Photoreceptor topography of the retina in the adult pigtail macaque (Macaca nemestrina)

Abstract

In spite of the crucial role retinal photoreceptors play in mapping optical images into a pattern of neural excitation, there are no complete studies of photoreceptor topography in any primate retina. We have measured the spatial density and inner segment areas of cones and rods across the whole mounted retinas of three adult pigtail macaques (Macaca nemestrina) and constructed maps of photoreceptor density and inner segment diameter. These retinas contain an average of 3.1 million cones (2.8-3.3 million), with an average peak foveal cone density of 210,000 cones/mm2 (190,000-260,000 cones/mm2). Cone density falls steeply with increasing eccentricity, to 100,000 cones/mm2 at 200 microns from the fovea, and to 50,000 cones/mm2 at 750 microns. Imposed on this gradient is a "streak" of higher cone density along the horizontal meridian. At equivalent eccentricities, cone density is higher in nasal and inferior retina. Cone inner segments increase in diameter from 2.3 microns at the foveal center to 11 microns in far temporal retina and 10 microns in far nasal retina. These retinas contain an average of 60.1 million rods (44.9-75.3 million). Rod density is zero within 20 microns of the foveal center, increases to the crest of a "rod ring" at the eccentricity of the optic disk, and then declines. Central rod topography is asymmetric, with higher densities in superior retina. Density along the crest of the rod ring peaks in superior retina at 177,000 rods/mm2, dips as low as 120,000 rods/mm2 along the horizontal meridian, and increases to about 150,000 rods/mm2 in inferior retina. Far peripheral rod topography is relatively symmetric around the fovea. Rod inner segment diameter ranged from 1.5 microns in the fovea to 4 microns at the temporal edge and 3.4 microns at the nasal edge of the retina. At eccentricities exceeding 6 mm, rod inner segment diameter was greater temporally than nasally. Cone inner segments cover 85-90% of the central fovea, with extrareceptor space accounting for the remainder. Cone coverage declines with increasing eccentricity to 20% at the temporal edge and 35% at the nasal edge of the retina. In contrast, rod coverage increases from zero at the foveal center to a maximum of 65% in temporal retina and 50% in nasal retina. The photoreceptor topography of the pigtail macaque is qualitatively similar to that of other macaques and to humans. Photoreceptor topography is formed by a complex interaction between regional changes in cone and rod density and inner segment diameter.