Chromatic Properties of Horizontal and Ganglion Cell Responses Follow a Dual Gradient in Cone Opsin Expression

Abstract

In guinea pig retina, immunostaining reveals a dual gradient of opsins: cones expressing opsin sensitive to medium wavelengths (M) predominate in the upper retina, whereas cones expressing opsin sensitive to shorter wavelengths (S) predominate in the lower retina. Whether these gradients correspond to functional gradients in postreceptoral neurons is essentially unknown. Using monochromatic flashes, we measured the relative weights with which M, S, and rod signals contribute to horizontal cell responses. For a background that produced 4.76 log 10 photoisomerizations per rod per second (Rh*/rod/s), mean weights in superior retina were 52% (M), 2% (S), and 46% (rod). Mean weights in inferior retina were 9% (M), 50% (S), and 41% (rod). In superior retina, cone opsin weights agreed quantitatively with relative pigment density estimates from immunostaining. In inferior retina, cone opsin weights agreed qualitatively with relative pigment density estimates, but quantitative comparison was impossible because individual cones coexpress both opsins to varying and unquantifiable degrees. We further characterized the functional gradients in horizontal and brisk-transient ganglion cells using flickering stimuli produced by various mixtures of blue and green primary lights. Cone weights for both cell types resembled those obtained for horizontal cells using monochromatic flashes. Because the brisk-transient ganglion cell is thought to mediate behavioral detection of luminance contrast, our results are consistent with the hypothesis that the dual gradient of cone opsins assists achromatic contrast detection against different spectral backgrounds. In our preparation, rod responses did not completely saturate, even at background light levels typical of outdoor sunlight (5.14 log 10 Rh*/rod/s).

Chromatic Bipolar Cell Pathways in the Mouse Retina

“…Opsin coexpression gradients have been found in several mammalian species, including mouse, rabbit, and guinea pig (Juliusson et al, 1994;Röhlich et al, 1994). The effect of the gradient on horizontal and ganglion cell responses has been studied in guinea pig (Yin et al, 2006(Yin et al, , 2009, where the local opsin coexpression ratio was found to relate to the chromatic tuning of the neurons-similar to our observations in mouse BCs. Yin et al (2009) found color-opponent GCs across the whole retina, with ventrally recorded cells showing reduced opponency.…”

“…Yin et al (2009) found color-opponent GCs across the whole retina, with ventrally recorded cells showing reduced opponency. Regional opsin coexpression may, however, offer functional advantages [e.g., to enhance contrast detection against different spectral backgrounds (i.e., blue sky vs greenish-brownish ground) (Yin et al, 2006)]. …”

A Mammalian Retinal Ganglion Cell Implements a Neuronal Computation That Maximizes the SNR of Its Postsynaptic Currents

“…The intensity of the rectangular area, which served as the background to a flashing spot, was equivalent to 27 nW mm Ϫ2 on the retina, which, due to the overlap of stimulus and photoreceptor spectra, caused the following isomerization rates (R*): 7 ϫ 10 4 R* s Ϫ1 in a rod, 2 ϫ 10 4 R* s Ϫ1 in an M cone, and 3 ϫ 10 2 R* s Ϫ1 in an S cone ( rod max ϭ 500 nm, cone max ϭ 529 nm; rod outer segment, 16.2 ϫ 3 m 2 ; cone outer segment, 8 ϫ 3 m 2 ; Yin et al, 2006). At these photoisomerization rates, the OFF delta cell has noncolor opponent responses that are approximately equally divided between rods and M cone signals (Yin et al, 2006). Also at these photoisomerization rates, rod signals enter ganglion cells predominantly via cones and cone bipolar cells (Manookin et al, 2008).…”

Cellular Basis for Contrast Gain Control over the Receptive Field Center of Mammalian Retinal Ganglion Cells

“…The primary stimulus was a 0.5-mm-diameter spot, centered on the cell body. The spot intensity was drawn from a Gaussian distribution with a mean equal to the mean luminance of the monitor: 10 3 -10 4 photoisomerizations per middle-wavelength-sensitive cone or rod per second, which is within the mesopic range (Yin et al, 2006). The SD of the Gaussian was either 0.1 or 0.3 times the mean luminance, for low and high contrast, respectively.…”