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

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 amacr...

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Published in:Current biology Vol. 31; no. 14; pp. 3040 - 3052.e9
Main Authors: Li, Yan, Chen, Pei-Ju, Lin, Tzu-Yang, Ting, Chun-Yuan, Muthuirulan, Pushpanathan, Pursley, Randall, Ilić, Marko, Pirih, Primož, Drews, Michael S., Menon, Kaushiki P., Zinn, Kai G., Pohida, Thomas, Borst, Alexander, Lee, Chi-Hon
Format: Journal Article
Language:English
Published: England Elsevier Inc 26-07-2021
Subjects:
Animals
Color Perception - physiology
color vision
Drosophila
GluClα
lateral inhibition
Neurons - physiology
receptive field
Retina
spatial opponency
spectral opponency
visual circuits
receptive field
lateral inhibition
spectral opponency
Drosophila
visual circuits
GluClα
spatial opponency
color vision
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Summary: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. [Display omitted] •The Drosophila amacrine neuron Dm8 exhibits spatio-chromatic opponency•Pale and yellow Dm8 subtypes have distinct UV/Vis color opponent properties•Lateral inhibition shapes Dm8’s center-surround antagonistic receptive field•GluClα is critical for Dm8’s spatial receptive field and fly’s phototaxis behavior Li et al. demonstrate spatio-chromatic opponency in a fly amacrine neuron and reveal its underlying neural circuit mechanisms, including antagonistic convergence of different photoreceptor inputs and lateral inhibition by mutual inhibitory connections. Double opponent neurons could arise in early visual pathways and play important behavioral roles.
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ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2021.04.068