Short-wavelength cone signals contribute to sparse, high-dimensional color tuning in primate OFF midget ganglion cells

Abstract

In the trichromatic primate retina, the midget retinal ganglion cell is the classical substrate for red-green color signaling, with a circuitry that enables antagonistic responses between long (L)- and medium (M)-wavelength sensitive cone inputs. Previous physiological studies show that some OFF midget ganglion cells may receive sparse input from short (S)-wavelength sensitive cones, but the effect of S-cone inputs on the chromatic tuning properties of such cells has been unexplored. Moreover, anatomical evidence for a synaptic pathway from S cones to OFF midget ganglion cells through OFF-midget bipolar cells remains ambiguous. In this study we address both questions for the macaque monkey retina. First, we used serial block-face electron microscopy (SBEM) to show that every S-cone in the parafoveal retina synapses principally with a single OFF-midget bipolar cell which in turn forms a private-line connection with an OFF midget ganglion cell. Second, we used patch electrophysiology to characterize the chromatic tuning of OFF midget ganglion cells in the near peripheral retina that receive combined input from L, M and S cones. These S-OFF midget cells have a characteristic S-cone spatial signature, but demonstrate heterogeneous color properties due to variable strength of L, M, and S cone input across the receptive field. Together these findings strongly support the hypothesis that the OFF midget pathway is the major conduit for S-OFF signals in primate retina, and redefines the pathway as a chromatically complex substrate that encodes color signals beyond the classically recognized L vs. M and S vs. L+M cardinal mechanisms.\n\nSignificance statementThe first step of color processing in the visual pathway of primates occurs when signals from short- (S), middle- (M) and long- (L) wavelength sensitive cone types interact antagonistically within the retinal circuitry to create color-opponent pathways. The midget (L vs. M or red-green) and small bistratified (S vs. L+M, or blue-yellow) appear to provide the physiological origin of the cardinal axes of human color vision. Here we confirm the presence of an additional S-OFF midget circuit in the macaque monkey fovea with scanning block-face electron microscopy (SBEM) and show physiologically that a subpopulation of S-OFF midget cells combine S, L and M cone inputs along non-cardinal directions of color space, expanding the retinal role in color coding.