The neural basis of color vision: (I) photoreceptor interactions and origin of color opponent processing.

• Applicant: Professor Dr. Dierk F. Reiff
• Subject Area: Cognitive, Systems and Behavioural Neurobiology ; Molecular Biology and Physiology of Neurons and Glial Cells
• Term: from 2018 to 2022
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 408330929

• Final Report Year: 2023

Final Report Abstract

Understanding the circuit implementation of color vision is a major goal in visual neuroscience. We recently paved the way for a rigorous analysis of the neuronal circuits underlying color vision in Drosophila. Inner photoreceptors R7/R8 of ‘pale’ and ‘yellow’ ommatidia convey [UVshort vs. blue] and [UVlong vs. green] color opponent (CO) signals to the color vision circuitry in the medulla, respectively. Two parallel mechanisms underlie this processing: R7/R8 of the same ommatidium mutually inhibit each other, and unidentified medulla neurons and mechanisms mediate feedback inhibition. Our research revealed that 2nd order visual interneurons Dm9 mediate feedback inhibition from the medulla to R7/R8. Dm9 are packed with glutamatergic synaptic vesicles, hyperpolarize to light of all wavelength, detect histaminergic R7/R8 input via Ort receptors, and receive excitation from R7py via unknown mechanisms. Ort is required in Dm9 for CO in R8, but not R7. Optogenetic inhibition of Dm9 that mimics light ON, hyperpolarizes R7p, R7y, R8p, and R8y, prohibits CO processing in all R7/R8, and shifts their sensitivity to higher light intensities. These findings suggest a simple feedback model in early color vision: light-activated R7/R8 hyperpolarize Dm9 that then release less ‘excitatory’ glutamate to R7/R8 to counteract light-induced depolarization of fly photoreceptors. This dual role of Dm9 in CO processing and adaptation represents an unexpected commonality with the multiple roles of vertebrate HCs in early visual processing. 2nd order visual interneurons Dm8 instead accomplish a second step in CO processing. Contradictory to the reported simple function of Dm8 in pooling R7 input, Dm8 cells exhibit complex [UV vs. VIS] CO responses. R7py inhibit Ort-expressing Dm8 via direct histaminergic synapses. In parallel, Dm8 receive strong indirect excitatory input from R8py and R1-R6 that together sample the entire spectrum visible to the fly (VIS). R1-R6 excite Dm8 via lamina monopolar cells and the medulla neuron Mi1, a keyplayer in ON-motion detection. R8 excite Dm8 by largely unknown mechanisms that involve cholinergic signaling. We revised some of these findings with a comparative perspective in our review article on insect color vision (awarded by J. Comp. Physiol. A with the Readers’ Choice Award 2022). In summary, we enabled significant advances in the understanding of early spectral processing in Drosophila and revealed surprising commonalities with the vertebrate retina. The new findings, here unmentioned results, and the engineering of a novel visual stimulation device open new perspectives on Drosophila color vision and provide us with a solid basis for ongoing and future research.

Publications

• Color vision in insects: insights from Drosophila. Journal of Comparative Physiology A, 206(2), 183-198.
  Schnaitmann, Christopher; Pagni, Manuel & Reiff, Dierk F.
  
• Interaction of “chromatic” and “achromatic” circuits in Drosophila color opponent processing. Current Biology, 31(8), 1687-1698.e4.
  Pagni, Manuel; Haikala, Väinö; Oberhauser, Vitus; Meyer, Patrik B.; Reiff, Dierk F. & Schnaitmann, Christopher