Double cones are the most common photoreceptor cell type in most avian retinas, but their precise functions remain a mystery. Among their suggested functions are luminance detection, polarized light detection, and light-dependent, radical pair-based magnetoreception. To better understand the function of double cones, it will be crucial to know how they are connected to the neural network in the avian retina. Here we use serial sectioning, multibeam scanning electron microscopy to investigate double-cone anatomy and connectivity with a particular focus on their contacts to other photoreceptor and bipolar cells in the chicken retina. We found that double cones are highly connected to neighboring double cones and with other photoreceptor cells through telodendria-to-terminal and telodendria-to-telodendria contacts. We also identified 15 bipolar cell types based on their axonal stratifications, photoreceptor contact pattern, soma position, and dendritic and axonal field mosaics. Thirteen of these 15 bipolar cell types contacted at least one or both members of the double cone. All bipolar cells were bistratified or multistratified. We also identified surprising contacts between other cone types and between rods and cones. Our data indicate a much more complex connectivity network in the outer plexiform layer of the avian retina than originally expected.

SIGNIFICANCE STATEMENT Like in humans, vision is one of the most important senses for birds. Here, we present the first serial section multibeam scanning electron microscopy dataset from any bird retina. We identified many previously undescribed rod-to-cone and cone-to-cone connections. Surprisingly, of the 15 bipolar cell types we identified, 11 received input from rods and 13 of 15 received at least part of their input from double cones. Therefore, double cones seem to play many different and important roles in avian retinal processing, and the neural network and thus information processing in the outer retina are much more complex than previously expected. These fundamental findings will be very important for several fields of science, including vertebrate vision, avian magnetoreception, and comparative neuroanatomy.

双锥体是大多数鸟类视网膜中最常见的感光细胞类型，但它们的精确功能仍然是个谜。他们建议的功能包括亮度检测、偏振光检测和光依赖、基于自由基对的磁感应。为了更好地理解双锥体的功能，了解它们如何连接到鸟类视网膜中的神经网络至关重要。在这里，我们使用连续切片、多束扫描电子显微镜来研究双锥体解剖结构和连通性，特别关注它们与鸡视网膜中其他光感受器和双极细胞的接触。我们发现双锥体通过 telodendria 到终端和 telodendria 到 telodendria 接触与相邻的双锥体和其他感光细胞高度连接。我们还根据它们的轴突分层、光感受器接触模式、体细胞位置以及树突和轴突场马赛克确定了 15 种双极细胞类型。这 15 种双极细胞类型中的 13 种与双锥体的至少一个或两个成员接触。所有双极细胞都是双层或多层的。我们还发现了其他锥体类型之间以及杆和锥体之间的惊人接触。我们的数据表明鸟类视网膜外丛状层中的连接网络比最初预期的要复杂得多。我们还发现了其他锥体类型之间以及杆和锥体之间的惊人接触。我们的数据表明鸟类视网膜外丛状层中的连接网络比最初预期的要复杂得多。我们还发现了其他锥体类型之间以及杆和锥体之间的惊人接触。我们的数据表明鸟类视网膜外丛状层中的连接网络比最初预期的要复杂得多。

重要性声明与人类一样，视觉是鸟类最重要的感官之一。在这里，我们展示了来自任何鸟类视网膜的第一个连续切片多光束扫描电子显微镜数据集。我们确定了许多以前未描述的杆对锥和锥对锥的连接。令人惊讶的是，在我们确定的 15 种双极细胞类型中，11 种从杆状细胞接收输入，15 种中的 13 种至少从双锥体接收部分输入。因此，双锥体似乎在鸟类视网膜处理中扮演着许多不同且重要的角色，而外层视网膜的神经网络和信息处理比以前预期的要复杂得多。这些基本发现对几个科学领域都非常重要，包括脊椎动物视觉、鸟类磁感受和比较神经解剖学。