Two-photon calcium recordings of cones

For colour vision, retinal circuits separate information about intensity and wavelength. This requires circuit-level comparison of at least two spectrally distinct photoreceptors. However, many vertebrates use all four 'ancestral' photoreceptors ('red', 'green', 'blue', 'UV'), and in those cases the nature and implementation of this computation remains poorly understood. Here, we establish the complete circuit architecture of outer retinal circuits underlying colour processing in the tetrachromatic larval zebrafish, which involves all four ancestral cone types and three types of horizontal cells. Our findings reveal that the synaptic outputs of red- and green-cones efficiently rotate the encoding of natural daylight in a principal component analysis (PCA)-like manner to yield primary achromatic and spectrally-opponent axes, respectively. Together, these two cones capture 91.3% of the spectral variance in natural light. Next, blue-cones are tuned so as to capture most remaining variance when opposed to green-cones. Finally, UV-cones present a UV-achromatic axis for prey capture. We note that fruit flies – the only other tetrachromat species where comparable circuit-level information is available - use essentially the same strategy to extract spectral information from their relatively blue-shifted terrestrial visual world. Together, our results suggest that rotating colour space into primary achromatic and chromatic axes at the eye's first synapse may be a fundamental principle of colour vision when using more than two spectrally well-separated photoreceptor types.

在色觉加工过程中，视网膜回路会分离光强与光波长相关的信息。该过程要求至少两种光谱特性迥异的光感受器（photoreceptor）开展回路级别的对比。然而，多数脊椎动物拥有全部四种“祖先型”光感受器——即红、绿、蓝、紫外光感受器，此类物种中该计算过程的本质与实现机制仍有待阐明。本研究明确了四色视觉斑马鱼幼体中参与色觉处理的视网膜外层回路的完整架构，该回路涵盖全部四种祖先型视锥细胞与三种水平细胞（horizontal cell）。研究结果显示，红、绿视锥细胞的突触输出以类似主成分分析（PCA）的方式，对自然光的编码进行高效旋转变换，分别生成主要的消色差轴与光谱拮抗轴。这两种视锥细胞可共同捕获自然光中91.3%的光谱方差。进一步分析表明，蓝视锥细胞经过调谐，可在与绿视锥细胞形成拮抗时捕获绝大多数剩余的光谱方差。最后，紫外视锥细胞则构建出服务于捕食行为的紫外消色差轴。我们注意到，果蝇——目前仅有的另一种拥有完整回路级实验数据的四色视觉物种——其视觉系统实质上采用了相同的策略，从其相对偏向蓝端的陆生视觉环境中提取光谱信息。综上，本研究结果表明，当拥有超过两种光谱特性差异显著的光感受器时，在视觉系统的第一突触位点将色觉空间旋转为主要消色差与色觉拮抗轴，或许是色觉处理的一项基本原理。