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

鸟类的视力超过人类，是所有脊椎动物中最快的。我们将阐明这种特殊的视觉能力是如何在视网膜水平上出现的。所有的视觉都始于光感受器，光感受器将持续不断的光子转换成可以被神经系统处理的电信号。因此，动物感光器的类型和特性直接决定了什么能被看到，什么不能被看到。例如，在夜间，我们的眼睛依靠敏感但“慢”的视杆细胞来支持视觉，而在白天，我们使用不太敏感但更快的“红”、“绿”和“蓝”视锥细胞来支持视觉。因此，与夜晚相比，我们的眼睛在白天能更好地看到快速变化。鸟类也经历着同样的权衡。然而，他们似乎“更好”地解决了这个问题。在几乎任何光线水平下，都有一些鸟类以极快的速度愉快地飞行，在树枝间穿梭，我们的眼睛几乎察觉不到，否则就太晚了。这怎么可能呢？我们假设答案可能很简单，但也很基本：鸟类使用和我们一样的视杆细胞和视锥细胞。然而，除了这些，它们还有一组额外的、独立的光感受器：所谓的“双视锥细胞”。在大多数鸟类中，这些双锥细胞占所有光感受器的40-50%。以前的解剖学、行为学和计算工作早就暗示了这些视锥细胞在支持“快速”视觉方面的可能作用，分子证据表明，双视锥细胞使用一种“红色”敏感的视觉色素。然而，与其他主要脊椎动物谱系（鱼类、两栖动物、爬行动物、哺乳动物）不同，鸟类视网膜神经元的直接光驱动记录尚未实现。因此，双视锥细胞支持快速视觉的观点从未被直接测试过，更不用说它在神经元和电路层面上是如何工作的了。我们最近克服了这个长期存在的实验障碍。据我们所知，我们已经开发出了一种工具，可以在培养皿中保存完好的鸟类视网膜，使其存活并发挥功能，为直接的生理研究做好准备。基于这种新能力，我们已经确定了鸟类的一组视网膜输出神经元，它们只对“快速”闪烁的光做出反应，对“红色”光有强烈的偏好。这种细胞群与所有其他记录的神经元非常不同，它们的速度要慢得多，颜色偏好也更多样化。因此，我们假设(i)这些“红色”和“快速”的输出神经元是由双视锥驱动的，（ii）它们直接支撑了鸟类的快速视觉。这一提议旨在直接检验这些假设。目标。我们将使用来自两种鸟类（雏鸟和斑胸草雀）的1000个视网膜输出神经元的电记录来描述这些“快”和“红”神经元的特征，并探索它们在支持快速视觉方面的作用，最终了解它们在支持飞行方面的作用。我们将把这些记录与专门设计的实验操作相结合，以干扰不同的锥状光感受器类型及其下游连接，以查明这些快速细胞是如何在电路水平上构建的。除了增加我们对鸟类如何“看”的仍然非常有限的理解之外，我们的工作还将为更一般的考虑提供信息，如何设计光传感器，如相机系统，以更有效地权衡拍摄场景的不同方面，如速度与色彩深度。

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.