Representation of color in the human retina

Abstract

Preceding the development of modern biological techniques, psychophysical experimentation and careful reasoning alone yielded an accurate account of human color perception predicated upon three opponent processes: blue versus yellow, red versus green and white versus black (Hurvich and Jameson, 1957). That is, when one of the opponent pairs, say blue, is perceived the other, yellow, is necessarily absent. The discovery, nearly five decades ago, by De Valois, Abramov and Jacobs of neurons early in the visual pathway with spectral characteristics similar to the theorized opponent interactions provided a plausible neurobiological substrate for hue perception (De Valois et al., 1966). In the decades since De Valois and colleagues published their seminal findings (De Valois et al., 1966), discrepancies between the properties of the lateral geniculate nucleus (LGN) cells reported and behavioral evidence have weakened the interpretation that these early visual cells directly map to human color perception (Stockman and Brainard, 2010). In particular, the contribution of S-cones to each opponent system has continued to be the subject of considerable experimental attention (Neitz and Neitz, 2011; Solomon and Lennie, 2007). On the basis of these discrepancies, De Valois and De Valois proposed a cortical transformation of LGN signals amounting to a rotation of the color axes (De Valois and De Valois, 1993). In light of evolutionary constraints and evidence from the genetic introduction of a third class of cones to a dichromatic retina (Mancuso et al., 2009), a simplied version of the De Valois model has been proposed (Neitz and Neitz, 2011; Mancuso et al., 2010; Schmidt et al., 2014). This model posits that the spectral opponency necessary to account for hue perception is already present in a subset of midget ganglion cells. Early reports from de Monasterio et al. (1975; 1978) described such retinal cells, with more recent support from a large sample of LGN neurons taken by Tailby et al. (2008). The goal of the research presented here was to directly test the hypothesis that hue perception is mediated by a small subset of midget ganglion cells that receive S-cone input via H2 horizontal cells.