Evidence That Each S Cone in Macaque Fovea Drives One Narrow-Field and Several Wide-Field Blue-Yellow Ganglion Cells

Abstract

A rule of retinal wiring is that many receptors converge onto fewer bipolar cells and still fewer ganglion cells. However, for each S cone in macaque fovea, there are two S-cone ON bipolar cells and two blue-yellow (BY) ganglion cells. To understand this apparent rule reversal, we reconstructed synaptic patterns of divergence and convergence and determined the basic three-tiered unit of connectivity that repeats across the retina. Each foveal S cone diverges to four S-cone ON bipolar cells but contacts them unequally, providing 1-16 ribbon synapses per cell. Next, each bipolar cell diverges to two BY ganglion cells and also contacts them unequally, providing ϳ14 and ϳ28 ribbon synapses per cell. Overall, each S cone diverges to approximately six BY ganglion cells, dominating one and contributing more modestly to the others. Conversely, of each pair of BY ganglion cells, one is dominated by a single S cone and one is diffusely driven by several. This repeating circuit extracts blue/yellow information on two different spatiotemporal scales and thus parallels the circuits for achromatic, spatial vision, in which each cone dominates one narrow-field ganglion cell (midget) and contributes some input to several wider-field ganglion cells (parasol). Finally, because BY ganglion cells have coextensive ϩS and Ϫ(LϩM) receptive fields, and each S cone contributes different weights to different BY ganglion cells, the coextensive receptive fields must be already present in the synaptic terminal of the S cone. The S-cone terminal thus constitutes the first critical locus for BY color vision.

The Primordial, Blue-Cone Color System of the Mouse Retina

“…Second, individual blue-cone bipolar cells contact between one and five S-cone pedicles (convergence), whereas S-cone pedicles are contacted by the dendrites of one to five blue-cone bipolar cells (divergence). Third, the density ratio of blue-cone bipolar cells to blue cones is between one and two in the primate Marshak, 1992, 1997;Wässle et al, 1994;Schein et al, 2004) and 1.17 in the mouse retina (Fig. 3).…”

Spatial Properties and Functional Organization of Small Bistratified Ganglion Cells in Primate Retina

“…bipolar cell signals. Instead, the data suggested that horizontal cells provide the (LϩM)-OFF surround (Dacey, 2000;Herr et al, 2003;Schein et al, 2004). The receptive fields of SBCs formed nonrandom mosaics with overlap and regularity similar to those of ON-parasol cells.…”

“…These results indicate that OFF-bipolar cells provide little if any functional input to SBCs in the present conditions. In the discussion, it is proposed that SBCs receive dominant LϩM cone input via H2 horizontal cell feedback (Dacey, 2000;Herr et al, 2003;Schein et al, 2004).…”

Biocytin wide‐field bipolar cells in rabbit retina selectively contact blue cones

“…In primates and mice, the density ratio of blue cone bipolar cells to blue cones is approximately 1:2 and each blue cone is contacted by more than one blue cone bipolar cell (Kouyama and Marshak, 1992;Kouyama and Marshak, 1997;Schein et al, 2004;Haverkamp et al, 2005). In rabbits, the divergence of blue cone input onto each wide-field bipolar cell depends on retinal eccentricity.…”