Horizontal Cell Feedback without Cone Type-Selective Inhibition Mediates “Red–Green” Color Opponency in Midget Ganglion Cells of the Primate Retina

Abstract

The distinctive red-green dimension of human and nonhuman primate color perception arose relatively recently in the primate lineage with the appearance of separate long (L) and middle (M) wavelength-sensitive cone photoreceptor types. "Midget" ganglion cells of the retina use center-surround receptive field structure to combine L and M cone signals antagonistically and thereby establish a "redgreen, color-opponent" visual pathway. However, the synaptic origin of red-green opponency is unknown, and conflicting evidence for either random or L versus M cone-selective inhibitory circuits has divergent implications for the developmental and evolutionary origins of trichromatic color vision. Here we directly measure the synaptic conductances evoked by selective L or M cone stimulation in the midget ganglion cell dendritic tree and show that L versus M cone opponency arises presynaptic to the midget cell and is transmitted entirely by modulation of an excitatory conductance. L and M cone synaptic inhibition is feedforward and thus occurs in phase with excitation for both cone types. Block of GABAergic and glycinergic receptors does not attenuate or modify L versus M cone antagonism, discounting both presynaptic and postsynaptic inhibition as sources of cone opponency. In sharp contrast, enrichment of retinal pHbuffering capacity, to attenuate negative feedback from horizontal cells that sum L and M cone inputs linearly and without selectivity, completely abolished both the midget cell surround and all chromatic opponency. Thus, red-green opponency appears to arise via outer retinal horizontal cell feedback that is not cone type selective without recourse to any inner retinal L versus M cone inhibitory pathways.

Systematic biases in adult color perception persist despite lifelong information sufficient to calibrate them

“…The retinal mosaic of cones is largely random and slightly clumped, and the wiring of L and M cones into the opponent surrounds of the parvocellular pathway is largely unspecific (see Crook, Manookin, Packer, & Dacey, 2011, for the most recent evidence). Furthermore, V1 cells vary widely in the relative contribution from parvo-and koniocellular chromatic pathways (i.e., ''red-green''' and ''blue-yellow'') (De Valois, Cottaris, Elfar, Mahon, & Wilson, 2000;Landisman & Ts'o, 2002;Mullen, Dumoulin, McMahon, de Zubicaray, & Hess, 2007).…”

“…This might have been a factor in the computer experiments, which had lower overall luminance than the natural ones. Secondly, as the number of cones projecting to each midget ganglion cell increases, the proportions of L and M cones contributing to the center and surrounds may equalize (Crook et al, 2011;Diller et al, 2004;Lennie, Haake, & Williams, 1991;Mullen, Sakurai, & Chu, 2005;Paulus & Kroger-Paulus, 1983;Solomon et al, 2005), which would also decrease the chromatic signal and thus might decrease saturation. Although midget ganglion cells may maintain their single-cone center up to about 108, larger surrounds could potentially have an impact within this region.…”

Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

“…Surrounds can be generated by horizontal cells in the outer retina [17,18,19,20,21] and amacrine cells in the inner retina [22,23,24,25,26] (Fig. 1a).…”

Towards a Generic Simulation Tool of Retina Models

“…These retina models simulate chromatic opponency, blue-yellow and red-green, and contrast adaptation mechanisms in the retina. The chromatic models we propose provide a neural basis for the retina architectures suggested by different authors [39][40][41]. The simulation tool was configured to reproduce both theories of the red-green pathway (the cone-type selective surround [40,42,43] and the randomwiring or mixed surround [41,44]) and the spatially coextensive receptive field of the blue-yellow pathway [39].…”

“…were inspired by the retina structures suggested by different authors [39][40][41]. We would like to remark that authors of these chromatic experiments used simple mathematical models, based on difference of Gaussian functions that depend on spatial frequency, to fit the physiological recordings.…”