Genetic Dissection Reveals Two Separate Retinal Substrates for Polarization Vision in Drosophila

Abstract

SUMMARY Background Linearly polarized light originates from atmospheric scattering, or surface reflections, and is perceived by, insects, spiders, cephalopods crustaceans and some vertebrates. Thus, the neural basis underlying how this fundamental quality of light is detected is of broad interest. Morphologically unique, polarization-sensitive ommatidia exist in the dorsal periphery of many insect retinas, forming the ‘Dorsal Rim Area’ (DRA). However, much less is known about the retinal substrates of behavioral responses to polarized reflections. Summary Drosophila exhibits polarotactic behavior, spontaneously aligning with the e-vector of linearly polarized light, when stimuli are presented either dorsally or ventrally. By combining behavioral experiments with genetic dissection and ultrastructural analyses, we show that distinct photoreceptors mediate the two behaviors: inner photoreceptors R7+R8 of DRA ommatidia are necessary and sufficient for dorsal polarotaxis, whereas ventral responses are mediated by combinations of outer and inner photoreceptors, both of which manifest previously unknown features that render them polarization-sensitive. Conclusions Drosophila uses separate retinal pathways for the detection of linearly polarized light emanating from the sky, or from shiny surfaces. This work establishes a behavioral paradigm that will enable genetic dissection of the circuits underlying polarization vision.

Homothorax and Extradenticle alter the transcription factor network in Drosophila ommatidia at the dorsal rim of the retina

“…Hence, important similarities exist between the genes and pathways responsible for patterning of retinal mosaics in both flies and vertebrates. Understanding the transcriptional networks responsible for specification of individual retinal cell fates is therefore of general interest.The DRA is both necessary and sufficient for mediating orientation responses to polarized light perceived with the dorsal eye (Wernet et al, 2012). Here we have shown how factors expressed specifically in DRA R7 and R8 alter the transcriptional network of Drosophila ommatidia, resulting in a unique pattern specific to the DRA.…”

“…A fourth ommatidial subtype is always found in the DRA, a narrow band along the dorsal head cuticle (Wada, 1974). The diameter of their inner photoreceptor rhabdomeres (light-gathering organelles) is enlarged, their rhabdomeric microvilli are untwisted, and their orientation in R7 is orthogonal to that of R8 microvilli (Wernet et al, 2012). As a result, DRA inner photoreceptors manifest high polarization sensitivity (Hardie, 1985).…”

Extreme polarization sensitivity in the retina of the corn borer moth Ostrinia

“…5E). Polarisation vision outside the DRA has been also demonstrated in the apposition eyes of the butterfly Papilio (Kelber et al, 2001;Kinoshita et al, 2011), backswimmer bugs, dragonflies and locusts to detect water (Schwind, 1983(Schwind, , 1985Wildermuth, 1998;Shashar et al, 2005), in horseflies to detect mammalian fur (Horvath et al, 2008), and in fruit flies (Wernet et al, 2012).…”

“…The probability of light absorption by the microvilli is highest when their long axis coincides with the direction of the electric field vector (e-vector) of incident light, and hence the PS of a photoreceptor can be inferred from the geometry of its rhabdomere (Meinecke and Langer, 1982;Wernet et al, 2012). In the main retina (i.e.…”

Establishing and maintaining gene expression patterns: insights from sensory receptor patterning

“…At the dorsal margin of the eye, the so-called dorsal rim area (DRA) ommatidia contain R7 and R8 PRs with enlarged rhabdomeres that both express Rh3 and mediate polarization vision Wernet et al, 2012). Furthermore, in the dorsal third of the eye y ommatidia are modified (located above the dotted line in Fig.…”