In vivo physiology of foveal retinal ganglion cells in Macaca fascicularis

The primate fovea is specialized for high-resolution spatial and chromatic vision, possessing a unique topography characterized by a pit in which the inner retina and associated vasculature have been excavated, the highest density of cones anywhere in the retina, and a disproportionately large representation in visual cortex. The crucial visual properties conferred by the fovea are mediated by retinal ganglion cells (RGCs) 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. This has been overcome in this study by combining high resolution fluorescence adaptive optics ophthalmoscopy with calcium imaging to optically record functional responses of foveal RGCs to visual stimuli in the living eye. Here we use this approach to study the chromatic responses of RGCs to uniform fields modulated in different directions in color space and achromatic responses with monochromatic drifting gratings. We repeated these recordings in many cells in each of three macaca fasicularis primates over weeks or months. We find that most of the L/M chromatically opponent cells serving the most central cones respond to high spatial frequencies, reflecting strong surround inhibition that sacrifices sensitivity at low frequencies in favor of the transmission of fine detail in the retinal image. In addition, we find the L/M cells vary in spatial frequency bandwidths, suggesting that L/M chromatic opponency, often considered largely due to input from single cones, has more diverse receptive field structure than previously thought. By characterizing the functional properties of retinal ganglion cells in vivo through adaptive optics, we provide a lower bound on the response characteristics of these cells in situ and their role in vision processing. ### Competing Interest Statement DRW and WHM receive funding from the National Eye Institute. DRW receives additional funding from the Arnold and Mabel Beckman Foundation, Alcon, and Warby Parker, and WHM receives funding from Research to Prevent Blindness. DHB receives funding from the National Institutes of Health, Johnson & Johnson, and Facebook Reality Labs. DRW has patents with the University of Rochester for adaptive optics imaging of the retina: US patent 6,199,986 "Rapid, automatic measurement of the eye's wave aberration". US patent 6,264,328 "Wavefront sensor with off-axis illumination"and US patent 6,338,559 "Apparatus and method for improving vision and retinal imaging". QY has patents with the University of Rochester, Canon Inc. and the University of Montana for image stabilization algorithms: US patent 9,226,656 "Real-time optical and digital image stabilization for adaptive optics scanning ophthalmoscopy", US patent 9,406,133 "System and method for real-time image registration", US patent 9,485,383 "Imaging based correction of distortion from a scanner" and US patent 9,454,084 "Light source modulation for a scanning microscope". DHB is an inventor on US patent 16/389,942. Additionally, QY has undertaken consultancy work for Oculus VR and Boston Micromachine Corporation.