In vivo calcium imaging reveals L/M opponent ganglion cells consistent with single cone receptive field centers at the macaque foveal center

Abstract

Purpose : The fovea is specialized for high spatial resolution and color vision, but there is a paucity of recordings that elucidate how retinal ganglion cells (RGCs) at the very center of the fovea facilitate this specialization. Here, we optically record responses to spatial and chromatic stimuli using a calcium indicator in the living eye to characterize the receptive field (RF) properties of RGCs serving the foveal center.

Methods : The calcium indicator GCaMP6s was expressed in the ganglion cell layer of a female macaque. Adaptive optics scanning light ophthalmoscopy (AOSLO) was used to image fluorescence (488nm ex., 520/35nm em.) from RGCs whose RF centers were driven by cones in the central 6 arcmin of the fovea. By recording responses to cone isolating and luminance flicker (1.3deg, 0.15Hz, LED 420nm, 530nm, 660nm), we derived cone weights in 34 RGCs. By recording responses to drifting gratings (1.9deg, 6Hz, 4-50c/deg, 561nm), we derived the spatial frequency responses of 15 L/M chromatic opponent RGCs. Employing computational modeling (ISETbio toolbox, isetbio.org) that accounted for residual blur in the instrument, the eye’s optics, cone aperture, and the spacing of individual cones, we inferred the number of cones feeding into RF centers and surrounds.

Results : Of the 34 RGCs, 44% exhibited L/M chromatic opponency, 15% were L+M ON, 6% were -L-M OFF, while the remaining 35% showed only L or only M responses. The spatial frequency response functions of 12/15 L/M opponent cells peaked at high spatial frequencies (25-40c/deg) and had a strong bandpass characteristic. Our model indicates that the responses of at least 9/15 L/M opponent cells are consistent with single cone input to their RF centers [Fig 1].

Conclusions : Using AOSLO to image calcium-mediated responses allows the study of the cone inputs to and spatial frequency responses of the very centermost foveal RGCs in the living primate eye. Our model establishes a framework for estimating sources of optical and neural information loss. The high spatial frequency tuning and single cone inputs we observed in L/M opponent cells emphasize the foveal specialization for spatial and chromatic vision by preserving information at the resolution of the photoreceptor mosaic.

This abstract was presented at the 2022 ARVO Annual Meeting, held in Denver, CO, May 1-4, 2022, and virtually.

 

L/M opponent cells consistent with single cone centers showing fitted data (top row) and RF models (bottom row).