Ancestral circuits for vertebrate colour vision emerge at the first retinal synapse

Abstract

SummaryFor colour vision, retinal circuits separate information about intensity and wavelength. This requires comparison of at least two spectrally distinct photoreceptors, as in the case of most mammals. However, many vertebrates use the full complement of four ‘ancestral’ cone-types (‘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 larval zebrafish, which involves the full ancestral complement of four cone- and three horizontal cell types. 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.