S-cone inputs to midget retinal ganglion cells and their implications for color vision

Abstract

Purpose : There is evidence for S-cone OFF midget retinal ganglion cells (RGCs) in the Old World (OW) primate retina. These provide an unique opportunity to link retinal circuitry to color vision. We have combined results from serial electron microscopy (EM) and single cell electrophysiology with human psychophysics with the goal of establishing the role of S-cone inputs to midget RGCs in vision.

Methods : Conflicting evidence for S-OFF midget RGCs may be due to differences in species, retinal eccentricity and methodology, thus we sought both anatomical and physiological confirmation in macaque central retina. We used serial EM to reconstruct the circuitry at 8 S-cones and 6 neighboring L/M-cones (Fig 1). S-cone identity was confirmed by S-ON bipolar cell (BC; n=14) and HII horizontal cell (HC; n=8) contacts, as well as input to small bistratified RGCs (n=2). For comparison, we also traced HI HCs and L/M-midget BCs. We recorded from central midget RGCs in an in vitro flat mount preparation. Cone inputs were measured with cone-isolating spots and spatiotemporal receptive fields mapped with expanding spots (Fig 2) and Gaussian noise.

Results : Each S-cone provided the sole input to an OFF BC with >20 basal synapses, which contacted a single OFF RGC with 39.3±0.49 (n=6) ribbon synapses. We recorded spike responses from 3 S-OFF midget RGCs. Their small center-surround receptive fields distinguished these cells from melanopsin RGCs, the other known primate S-OFF RGC (Fig 2). HII HCs densely innervated S-cones but also made sparse L/M-cone contacts. We also confirm the presence of feed-forward synapses from HII HCs onto S-ON BC dendrites.

Conclusions : Our work highlights features unique to the OW primate retina that enable S-cone inputs to the midget pathway and may have evolved to support color vision. We provide both anatomical and physiological evidence that midget RGCs with single S-cone centers exist in primate retina. However, in separate psychophysical experiments, we show that stimuli designed to produce strong S-cone decrements and excite S-cone OFF midgets do not produce hue percepts. This is consistent with the hypothesis that the visual system does not extract all available chromatic information from the retina, but instead uses parallel midget RGC pathways for hue perception and detection of chromatic boundaries.

This is an abstract that was submitted for the 2018 ARVO Annual Meeting, held in Honolulu, Hawaii, April 29 - May 3, 2018.

 

Each S-cone terminal contacts an OFF midget BC

 

Curves are fits to a Difference of Gaussians model