The Fly Sensitizing Pigment Enhances UV Spectral Sensitivity While Preventing Polarization-Induced Artifacts

Abstract

Microvillar photoreceptors are intrinsically capable of detecting the orientation of e-vector of linearly polarized light. They provide most invertebrates with an additional sensory channel to detect important features of their visual environment. However, polarization sensitivity (PS) of photoreceptors may lead to the detection of polarization-induced false colors and intensity contrasts. Most insect photoreceptors are thus adapted to have minimal PS. Flies have twisted rhabdomeres with microvilli rotated along the length of the ommatidia to reduce PS. The additional UV-absorbing sensitizing pigment on their opsin minimizes PS in the ultraviolet. We recorded voltage from Drosophila photoreceptors R1–6 to measure the spectral dependence of PS and found that PS in the UV is invariably negligible but can be substantial above 400 nm. Using modeling, we demonstrate that in R1–6 without the sensitizing pigment, PS in the UV (PSUV) would exceed PS in the visible part of the spectrum (PSVIS) by a factor PSUV/PSVIS = 1.2–1.8, as lower absorption of Rh1 rhodopsin reduces self-screening. We use polarimetric imaging of objects relevant to fly polarization vision to show that their degree of polarization outdoors is highest in the short-wavelength part of the spectrum. Thus, under natural illumination, the sensitizing pigment in R1–6 renders even those cells with high PS in the visible part unsuitable for proper polarization vision. We assume that fly ventral polarization vision can be mediated by R7 alone, with R1–6 serving as an unpolarized reference channel.

Modular assays for the quantitative study of visually guided navigation in both flying and walking flies

“…To verify the efficacy of this stimulus presentation system, we have characterized the stimuli emanating from our apparatus using a polarimetric camera 27 (Figure 3B). By calculating the degree of linear polarization as previously described 27 , we confirm that the polarized stimuli manifest a high degree of polarization both in the UV (365 nm) as well as with a green LED (510 nm). In contrast, virtually no polarization is detected when the polarization filter / diffuser combination of the upper filter cassette is inverted.…”

Horsefly object-directed polarotaxis is mediated by a stochastically distributed ommatidial subtype in the ventral retina

“…We have previously shown that the contrast between the polarized patterns reflected from fur or water and the surrounding visual clutter is optimal in the UV- and blue-wavelength range (60). This has most likely driven the evolution of horsefly VPV to employ UV- and blue-sensitive photoreceptors.…”

“…The anatomical data were used to calculate the PS A as an estimate of the physiological photoreceptor PS. The calculations were based on a discrete model (60), modified from ref. 42.…”