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
Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, Taiwan, Republic of China.
Section on Neuronal Connectivity, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892, USA.
Curr Biol. 2021 Jul 26;31(14):3040-3052.e9. doi: 10.1016/j.cub.2021.04.068. Epub 2021 May 24.
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.
视觉动物能够检测光强度和波长组成的空间变化。拮抗编码是减少信息冗余的常见策略。在脊椎动物中已鉴定出具有空间和光谱拮抗能力的神经元，但在昆虫中尚未发现。最近有报道称果蝇无长突神经元Dm8表现出颜色拮抗。在此，我们证明Dm8表现出空间 - 颜色拮抗。来自紫外线敏感的R7s的直接输入以及通过Tm3和Mi1来自宽带受体R1 - R6的间接输入的拮抗汇聚足以赋予Dm8紫外线/可见光拮抗能力。使用高分辨率单色刺激，我们发现继承视网膜镶嵌特征的Dm8的浅色和黄色亚型具有不同的光谱调谐特性。使用二维白噪声刺激和反向相关分析，我们发现Dm8的紫外线感受野（RF）具有中心抑制/周边兴奋结构。在没有紫外线敏感的R7输入的情况下，由于来自宽带光感受器R1 - R6的兴奋性输入，RF的极性会反转。使用基于内源性神经递质受体的新synGRASP方法，我们表明相邻的Dm8形成由谷氨酸门控氯离子通道GluClα介导的相互抑制连接，这对于Dm8的空间拮抗和动物的趋光行为都至关重要。我们的研究表明空间 - 颜色拮抗可能出现在早期视觉阶段，这表明无脊椎动物和脊椎动物中存在共同的信息处理策略。
