Motion vision is independent of color in Drosophila

Abstract

Whether motion vision uses color contrast is a controversial issue that has been investigated in several species, from insects to humans. We used Drosophila to answer this question, monitoring the optomotor response to moving color stimuli in WT and genetic variants. In the fly eye, a motion channel (outer photoreceptors R1-R6) and a color channel (inner photoreceptors R7 and R8) have been distinguished. With moving bars of alternating colors and high color contrast, a brightness ratio of the two colors can be found, at which the optomotor response is largely missing (point of equiluminance). Under these conditions, mutant flies lacking functional rhodopsin in R1-R6 cells do not respond at all. Furthermore, genetically eliminating the function of photoreceptors R7 and R8 neither alters the strength of the optomotor response nor shifts the point of equiluminance. We conclude that the color channel (R7/R8) does not contribute to motion detection as monitored by the optomotor response.apparent motion ͉ equiluminance ͉ motion detection ͉ opsin mutants ͉ R7/R8 system T he role of color vision in motion detection is still a matter of debate (for reviews, see refs. 1-3). In human vision, it was widely believed that color and motion are processed by parallel pathways (4). More recently, however, the complete segregation of motion detection and color vision came into question (for a review, see ref.2), because motion of the patterns of two equiluminant colors could still be detected. Thus, either the color vision system contributes to motion detection, or a residual difference in luminance could not have been eliminated experimentally (for a review, see ref. 1).In insects, it was first shown for the fleshfly Phormia that motion vision as monitored by the optomotor response depends on luminance contrast (5). Also in the honey bee, for which color vision is well established (6), the optomotor response has been shown to be largely insensitive to color contrast (7). The same was found for the landing response (8). Similar results were reported in vertebrate systems. In goldfish, which have a tetrachromatic color vision system (9), only L-cones (red) contribute to the optomotor response (10). In zebrafish larvae, both M-and L-cones seem to mediate motion responses, although only luminance information appears to be used (11). These studies clearly show that luminance contrast plays a major role in motion detection, as it does in humans. However, at the point of equiluminance, residual responses are frequently observed (5, 10), leaving the possibility that moving color contrast can, after all, elicit motion responses. So far, it was not possible to selectively switch off the color channel. Here, we used genetic intervention and the detailed knowledge of the Drosophila retina to address whether the color vision system contributes to motion detection.Drosophila has been shown to possess color vision (12, 13). As a prerequisite for this quality, an animal needs at least two types of photoreceptors differing in spectral sensitivity...

Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila

“…We have shown that all four photoreceptor types [R1-R6, R7(p, y), R8p, and R8y] are involved in phototaxis, in contrast to motion detection, which relies exclusively on R1-R6 photoreceptors (7,8). The wild-type attractiveness function cannot be described as the sum of the attractiveness functions of flies lacking one or more functional photoreceptor types.…”

“…To test this, we examined mutants defective for both R7 and R8 function. Because sev mutant flies lack R7 and have very few R8p cells, sev rh6 1 double mutants have only very few R8 cells expressing Rh5, and the sev rh5 2 rh6 1 triple mutant should have no functional opsins expressed in the inner photoreceptors; therefore, the contributions of R7 and R8 to the attractiveness function should be lost (8). These flies showed a preference for blue over UV.…”

“…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.…”

Elementary Motion Detection

“…There is a strong separation between different visual pathways. The different absorption spectra of the photoreceptors leads to a spilt of visual information into a chromatic and an achromatic channel (Cook and Desplan, 2001;Hardie, 1979;Sanes and Zipursky, 2010;Yamaguchi et al, 2008).…”

“…R1-R6 neurons provide an achromatic channel which is further divided into multiple information pathways including circuits for motion computation and phototaxis behavior (Hardie, 1979;Sanes and Zipursky, 2010;Yamaguchi et al, 2008;Zhu et al, 2009). The minimal circuitry presumed to be involved in motion detection starts with the photoreceptors R1-R6 which project into the lamina ( fig.…”