In vivo chromatic and spatial tuning of foveolar retinal ganglion cells in Macaca fascicularis

Abstract

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.

Cone-Opponent Ganglion Cells in the Primate Fovea Tuned to Non-Cardinal Color Directions

“…During a larger study on spatial frequency tuning of L vs. M foveal midget RGCs, we identified candidate L vs. M+S and M vs. L+S neurons with cone-isolating, isoluminant and achromatic stimuli modulated sinusoidally in time (Godat et al, 2022). Here, we performed a focused investigation of these neurons, incorporating new data ( Fig.…”

“…Could the neurons identified with L vs. M ± S opponency reflect the responses of two overlapping neurons, one with L vs. M opponency and one with S-cone input? Here we manually segmented only cells that were laterally well-isolated across all imaging sessions, as previously described (Godat et al, 2022). Any out-of-focus cell eluding detection during segmentation would be very dim and expected to contribute weakly to a segmented cell’s response.…”

“…All animals were in the care of the Department of Comparative Medicine veterinary staff of the University of Rochester’s Medical Center, including several full-time veterinarians, veterinary technicians, and an animal care staff who monitored animal health. Additional details on the vivarium environment are detailed in our previous work (McGregor et al, 2020; Godat et al, 2022). This study was carried out in strict accordance with the Association for Research in Vision and Ophthalmology (ARVO) Statement for the Use of Animals and the recommendations in the Guide for the Care and Use of Laboratory Animals from the National Institutes of Health.…”

“…Imaging Preparation. Anesthesia and animal preparation procedures have been previously published (McGregor et al, 2020; Godat et al, 2022) and are briefly summarized here. All anesthesia and preparation followed established lab protocols and was performed by a veterinary technician licensed by the State of New York (USA).…”

“…A control stimulus was also presented without modulation around the mean, which had the approximate chromaticity coordinates of (0.33, 0.33). Stimuli were calculated using the Psychophysics Toolbox (Brainard, 1997; RRID: SCR_-002881) and calibrated as previously described (Godat et al, 2022). Within an imaging session, each stimulus was presented three times.…”