Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila

Abstract

The visual systems of most species contain photoreceptors with distinct spectral sensitivities that allow animals to distinguish lights by their spectral composition. In Drosophila, photoreceptors R1-R6 have the same spectral sensitivity throughout the eye and are responsible for motion detection. In contrast, photoreceptors R7 and R8 exhibit heterogeneity and are important for color vision. We investigated how photoreceptor types contribute to the attractiveness of light by blocking the function of certain subsets and by measuring differential phototaxis between spectrally different lights. In a "UV vs. blue" choice, flies with only R1-R6, as well as flies with only R7/R8 photoreceptors, preferred blue, suggesting a nonadditive interaction between the two major subsystems. Flies defective for UV-sensitive R7 function preferred blue, whereas flies defective for either type of R8 (blue-or green-sensitive) preferred UV. In a "blue vs. green" choice, flies defective for R8 (blue) preferred green, whereas those defective for R8 (green) preferred blue. Involvement of all photoreceptors [R1-R6, R7, R8 (blue), R8 (green)] distinguishes phototaxis from motion detection that is mediated exclusively by R1-R6.differential phototaxis | attractiveness function | R7/R8 sytem | color vision D epending on its spectral composition and intensity, light can serve as an attractive or repulsive landmark for orientation. Accordingly, animals identify an object or a light source at a certain location in visual space and approach or retreat from it. Phototaxis in insects has been a useful paradigm to gain a better understanding of this behavior. Here we take advantage of Drosophila genetics to investigate the function of the different subtypes of photoreceptors in this behavior.The Drosophila compound eye consists of about 750 ommatidia, each containing 8 photoreceptor cells (1). The six outer photoreceptors (R1-R6) contain a blue-sensitive rhodopsin (Rh1) and show a second sensitivity peak in the UV due to a sensitizing pigment (1-5). They are specialized for vision at low light levels and low pattern contrast (1, 6). They are necessary and sufficient for motion vision, and fly optomotor responses are abolished in their absence (7,8). The two inner photoreceptors (R7 and R8) are heterogeneous. Along the dorsal margin of the eye, both R7 and R8 express rhodopsin Rh3 that is sensitive to shorter wavelength UV (9). This part of the retina is specialized for the detection of the e-vector of polarized light (10, 11). The remaining part of the retina contains two types of ommatidia called pale (p) and yellow (y). In p-type ommatidia, R7 cells contain Rh3 (R7p) and R8 express bluesensitive Rh5 (R8p). In y-type ommatidia, R7 cells express Rh4 sensitive to longer wavelength UV (R7y) and R8 cells contain green-sensitive Rh6 (R8y) (Fig. 1A) (5, 12-15). R7y cells in the dorsal third of the eye coexpress Rh3 and Rh4 (16). Approximately 30% of the ommatidia are of the p-and 70% of the y-type, with the p-and y-subtypes distributed stochastically in ...

Proper splicing contributes to visual function in the aging Drosophila eye

“…In addition, no retinal degeneration was observed using either the Rh1‐luc reporter (Figure 4b) or optical neutralization (Supporting Information Figure S2). Previous studies have shown that the outer R1–R6 photoreceptors are not essential for phototaxis (Yamaguchi et al, 2010), suggesting a possible explanation for the stronger phototaxis phenotype observed with the pan‐photoreceptor longGMR‐Gal4 driver. Our data tentatively suggest that CG7564 and snRNP‐U1–70K might have a stronger role in regulating splicing of genes necessary for proper visual function.…”

“…Drosophila have eight photoreceptors in each ommatidium in the compound eye: six outer photoreceptors that express Rh1 and are largely responsible for motion, and two inner photoreceptors that are involved in color vision (Yamaguchi, Desplan, & Heisenberg, 2010). Our splicing analysis in photoreceptors examined the Rh1‐expressing outer photoreceptors, and so we next asked whether proper splicing was also necessary in these outer photoreceptors for visual behavior.…”

CRYPTOCHROME mediates behavioral executive choice in response to UV light

“…Light can serve as either a repellent or an attractive signal for an animal's behavior, depending on intensity and spectra. Many insects exhibit an innate spectral attraction to low-intensity UV light, as shown by phototaxis behavioral assays (36)(37)(38). In contrast, highintensity UV light induces avoidance behavior, particularly in larvae and egg-laying females (39,40), and reduces mating activity in adult male Drosophila (41).…”

Subcellular mapping of dendritic activity in optic flow processing neurons

“…Each ommatidium contains eight photoreceptor cells, R1--8, behind its own small lens. R7 and R8, the inner two receptor cells, are mainly involved in color vision [24,25], whereas R1--6 all contain the same light--sensitive pigment, rhodopsin 1 (rh1), and feed into motion detection circuits [26--28]. Rh1 has two absorption peaks, [modified from https://www.flickr.com/photos/77350506@N04/8971480924/in/photostream/].…”