Center for Visual Science, University of Rochester, Rochester, NY, United States of America.
Institute of Optics, University of Rochester, Rochester, NY, United States of America.
PLoS One. 2022 Nov 29;17(11):e0278261. doi: 10.1371/journal.pone.0278261. eCollection 2022.
The primate fovea is specialized for high acuity chromatic vision, with the highest density of cone photoreceptors and a disproportionately large representation in visual cortex. The unique visual properties conferred by the fovea are conveyed to the brain by retinal ganglion cells, the somas of which lie at the margin of the foveal pit. Microelectrode recordings of these centermost retinal ganglion cells have been challenging due to the fragility of the fovea in the excised retina. Here we overcome this challenge by combining high resolution fluorescence adaptive optics ophthalmoscopy with calcium imaging to optically record functional responses of foveal retinal ganglion cells in the living eye. We use this approach to study the chromatic responses and spatial transfer functions of retinal ganglion cells using spatially uniform fields modulated in different directions in color space and monochromatic drifting gratings. We recorded from over 350 cells across three Macaca fascicularis primates over a time period of weeks to months. We find that the majority of the L vs. M cone opponent cells serving the most central foveolar cones have spatial transfer functions that peak at high spatial frequencies (20-40 c/deg), reflecting strong surround inhibition that sacrifices sensitivity at low spatial frequencies but preserves the transmission of fine detail in the retinal image. In addition, we fit to the drifting grating data a detailed model of how ganglion cell responses draw on the cone mosaic to derive receptive field properties of L vs. M cone opponent cells at the very center of the foveola. The fits are consistent with the hypothesis that foveal midget ganglion cells are specialized to preserve information at the resolution of the cone mosaic. By characterizing the functional properties of retinal ganglion cells in vivo through adaptive optics, we characterize the response characteristics of these cells in situ.
灵长类动物的中央凹是专门用于高分辨率色觉的，这里拥有最高密度的视锥细胞和不成比例大的视皮层代表区。中央凹赋予的独特视觉属性是通过视网膜神经节细胞传递到大脑的，这些细胞的体位于中央凹坑的边缘。由于在切除的视网膜中中央凹非常脆弱，因此对这些最中心的视网膜神经节细胞进行微电极记录一直具有挑战性。在这里，我们通过结合高分辨率荧光自适应光学眼底镜和钙成像，克服了这一挑战，从而可以在活体眼中对中央凹视网膜神经节细胞的功能反应进行光学记录。我们使用这种方法来研究色觉反应和视网膜神经节细胞的空间传递函数，使用在颜色空间中以不同方向调制的空间均匀场和单色漂移光栅。我们在三只猕猴身上进行了超过 350 个细胞的记录，时间跨度为数周至数月。我们发现，为最中心的中央凹锥提供服务的大多数 L 与 M 锥对立细胞具有空间传递函数，其峰值出现在高空间频率（20-40 c/deg），反映出强烈的环绕抑制，牺牲了低空间频率的灵敏度，但保留了视网膜图像中的精细细节传输。此外，我们根据漂移光栅数据拟合了一个详细的模型，说明了神经节细胞的反应如何利用锥状细胞镶嵌来推导中央凹非常中心的 L 与 M 锥对立细胞的感受野特性。这些拟合结果与中央凹小型神经节细胞专门用于保留与锥状细胞镶嵌分辨率相同的信息的假设一致。通过自适应光学对活体视网膜神经节细胞的功能特性进行特征描述，我们对这些细胞在原位的反应特征进行了特征描述。
