Retinal Processing of Achromatic and Chromatic Signals in Guinea Pig Along the Dual Gradient in Cone Opsin Expression.

In guinea pig retina immunostaining revealed a dual gradient of opsins: cones expressing opsin sensitive to medium wavelengths (M) predominate in superior retina, whereas cones expressing opsin sensitive to shorter wavelengths (S) predominate in inferior retina (Rohlich et al., 1994). To learn whether these gradients correspond to functional gradients in post-receptoral neurons, we examined the visual processing along two retinal pathways. One is the achromatic pathway mediated by horizontal and brisk-transient ganglion cells, processing achromatic contrast. Another is the chromatic pathway mediated by S/M opponent ganglion cells, processing S/M opponent signal. Using monochromatic flashes, and also flickering stimuli produced by mixtures of blue and green primary lights, we measured the relative weights with which M, S, and rod signals contribute to the responses of a retinal neuron. We showed that both horizontal and brisk-transient ganglion cells preserved the dual gradient in their relative M/S weights. In superior retina, M/S weights agreed quantitatively with relative pigment density estimates from immunostaining. In inferior retina, M/S weights agreed qualitatively with relative pigment density estimates. We also showed that S/M opponency varied across retina consistent with the dual gradient. In superior retina, S/M opponent ganglion cells had well-balanced M and S weights. In inferior retina, S/M opponent ganglion cells had unbalanced M and S weights, with the M weights being much weaker. These suggested that S signal to S/M opponent ganglion cell in superior retina was selectively amplified, but M signal to S/M opponent ganglion cell in inferior retina was not. Results from both pathways support the hypothesis that the dual gradient is an adaptation to assist achromatic contrast detection against different spectral backgrounds (e.g., an approaching avian predator), and in doing so color vision in guinea pig inferior retina is sacrificed. We also made two additional findings. First, in our preparation rods contributed significantly to vision even at background intensities typically considered to be photopic. Second, both S+/M- and S-/M+ opponent ganglion cells co-stratified in the ON stratum of the inner plexiform layer, and are new ganglion cell types that differ from the bistratified blue-yellow ganglion cells in primates.