Mechanisms of Color Coding in Insects

Models of sensory processing have historically abstracted underlying biological circuits, due to unknown connectivity and/or complexity. In contrast, the use of tractable and anatomically well-characterized model organisms such as the fruit fly Drosophila melanogaster allows us to utilize biological constraints in models of sensory processing to understand underlying circuit mechanisms and make more accurate predictions. This approach has been used to dissect motion vision circuits, but investigations into color vision - a salient visual feature for many animals - have been limited. Here, we investigate the circuit mechanisms of the early color circuit of the fruit fly and assess its information processing capabilities. Using in vivo two-photon calcium imaging and genetic manipulations, we measure the chromatic tuning properties of photoreceptor axons and their primary targets in the medulla neuropil. At the level of photoreceptor axons, we show that opponent processes are the result of a dual mechanism - a direct pathway specific to insect physiology and an indirect pathway found across the animal kingdom. Both pathways are necessary to decorrelate incoming signals and efficiently represent chromatic information. We built an anatomically constrained model that is able to quantitatively reproduce these color opponent responses without fitting synaptic weights. Instead, we used electron-microscopy-derived synaptic count, an anatomically defined measure, as a proxy for synaptic weight, thereby linking structure to function. Downstream of photoreceptors, we find that neurons shift their tuning and become highly selective for particular directions in color space - similar to “hue-selective” neurons in primate cortex. To achieve this selectivity, these neurons require input from all types of photoreceptors and an interneuron that determines the neuron's preferred chromatic direction. We extended our anatomically constrained model to incorporate these downstream neurons and are able to predict their responses, qualitatively and quantitatively.In summary, the detailed reconstruction of the fly circuit anatomy predicts the mechanisms of multiple stages of color information processing and allows us to infer functional roles for each part of the circuit. The circuit motifs, we uncover, are shared across species and hint at convergent mechanisms that underlie the transformation from an opponent neural code to a hue selective code.