Neurosensorics/Animal Navigation, Institute for Biology and Environmental Sciences, Carl von Ossietzky University of Oldenburg, 26129 Oldenburg, Germany.
Research Center for Neurosensory Sciences, Carl von Ossietzky University of Oldenburg, 26129 Oldenburg, Germany.
J Neurosci. 2021 Jun 9;41(23):5015-5028. doi: 10.1523/JNEUROSCI.2495-20.2021. Epub 2021 Apr 23.
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. 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.
双锥形细胞是大多数鸟类视网膜中最常见的光感受器细胞类型，但它们的确切功能仍是一个谜。它们的建议功能包括亮度检测、偏振光检测以及光依赖的、基于自由基对的磁受体。为了更好地理解双锥形细胞的功能，了解它们与鸟类视网膜中的神经网络的连接方式将是至关重要的。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形细胞的解剖结构和连接方式，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，双锥形细胞通过 telodendria-to-terminal 和 telodendria-to-telodendria 接触与邻近的双锥形细胞以及其他光感受器细胞高度连接。我们还根据轴突分层、光感受器接触模式、体位置以及树突和轴突场镶嵌体，确定了 15 种双极细胞类型。这 15 种双极细胞类型中的 13 种至少与双锥形细胞的一个或两个成员接触。所有双极细胞均为双分层或多分层。我们还发现了其他锥体类型之间以及锥体与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的连接网络比最初预期的要复杂得多。与人类一样，视觉是鸟类最重要的感觉之一。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状细胞与锥状细胞以及锥状细胞与锥状细胞之间的连接。令人惊讶的是，在我们确定的 15 种双极细胞类型中，有 11 种接受来自杆状细胞的输入，而 15 种中的 13 种至少部分接受来自双锥形细胞的输入。因此，双锥形细胞似乎在鸟类视网膜处理中发挥着许多不同且重要的作用，外视网膜的神经网络因此信息处理比以前预期的要复杂得多。这些基本发现对于包括脊椎动物视觉、鸟类磁受体和比较神经解剖学在内的多个科学领域都非常重要。
