An S-cone circuit for edge detection in the primate retina

Abstract

Midget retinal ganglion cells (RGCs) are the most common RGC type in the primate retina. Their responses mediate both color and spatial vision, yet the specific links between midget RGC responses and visual perception are unclear. Previous research on the dual roles of midget RGCs has focused on those comparing long (L) vs. middle (M) wavelength sensitive cones. However, there is evidence for several other rare midget RGC subtypes receiving S-cone input, but their role in color and spatial vision is uncertain. Here, we confirm the existence of the single S-cone center OFF midget RGC circuit in the central retina of macaque monkey both structurally and functionally, by combining single cell electrophysiology with 3D electron microscopy reconstructions of the upstream circuitry. Like the well-studied L vs. M midget RGCs, the S-OFF midget RGCs have a centersurround receptive field consistent with a role in spatial vision. While spectral opponency in a primate RGC is classically assumed to contribute to hue perception, a role supporting edge detection is more consistent with the S-OFF midget RGC receptive field structure and studies of hue perception.

Reconciling Color Vision Models With Midget Ganglion Cell Receptive Fields

“…For example, a full-field stimulus (Lee et al, 1998) may have reduced S-cone responses by driving the antagonistic S-cone surround receptive field mediated by HII horizontal cell feedback (Dacey et al, 1996). Indeed, the Sun et al (2006) experiments did not detect S-OFF midget RGCs, despite a growing consensus that these neurons make up 5–10% of OFF midget RGCs in the macaque central retina (Klug et al, 2003; Field et al, 2010; Tsukamoto and Omi, 2015; Patterson et al, 2019). Taken together, these results further demonstrate the need to account for both the spatial and spectral dimensions of midget RGC receptive fields.…”

A Color Vision Circuit for Non-Image-Forming Vision in the Primate Retina

“…Reliable identification of upstream S-cone circuitry is essential for identifying a novel S-cone neuron, and thus, we began by reconstructing the established S-cone connectome, building on our previous reconstructions of S-cone bipolar cells in the outer retina [17]. Briefly, S-cones were distinguished from L/M-cones by their highly stereotyped post-synaptic contacts [18].…”

“…A block of inferior parafoveal retinal tissue at 1 mm eccentricity from the fovea center was processed as previously described [44]. A transmission electron microscopic image of a cross-section of the retina can be seen in Figure 1A of our previously published work [17]. Briefly, the eyecup was placed in 4% glutaraldehyde in 0.1M sodium cacodylate buffer pH 7.4 and while in this solution a 1 mm square of retina centered 1.5 mm inferior to the center of the fovea was cut out and then fixed overnight at 4 C. The tissue was next washed 5 3 5 min in 0.1M coacodylte buffer, then post fixed in osmium ferrocyanide for 1 h on ice.…”

“…Data analysis and 3D rendering were performed using SBFSEM-tools, an open-source MATLAB (Mathworks) program developed in the Neitz lab (https://github.com/neitzlab/sbfsem-tools) [17,49]. Final figures were compiled in Adobe Illustrator.…”

Wide‐field amacrine cell inputs to ON parasol ganglion cells in macaque retina

“…All procedures were approved by the Institutional Animal Care and Use Committee at the University of Washington. The anterior half of the eye and the vitreous humor were removed, and the eyecup was fixed and processed as previously described (Patterson, Kuchenbecker, et al, ). Briefly, the eyecup was fixed in 4% glutaraldehyde in 0.1M sodium cacodylate buffer pH 7.4 and, while in this solution, a 1 mm square of retina centered 2 mm temporal to the center of the fovea was cut out and then fixed overnight at 4°C.…”