Morphology of a small-field bistratified ganglion cell type in the macaque and human retina

Abstract

In in-vitro preparations of both macaque and human retina, intracellular injections of Neurobiotin and horseradish peroxidase were used to characterize the morphology, depth of stratification, and mosaic organization of a type of bistratified ganglion cell. This cell type, here called the small bistratified cell, has been shown to project to the parvocellular layers of the dorsal lateral geniculate nucleus (Rodieck, 1991) and is therefore likely to show color-opponent response properties. In both human and macaque, the two dendritic tiers of the bistratified cell are narrowly stratified close to the inner and outer borders of the inner plexiform layer. The inner tier is larger in diameter and more densely branched than the outer tier and gives rise to distinct spine-like branchlets bearing large, often lobulated heads. By contrast the smaller, outer tier is sparsely branched and relatively spine-free. In human retina, the small bistratified cells range in dendritic field diameter from ∼50 µm in central retina to ∼400 µm in the far periphery. The human small bistratified cells are about 20% larger in dendritic-field diameter than their counterparts in the macaque. However, when the difference in retinal magnification between human and macaque is taken into account, the small bistratified cells are similar in size in both species. In macaque, the small bistratified cell has a dendritic-field size that is ~10% larger than that of the magnocellular-projecting parasol ganglion cell. Human small bistratified ganglion cells tend to have smaller dendritic-field diameters than parasol cells. This is because parasol ganglion cells are larger in human than in macaque retina (Dacey & Petersen, 1992). In macaque retina, intracellular injections of Neurobiotin revealed heterotypic tracer coupling to a distinct mosaic of amacrine cells and probable homotypic coupling to an array of neighboring ganglion cells around the perimeter of the injected cell's dendritic tree. The amacrine cell mosaic had a density of 1700 cells/mm2 in peripheral retina. Individual amacrines had small, densely branched and bistratified dendritic fields. From the homotypic coupling, it was possible to estimate for the small bistratified cell a coverage factor of ~1.8, and a density of ~1% of the total ganglion cells in central retina, increasing to ~6–10% in the retinal periphery. The estimated density, dendritic-field size, and depth of stratification all suggest that the small bistratified ganglion cell type is the morphological counterpart of the common short-wavelength sensitive or ‘blue-ON’ physiological type.