Seeing red: The retinal basis for temporal and motion vision in birds

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Surpassing humans, birds have the fastest vision of all vertebrates. We will elucidate how this exceptional visual capability emerges at the level of the retina.Background. All vision begins with photoreceptors that transduce the constant flux of photons into electrical signals that can be processed by the nervous system. Accordingly, the types and properties of an animals' photoreceptors directly dictate what can and cannot be seen. For example, to enable vision at night our own eyes rely on sensitive but "slow" rods, while to support vision during the day, we use our less sensitive but faster 'red', 'green', and 'blue' cones instead. Consequently, our eyes are much better at seeing fast change during the day compared to the night. Birds experience the same trade-off. However, they seem to solve it "better". At pretty much any light level, there exist species of birds that quite happily fly at breakneck speeds, weaving through branches that our own eyes would barely detect before it is too late. How is this possible?We hypothesise that the answer might be quite simple, but also quite fundamental: Birds use the same rods and cones that we do. However, in addition to those, they also have an extra, separate set of photoreceptors: the so-called "double cones". In most species of birds, these double cones make up as many as 40-50% of all photoreceptors. Previous anatomical, behavioural, and computational work has long hinted at a possible role of these cones in supporting 'fast' vision, and molecular evidence shows that double cones use a 'red' sensitive visual pigment. However, unlike for any other major vertebrate lineage (fish, amphibians, reptiles, mammals), direct light-driven recordings from retinal neurons of birds have not been achieved. Consequently, the idea that these double cones support fast vision has never been directly tested, let alone how exactly this would work at a neuronal and circuit level.We recently overcame this long-standing experimental roadblock. We have developed the tools - to our knowledge for the first time - to keep intact bird retina alive and functioning in a dish, ready for direct physiological investigations. Based on this new capability, we have identified a set of retinal output neurons in birds that exclusively respond to 'fast' flickering light, with a strong preference for 'red' light. This population of cells is very different from all other recorded neurons, which are substantially slower and more diverse in their colour preferences. Accordingly, we hypothesise that (i) these 'red'&'fast' output neurons are driven by the double cones, and that (ii) they directly underpin birds' fast vision. This proposal sets out to directly test these hypotheses. Objectives. We will use electrical recordings from 1,000s of retinal output neurons in two species of birds (poultry chicks and zebra finch) to characterise these 'fast'&'red' neurons, and to probe their role in supporting fast vision, ultimately in view in understanding their role in supporting flight. We will combine these recordings with experimental manipulations specifically designed to interfere with different cone-photoreceptor types and their downstream connections to pinpoint how these fast cells are built at a circuit level.Impact. Beyond adding to our still very limited understanding of how birds 'see', our work will also feed into more general considerations how to design light-sensors such as camera systems to more effectively trade-off different aspects of the filmed scene, such as speed versus colour depth.