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Published July 26, 2021 | Supplemental Material
Journal Article Open

Neural mechanism of spatio-chromatic opponency in the Drosophila amacrine neurons


Visual animals detect spatial variations of light intensity and wavelength composition. Opponent coding is a common strategy for reducing information redundancy. Neurons equipped with both spatial and spectral opponency have been identified in vertebrates but not yet in insects. The Drosophila amacrine neuron Dm8 was recently reported to show color opponency. Here, we demonstrate Dm8 exhibits spatio-chromatic opponency. Antagonistic convergence of the direct input from the UV-sensing R7s and indirect input from the broadband receptors R1–R6 through Tm3 and Mi1 is sufficient to confer Dm8's UV/Vis (ultraviolet/visible light) opponency. Using high resolution monochromatic stimuli, we show the pale and yellow subtypes of Dm8s, inheriting retinal mosaic characteristics, have distinct spectral tuning properties. Using 2D white-noise stimulus and reverse correlation analysis, we found that the UV receptive field (RF) of Dm8 has a center-inhibition/surround-excitation structure. In the absence of UV-sensing R7 inputs, the polarity of the RF is inverted owing to the excitatory input from the broadband photoreceptors R1–R6. Using a new synGRASP method based on endogenous neurotransmitter receptors, we show that neighboring Dm8s form mutual inhibitory connections mediated by the glutamate-gated chloride channel GluClα, which is essential for both Dm8's spatial opponency and animals' phototactic behavior. Our study shows spatio-chromatic opponency could arise in the early visual stage, suggesting a common information processing strategy in both invertebrates and vertebrates.

Additional Information

© 2021 Elsevier. Received 23 March 2021, Revised 26 April 2021, Accepted 27 April 2021, Available online 24 May 2021. We thank Dr. Vanessa Ruta for providing the construct of synaptotagmin::GCaMP6s, Drs. Doekele Stavenga and Gregor Belušič for helpful comments, and Marcus Calkins for editing and manuscript handling. This work was supported by Academia Sinica (to C.-H.L., Y.L., P.-J.C., and T.-Y.L.), the Intramural Research Program (to C.-Y.T., P.M., R.P., and T.P.), NIH (R01 EY028116 to K.G.Z.), the Air Force Office of Scientific Research/European Office of Aerospace Research and Development (AFOSR/EOARD) (FA9550-15-1-0068 to M.I.), MoST (110-2311-B-001-005-MY3 to C.-H.L.), the European Regional Development Fund (International Competitiveness of Research, Innovation and Technological Development), and MESS of R Slovenia (Early Career Researchers scheme, decision letter 5442-1/2018/434 to P.P.). Author contributions. Conceptualization, Y.L., P.-J.C., and C.-H.L.; methodology, C.-Y.T., R.P., M.I., P.P., T.P., M.S.D., and A.B.; investigation, Y.L., P.-J.C., T.-Y.L., C.-Y.T., and C.-H.L.; writing, Y.L., P.-J.C., P.P., and C.-H.L.; funding acquisition, M.I., P.P., K.G.Z., and C.-H.L.; resources, P.M., K.P.M., and K.G.Z.; supervision, C.-H.L. The authors declare no competing interests.

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August 22, 2023
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