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

看到红色：鸟类时间视觉和运动视觉的视网膜基础

• 批准号: BB/X020053/1
• 负责人: Tom Baden
• 金额: $ 104.44万
• 依托单位: University of Sussex
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2023
• 资助国家: 英国
• 起止时间: 2023 至 无数据
• 项目状态: 未结题
• 来源: https://gtr.ukri.org/projects?ref=BB%2FX020053%2F1
• 关键词: Seeing; red; retinal; basis; temporal

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.

鸟类的视力超过人类，是所有脊椎动物中视力最快的。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。所有的视觉都是从光感受器开始的，光感受器将恒定的光子流转化为可以被神经系统处理的电信号。因此，动物光感受器的类型和性质直接决定了什么可以看到，什么不能看到。例如，为了在夜间实现视觉，我们自己的眼睛依赖于敏感但“缓慢”的杆，而为了在白天支持视觉，我们使用不太敏感但更快的“红色”，“绿色”和“蓝色”锥。因此，与夜晚相比，我们的眼睛在白天更容易看到快速变化。鸟类也经历同样的权衡。不过，他们似乎解决得“更好”。在几乎任何光线水平下，都有一些鸟类以极快的速度快乐地飞行，在我们自己的眼睛几乎无法察觉的树枝上穿梭。这怎么可能？我们假设答案可能很简单，但也很基本：鸟类使用与我们相同的杆和锥。然而，除了这些，它们还有一套额外的、独立的光感受器：所谓的“双锥”。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锥细胞在支持“快速”视觉中的可能作用，分子证据表明双锥细胞使用“红色”敏感的视觉色素。然而，与任何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，这些双锥细胞支持快速视觉的想法从未被直接测试过，更不用说在神经元和电路水平上如何确切地发挥作用了。据我们所知，我们已经开发出了第一种工具，可以在培养皿中保持完整的鸟类视网膜存活并发挥作用，为直接的生理研究做好准备。基于这种新的能力，我们已经在鸟类中确定了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。这群细胞与所有其他记录的神经元非常不同，这些神经元的速度要慢得多，颜色偏好也更多样化。因此，我们假设（i）这些“红色”和“快速”输出神经元是由双锥驱动的，并且（ii）它们直接支撑鸟类的快速视觉。本提案旨在直接检验这些假设。目标.我们将使用来自两种鸟类（家禽小鸡和斑胸草雀）的1,000个视网膜输出神经元的电子记录来识别这些“快速”和“红色”神经元，并探索它们在支持快速视觉中的作用，最终了解它们在支持飞行中的作用。我们将联合收割机将这些记录与专门设计的实验操作相结合，以干扰不同的视锥细胞类型及其下游连接，以确定这些快速细胞是如何在电路水平上建立的。除了增加我们对鸟类如何“看到”的仍然非常有限的理解之外，我们的工作还将为如何设计光传感器（如相机系统）提供更一般的考虑，以更有效地权衡拍摄场景的不同方面，例如速度与颜色深度。