Contrast gain control in the primate retina: P cells are not X-like, some M cells are

Abstract

Primate retinal ganglion cells that project to the magnocellular layers of the lateral geniculate nucleus (M) are much more sensitive to luminance contrast than those ganglion cells projecting to the parvocellular layers (P). We now report that increasing contrast modifies the temporal-frequency response of M cells, but not of P cells. With rising contrast, the M cells' responses to sinusoidal stimuli show an increasing attenuation at low temporal frequencies while the P cells' responses scale uniformly. The characteristic features of M-cell dynamics are well described by a model originally developed for the X and Y cells of the cat, where the hypothesized nonlinear feedback mechanism responsible for this behavior has been termed the contrast gain control (Shapley & Victor, 1978Victor, 1987Victor, , 1988. These data provide further physiological evidence that the M-cell pathway differs from the P-cell pathway with regard to the functional elements in the retina. Furthermore, the similarity in dynamics between primate M cells and cat X and Y retinal ganglion cells suggests the possibility that P cells, being different from either group, are a primate specialization not found in the retinae of lower mammals.

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

“…This might seem surprising in light of the correlation between mammalian ganglion cell types that show strong gain control and those that receive a large degree of amacrine cell input (Shapley and Victor, 1978;Freed and Sterling, 1988;Benardete et al, 1992;Kolb and Nelson, 1993;Weber and Stanford, 1994;Jacoby et al, 1996Jacoby et al, , 2000. Our results are consistent, however, with studies in salamander, which showed that gain control in ganglion cells can be explained primarily by gain control in presynaptic bipolar cells (Kim and Rieke, 2001;Rieke, 2001).…”

“…For example, primate midget (parvocellularpathway) ganglion cells lack gain control, and this is presumably explained not by their lack of specialized amacrine cell input, but rather by a lack of gain control in their presynaptic midget bipolar cell inputs (Benardete et al, 1992). Parasol (magnocellularpathway) ganglion cells show strong gain control, and this is presumably explained by gain control present in their presynaptic diffuse bipolar cell inputs (Jacoby et al, 1996(Jacoby et al, , 2000Benardete and Kaplan, 1999;Chander and Chichilnisky, 2001).…”

“…Y-type cells, and homologous cells in other species, show strong contrast gain control (Shapley and Victor, 1978;Benardete et al, 1992;Chander and Chichilnisky, 2001). For a given cell, we first recorded spiking responses with a patch electrode in the loose-patch configuration.…”

Identification and Characterization of a Y-Like Primate Retinal Ganglion Cell Type

“…Cells with similar visual response properties, the Y-cells, were first observed more than forty years ago in the cat retina (Enroth-Cugell and Robson, 1966). The original observation of the cat Y-cells was followed by a decades-long search for the counterpart of these cells both in the primate retina and in the primate lateral geniculate nucleus (LGN) (de Monasterio, 1978;Kaplan and Shapley, 1982;Derrington and Lennie, 1984;Blakemore and Vital-Durand, 1986;Benardete et al, 1992;Levitt et al, 2001;White et al, 2002). Until this report, no clear evidence had been found for a distinct type of Y-like retinal ganglion cell in the primate.…”

Metacontrast, target recovery, and the magno- and parvocellular systems: A reply to the perspective

“…Other major physiological differences reported between parvo-and magnocellular populations include contrast gain (Kaplan & Shapley, 1986;Croner & Kaplan, 1995) and contrast gain control (Benardete et al, 1992;Benardete & Kaplan, 1997. All these results were obtained for achromatic stimuli.…”