Zhao Arthur, Gruntman Eyal, Nern Aljoscha, Iyer Nirmala, Rogers Edward M, Koskela Sanna, Siwanowicz Igor, Dreher Marisa, Flynn Miriam A, Laughland Connor, Ludwig Henrique, Thomson Alexander, Moran Cullen, Gezahegn Bruck, Bock Davi D, Reiser Michael B
HHMI Janelia Research Campus, Ashburn, VA, USA.
Department of Neurological Sciences, University of Vermont, Burlington, VT, USA.
Nature. 2025 Jul 23. doi: 10.1038/s41586-025-09276-5.
Many animals use vision to navigate their environment. The pattern of changes that self-motion induces in the visual scene, referred to as optic flow, is first estimated in local patches by directionally selective neurons. However, how arrays of directionally selective neurons, each responsive to motion in a preferred direction at specific retinal positions, are organized to support robust decoding of optic flow by downstream circuits is unclear. Understanding this global organization requires mapping fine, local features of neurons across an animal's field of view. In Drosophila, the asymmetrical dendrites of the T4 and T5 directionally selective neurons establish their preferred direction, which makes it possible to predict directional tuning from anatomy. Here we show that the organization of the compound eye shapes the systematic variation in the preferred directions of directionally selective neurons across the entire visual field. To estimate the preferred directions across the visual field, we reconstructed hundreds of T4 neurons in an electron-microscopy volume of the full adult fly brain, and discovered unexpectedly stereotypical dendritic arborizations. We then used whole-head micro-computed-tomography scans to map the viewing directions of all compound eye facets, and found a non-uniform sampling of visual space that explains the spatial variation in preferred directions. Our findings show that the global organization of the directionally selective neurons' preferred directions is determined mainly by the fly's compound eye, revealing the intimate connections between eye structure, functional properties of neurons and locomotion control.
许多动物利用视觉在其环境中导航。自我运动在视觉场景中引起的变化模式，即光流，首先由方向选择性神经元在局部斑块中进行估计。然而，尚不清楚方向选择性神经元阵列（每个神经元在特定视网膜位置对偏好方向的运动做出反应）是如何组织起来，以支持下游回路对光流进行可靠解码的。要理解这种全局组织，需要绘制动物视野中神经元的精细局部特征。在果蝇中，T4和T5方向选择性神经元的不对称树突确定了它们的偏好方向，这使得从解剖结构预测方向调谐成为可能。在这里，我们表明复眼的组织塑造了整个视野中方向选择性神经元偏好方向的系统变化。为了估计整个视野的偏好方向，我们在成年果蝇全脑的电子显微镜体积中重建了数百个T4神经元，并意外地发现了 stereotypical 树突分支。然后，我们使用全脑微计算机断层扫描来绘制所有复眼小眼的观察方向，并发现了视觉空间的非均匀采样，这解释了偏好方向的空间变化。我们的研究结果表明，方向选择性神经元偏好方向的全局组织主要由果蝇的复眼决定，揭示了眼睛结构、神经元功能特性和运动控制之间的密切联系。
