ a comparative approach in frogs to determine the physiological sensitivity of eyes in two nocturnal (Rana pipiens, Hyla cinerea) and two diurnal species (Oophaga pumilio, Mantella viridis), examining whether differences in retinal thresholds can be explained by ocular and cellular anatomy. Scotopic electroretinogram (ERG) analysis of relative b-wave amplitude reveals 10- to 100-fold greater light sensitivity in nocturnal compared to diurnal frogs. Ocular and cellular optics (aperture, focal length, and rod outer segment dimensions) were assessed via the Land equation to quantify differences in optical sensitivity. Variance in retinal thresholds was overwhelmingly explained by Land equation solutions, which describe the optical sensitivity of single rods. Thus, at the b-wave, stimulus-response thresholds may be unaffected by photoreceptor convergence (which create larger, combined collecting areas). Follow-up experiments were conducted using photopic ERGs, which reflect cone vision. Under these conditions, the relative difference in thresholds was reversed, such that diurnal species were more sensitive than nocturnal species. Thus, photopic data suggest that rod-specific adaptations, not ocular anatomy (e.g., aperture and focal distance), drive scotopic thresholds differences. To the best of our knowledge, these data provide the first quantified relationship between optical and physiological sensitivity in vertebrates active in different light regimes.

Reproductive State Modulates Retinal Sensitivity to Light in Female Túngara Frogs

“…This resulted in a relative response curve with responses ranging from 0 to 1 (Miller and Dowling, 1970). Consistent with our previous work (Rosencrans et al, 2018), response threshold was defined as the light intensity eliciting a response 10% the amplitude of the maximum response. This light level was calculated after analyzing each individual V-Log(I) curve using a least-squares fit of the standard Boltzmann function:…”

“…All animal care, experimental and analysis methods are based on our previous work in frogs (Rosencrans et al, 2018).…”

“…While ERG recordings were taken from both eyes, only the recording from the eye with the highest signal-to-noise ratio was used to determine threshold, saturation, and slope of the V-Log(I) function, which shows the relative b-wave amplitude as a function of stimulus luminance. Based on our earlier study in frogs (Rosencrans et al, 2018), the b-wave amplitude was defined as the difference between the average voltage over 20 ms before the light flash and the maximum voltage between 50 and 400 ms after the flash. The initial step for each procedure consisted of four recordings (sweeps) with no light flash, enabling correction for DC potential in recordings.…”

“…Outer segments from 3 males and 3 females (30 cells from each sex) were measured using a light microscope with a calibrated reticule attachment. Although using thin slice plastic sections may limit analysis of some cells not sectioned at their longest or widest point, the method yields results not different from those using whole mounted retina and an adjustable focal plane (e.g., DIC microscopy; Rosencrans et al, 2018). Land optical sensitivity (Eq.…”

“…Frogs are visual animals (Lettvin et al, 1959;Ewert, 1987); even nocturnal species see well at night (Rosencrans et al, 2018). In some species, visual cues, such as vocal sac or body coloration, mediate aspects of their mate choice (Summers et al, 1999;Gomez et al, 2009;Starnberger et al, 2014).…”