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

Sara S Patterson,James A Kuchenbecker,James R Anderson,Maureen Neitz,Andrea S Bordt,David W Marshak,Jay Neitz

doi:10.1038/s41598-019-48042-2

Sara S Patterson, James A Kuchenbecker + Show 5 more

Open Access

https://doi.org/10.1038/s41598-019-48042-2

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Abstract

Midget retinal ganglion cells (RGCs) are the most common RGC type in the primate retina. Their responses have been proposed to 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. We investigated the receptive field properties of the S-OFF midget circuit with single cell electrophysiology and 3D electron microscopy reconstructions of the upstream circuitry. Like the well-studied L vs. M midget RGCs, the S-OFF midget RGCs have a center-surround 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.

Highlights

Anatomical evidence for S-OFF midget retinal ganglion cells (RGCs) is seen in the macaque (Old World) monkeys[1,2,3,4], but not in New World monkeys[6,7]
We find that every cone in the central retina provides the sole input to an OFF midget bipolar cell
The pure S-cone midget RGC centers are not observed in the peripheral retina

Summary

Introduction

Anatomical evidence for S-OFF midget RGCs is seen in the macaque (Old World) monkeys[1,2,3,4], (but see Kolb et al.5) but not in New World monkeys[6,7]. The existence and function of S-OFF midget RGCs is relevant to a major unsolved question: how and where color and spatial information are separated in the visual pathway. Each L- and M-cone provides the sole direct input to an ON and OFF midget circuit, forming a “private line” pathway from single cones to the parvocellular lateral geniculate nucleus (LGN)[24]. Their center-surround receptive fields perform a simple computation: comparing a single L- or M-cone center to neighboring L/M-cones in the surround. The goal of this work is to confirm the existence of S-OFF midget RGCs but understand the details of their circuity and receptive field properties so they can be fit into a larger understanding of the role of midget RGCs in color and spatial vision

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