Dataset Information

Physiology and morphology of color-opponent ganglion cells in a retina expressing a dual gradient of S and M opsins.

ABSTRACT: Most mammals are dichromats, having short-wavelength-sensitive (S) and middle-wavelength-sensitive (M) cones. Smaller terrestrial species commonly express a dual gradient in opsins, with M opsin concentrated superiorly and declining inferiorly, and vice-versa for S opsin. Some ganglion cells in these retinas combine S- and M-cone inputs antagonistically, but no direct evidence links this physiological opponency with morphology; nor is it known whether opponency varies with the opsin gradients. By recording from >3000 ganglion cells in guinea pig, we identified small numbers of color-opponent cells. Chromatic properties were characterized by responses to monochromatic spots and/or spots produced by mixtures of two primary lights. Superior retina contained cells with strong S+/M- and M+/S- opponency, whereas inferior retina contained cells with weak opponency. In superior retina, the opponent cells had well-balanced M and S weights, while in inferior retina the weights were unbalanced, with the M weights being much weaker. The M and S components of opponent cell receptive fields had approximately the same diameter. Opponent cells injected with Lucifer yellow restricted their dendrites to the ON stratum of the inner plexiform layer and provided sufficient membrane area (approximately 2.1 x 10(4) microm(2)) to collect approximately 3.9 x 10(3) bipolar synapses. Two bistratified cells studied were nonopponent. The apparent decline in S/M opponency from superior to inferior retina is consistent with the dual gradient and a model where photoreceptor signals in both superior and inferior retina are processed by the same postreceptoral circuitry.

SUBMITTER: Yin L

PROVIDER: S-EPMC2677103 | biostudies-literature | 2009 Mar

REPOSITORIES: biostudies-literature

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Publications

Physiology and morphology of color-opponent ganglion cells in a retina expressing a dual gradient of S and M opsins.

Yin Lu L Smith Robert G RG Sterling Peter P Brainard David H DH

The Journal of neuroscience : the official journal of the Society for Neuroscience 20090301 9

Most mammals are dichromats, having short-wavelength-sensitive (S) and middle-wavelength-sensitive (M) cones. Smaller terrestrial species commonly express a dual gradient in opsins, with M opsin concentrated superiorly and declining inferiorly, and vice-versa for S opsin. Some ganglion cells in these retinas combine S- and M-cone inputs antagonistically, but no direct evidence links this physiological opponency with morphology; nor is it known whether opponency varies with the opsin gradients. B ...[more]

PMID: 19261865

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Project description: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 showed 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 not been explored. 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 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 the 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 versus M and S versus L+M cardinal mechanisms.SIGNIFICANCE STATEMENT The 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 versus M or "red-green") and small bistratified (S vs L+M, or "blue-yellow") ganglion cell pathways 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 and show physiologically that a subpopulation of S-OFF midget cells combine S, L, and M cone inputs along noncardinal directions of color space, expanding the retinal role in color coding.

Dataset Information

Physiology and morphology of color-opponent ganglion cells in a retina expressing a dual gradient of S and M opsins.

Publications

Physiology and morphology of color-opponent ganglion cells in a retina expressing a dual gradient of S and M opsins.

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