Bipolar cells specific for blue cones in the macaque retina

Abstract

A distinct subpopulation of bipolar cells in macaque monkey retina was labeled with antisera that recognize glycine-extended cholecystokinin precursors. The labeled bipolar cells were found throughout the retina and had dendrites contacting a subpopulation of cone pedicles and axons ramifying in the fifth stratum of the inner plexiform layer. Several lines of evidence indicate that the labeled bipolar cells are a single type despite some variations in their morphology. First, the density of perikarya and their diameters varied continuously as a function of eccentricity. Second, the positions of perikarya within the inner nuclear layer and the level at which the axons branched in the inner plexiform layer were constant at all eccentricities. Bipolar cells with similar morphology have been described previously as "blue cone bipolar cells" (Mariani, 1984b), but there was no direct evidence that this was the case. In this study, we show by light microscopy that labeled bipolar cells have dendrites ending exclusively upon presumptive blue cones labeled by Procion black dye. All blue cones were contacted by labeled bipolar cells, and virtually all bipolar cells contacted blue cones, the only exceptions being in regions where blue cones had been lost. Approximately 20% more labeled bipolar cells than blue cones were found at every eccentricity; thus, connections between blue cones and labeled bipolar cells were not strictly one to one. The mean number of cones presynaptic to each bipolar cell was 1.2, and the mean number of bipolar cells postsynaptic to each cone was 1.8. By an electron microscopic study of labeled bipolar cell dendrites, we determined that they became central elements of ribbon synapses in blue cones. Some of their ribbon synapses were unusual: in one type, a single, large labeled dendrite was postsynaptic to two or more ribbons, while in the other type, ribbons had two or more central elements. The presence of these invaginating contacts and the axonal terminals in the proximal inner plexiform layer suggest that the labeled bipolar cells depolarize to short-wavelength stimuli and function to relay information from blue cones to the inner plexiform layer. There were also other, unlabeled bipolar cell dendrites that received inputs from blue cones at basal junctions and triad-associated flat contacts, which suggests that there are additional types of bipolar cells conveying information from short-wavelength cones in the primate retina.

The human blue opsin promoter directs transgene expression in short-wave cones and bipolar cells in the mouse retina.

“…Cellular connections observed between (3-gal-expressing cone cells and some of the transgene-expressing bipolar cells suggest that at least some of the transgene-expressing bipolar cells may be specific for short-wave cone cells. Based on current knowledge of blue cone bipolar cells in the monkey retina, it is unlikely that the labeled bipolar cells are exclusively blue cone bipolar cells, which are reported to ramify in a single stratum of the inner plexiform layer (34). Thus the presence of two strata of ramification in the inner plexiform layer suggests that other classes of cone bipolar cells express the transgene as well.…”

Cell density ratios in a foveal patch in macaque retina

“…Inner S-cone bipolar cells (1S in Fig. 1B) were contacted by multiple, widely spaced S-cone pedicles (Mariani, 1984;Kouyama & Marshak, 1992;Dacey, 1993a). Like diffuse bipolar cells, their main dendrites branched at the INL0 OPL border.…”

Functional Asymmetries in Visual Pathways Carrying S-Cone Signals in Macaque

“…Dacey and colleagues (Dacey and Packer, 2003;Dacey et al, 2005) identified at least two kinds of ganglion cells that carry strong Sϩ signals and at least one type of SϪ cell, but the pathways that provide S-cone signals to these cells are not yet clear. Although it has long been established that a specialized bipolar cell carries Sϩ signals (Mariani, 1984;Kouyama and Marshak, 1992), the existence of an SϪ bipolar cell remains controversial (Klug et al, 2003;. If there is no such cell, Sϩ signals might be inverted and provided to the ganglion cell by amacrine cells or might feed an inverting synapse on the ganglion cell.…”