Interaction of “chromatic” and “achromatic” circuits in Drosophila color opponent processing

Color vision is an important sensory capability of humans and many animals. It relies on color opponent processing in visual circuits that gradually compare the signals of photoreceptors with different spectral sensitivities. In Drosophila, this comparison begins already in the presynaptic terminals of UV-sensitive R7 and longer wavelength-sensitive R8 inner photoreceptors that inhibit each other in the medulla. How downstream neurons process their signals is unknown. Here, we report that the second order medulla interneuron Dm8 is inhibited when flies are stimulated with UV light and strongly excited in response to a broad range of longer wavelength (VIS) stimuli. Inhibition to UV light is mediated by histaminergic input from R7 and expression of the histamine receptor ort in Dm8, as previously suggested. However, two additional excitatory inputs antagonize the R7 input. First, activation of R8 leads to excitation of Dm8 by non-canonical photoreceptor signaling and cholinergic neurotransmission in the visual circuitry. Second, activation of outer photoreceptors R1–R6 with broad spectral sensitivity causes excitation in Dm8 through the cholinergic medulla interneuron Mi1, which is known for its major contribution to the detection of spatial luminance contrast and visual motion. In summary, Dm8 mediates a second step in UV/VIS color opponent processing in Drosophila by integrating input from all types of photoreceptors. Our results demonstrate novel insights into the circuit integration of R1–R6 into color opponent processing and reveal that chromatic and achromatic circuitries of the fly visual system interact more extensively than previously thought. •Calcium imaging reveals a second step in color opponent processing in Drosophila•Dm8 antagonistically processes R7 (UV) and R8 + R1–R6 (UV to VIS) inputs•Activation of R8 causes excitation in Dm8 by non-canonical photoreceptor signaling•R1–R6 convey “achromatic” input to Dm8 through cholinergic Mi1 neurons Pagni et al. reveal physiological insight into color opponent processing in a second order visual interneuron in Drosophila. Chromatic and achromatic circuits interact extensively to enable UV/VIS color opponent processing in this cell type that can explain its role in spectral behavior.