Physiology and Morphology of Color-Opponent Ganglion Cells in a Retina Expressing a Dual Gradient of S and M Opsins

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 (similar to 2.1 X 10(4) mu m(2)) to collect similar to 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.