excitation and inhibition cancel (7). Although this spectral opponency has been studied for more than 30 years, the underlying retinal circuitry remains unclear.

Wiesel and Hubel (8) were the first to suggest a simple circuitry by which color opponency could arise in macaque ganglion cells. Recording from the the lateral geniculate nucleus (LGN), the target of color-responsive ganglion cells, they reported that inputs from the different cone types appeared to be segregated to the center and the surround of the classical receptive field. Color opponency thus could arise by piggy-backing on the antagonistic center–surround organization found in many ganglion cells. For example, a red-ON/ green-OFF opponent cell would receive excitatory L-cone input to the receptive-field center and inhibitory M-cone input to the receptive-field surround. A consequence of this combined spatial and cone opponency is that this type of cell could signal achromatic luminance variation, due to center–surround spatial antagonism, and also signal chromatic change that engaged both the excitatory and inhibitory cone pathways (9). This type of spatially and chromatically opponent receptive field was labeled “Type 1” (Fig. 1).

Wiesel and Hubel (8) described a second, Type 2, opponent cell class, which also appeared to receive excitatory and inhibitory input from different cone types, but which lacked a clear center–surround organization. Instead, opposing cone inputs were distributed in spatially coextensive ON and OFF responding fields (Fig. 1). As recognized by Hubel and Wiesel and others to follow, this Type 2 receptive-field organization suggested a specialization for color coding independent of any role in spatial vision.

FIG. 1. Classical cone-type-specific circuitry (labeled-line model) for color opponency in ganglion cells. In the Type 1 receptive field, inputs from different cone types (L- and M-cones in this example) are segregated to the center vs. the surround of the receptive field. Type 1 cells show a center–surround antagonism to luminance changes and a spatially uniform response to full-field, equiluminant color changes (in this case an excitatory response to a shift to a longer wavelength). In Type 2 cells, opposing inputs (S-cones vs. L- and M-cones) form two spatially coextensive fields and thus lack the center–surround antagonism to luminance changes.

Clearly, although they both display opponency, Type 1 and Type 2 cells must be linked somewhat differently to cones and interneurons. In Type 1 cells, the cone inputs must be segregated spatially, while in Type 2 cells, the cone inputs are coextensive but opposite in sign. Nonetheless, the cornerstone for the circuitries of both Type 1 and Type 2 cells is the existence of labeled lines, that is, the anatomical segregation of the different cone signals from the receptors through the connecting interneurons to the ganglion cell. This labeled line model predicts a retinal circuitry that can sort out the L-and M-cone signals and deliver them with the appropriate sign to the appropriate part of the receptive field.

Identifying the Color Opponent Ganglion Cell Types

To explore the labeled line model and determine the retinal circuitry giving rise to red–green and blue–yellow opponency in ganglion cells, the ganglion cell types that transmit these signals must first be identified. In an early attempt, DeMonasterio (10), using intracellular recording and staining methods, tentatively suggested that a morphologically identified group of ganglion cells with large cell bodies, called parasol cells, were the blue-ON/yellow-OFF opponent cells and that cells with small cell bodies and small dendritic trees, called midget ganglion cells, probably transmitted red–green opponent signals. Parasol cells have since been shown to project exclusively to the magnocellular LGN layers where achromatic, nonopponent cells are recorded and so play no part in color coding. However, midget ganglion cells provide the major input to the the parvocellular layers of the LGN where both red–green and blue–yellow opponent cells are found (11,12). Thus, the midget ganglion cells came to be associated with the overall group of color opponent cells despite significant differences in the receptive-field properties of the red–green and blue–yellow opponent ganglion cells (13,14). A more direct link between anatomy and physiology requires the direct correlation of an identified ganglion cell type with a color opponent receptive field.

Studying Color Circuitry with an in Vitro Preparation. Recently developed techniques have enabled breakthroughs in linking structure to function in the retina. In pioneering studies of rabbit retina by Masland and Vaney and their colleagues (15,16), an isolated retina was maintained in vitro, and fluorescent markers were used to identify cell types under the light microscope. Targeted cells could then be intracellularly filled with dyes to reveal the cell's dendritic morphology. This in vitro approach was later applied to macaque retina (17,18) and eventually extended to combined anatomical and physiological experiments (1922). The key to the success of this preparation is that neuronal light responses can be recorded from cell types that have been visually identified.

In macaque, the L-, M-, and S-cone spectral sensitivities are known, so the method of silent substitution can be used to identify cone inputs to a cell. With this method, two lights of differing spectral composition are alternated and their relative radiances adjusted so that the alternation between the pair of lights will give rise to a modulated response in one but not the other (the silent) cone type (2325). We have now used this approach in macaque retina in vitro to explore circuits that underlie opponency.

Circuitry for Blue–Yellow Opponency and the Role of the Small Bistratified Cell. The first cell type studied with this approach was the small bistratified ganglion cell, one of a number of ganglion cell types that, in addition to the midget ganglion cell, projects to the parvocellular geniculate layers (26,27). The cell's distinctive dendritic tree stratifies in two separate sublayers within the inner plexiform layer (Fig. 2). The innermost tier of dendrites costratifies with the axon terminals of a cone bipolar cell type that makes exclusive



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