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

Li, Yan and Chen, Pei-Ju and Lin, Tzu-Yang and Ting, Chun-Yuan and Muthuirulan, Pushpanathan and Pursley, Randall and Ilić, Marko and Pirih, Primož and Drews, Michael S. and Menon, Kaushiki P. and Zinn, Kai G. and Pohida, Thomas and Borst, Alexander and Lee, Chi-Hon (2021) Neural mechanism of spatio-chromatic opponency in the Drosophila amacrine neurons. Current Biology, 31 (14). pp. 3040-3052. ISSN 0960-9822. doi:10.1016/j.cub.2021.04.068. https://resolver.caltech.edu/CaltechAUTHORS:20210526-160617577

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Abstract

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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.cub.2021.04.068DOIArticle
ORCID:
AuthorORCID
Chen, Pei-Ju0000-0002-7099-9169
Lin, Tzu-Yang0000-0002-1968-177X
Ting, Chun-Yuan0000-0002-2302-4203
Muthuirulan, Pushpanathan0000-0001-6240-3073
Pursley, Randall0000-0002-7933-3291
Menon, Kaushiki P.0000-0003-1039-4704
Zinn, Kai G.0000-0002-6706-5605
Borst, Alexander0000-0001-5537-8973
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.
Funders:
Funding AgencyGrant Number
Academia SinicaUNSPECIFIED
NIHR01 EY028116
Air Force Office of Scientific Research (AFOSR)FA9550-15-1-0068
Ministry of Science and Technology (Taipei)110-2311-B-001-005-MY3
European Regional Development FundUNSPECIFIED
Ministry of Education, Science and Sport (Slovenia)5442-1/2018/434
Subject Keywords:Drosophila; color vision; visual circuits; spectral opponency; spatial opponency; receptive field; lateral inhibition; GluClα
Issue or Number:14
DOI:10.1016/j.cub.2021.04.068
Record Number:CaltechAUTHORS:20210526-160617577
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210526-160617577
Official Citation:Yan Li, Pei-Ju Chen, Tzu-Yang Lin, Chun-Yuan Ting, Pushpanathan Muthuirulan, Randall Pursley, Marko Ilić, Primož Pirih, Michael S. Drews, Kaushiki P. Menon, Kai G. Zinn, Thomas Pohida, Alexander Borst, Chi-Hon Lee, Neural mechanism of spatio-chromatic opponency in the Drosophila amacrine neurons, Current Biology, Volume 31, Issue 14, 2021, Pages 3040-3052.e9, ISSN 0960-9822, https://doi.org/10.1016/j.cub.2021.04.068.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109264
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:26 May 2021 23:22
Last Modified:02 Aug 2021 20:14

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