Unusual retinal organization in the howler monkey, Alouatta caraya

Abstract

Abstract: : Purpose: To evaluate the number and spatial distribution of retinal ganglion cells in the New World monkey Alouatta caraya. Unlike the callitrichine and cebine New World monkeys, which have sex–linked, non–obligatory trichromacy, ateline Alouatta has trichromatic color vision similar to Old World monkeys. Unlike both groups, the fovea of Alouatta has twice the density of cones with a corresponding reduction of cone diameter. The consequences of this unusually high foveal cone packing for the convergence of photoreceptors to ganglion cells, and thus potential spatial and chromatic acuity are unknown. Methods: The left retinas of 3 howler monkeys were assessed for number and distribution of retinal ganglion cells with light microscopy, and their optic nerves for total axon numbers with electron microscopy. After aldehyde perfusion, the retinas were flat–mounted. Retinal ganglion cells, identified in Nissl material by comparison with retinal ganglion cells labeled retrogradely with HRP or biocytin, were counted at regular intervals along 12 radii centered on the fovea. For each optic nerve, four contiguous complete sections were made and mounted on 2mm grids to produce an unobstructed view of the right, left top and bottom aspects of the nerve face in turn, and reconstructed with respect to a thick section to reproduce the entire optic nerve face. Axon numbers were sampled in a regular grid with appropriate stereological procedures. Results: The mean number of optic nerve axons (1.08 x 10⁶, 5.3% unmyelinated; individual values 1.088, .965 and 1.18 x 10⁶) conformed closely to predictions derived from retinal and brain allometry in other diurnal primates. The spatial distribution of ganglion cells in Alouatta, however, mirrored its atypical cone distribution, that is, much denser in the central retina and sparser in the peripheral retina than comparable diurnal primates. The higher acuity made possible by increased foveal photoreceptor density could thus be transmitted by the greater number of central ganglion cells. Conclusions: The unusually compacted fovea and the parafoveal region of Alouatta comprise not only cones, but also increased numbers of rods and retinal ganglion cells. Since neither cone, rod nor retinal ganglion cell numbers are unexpectedly high for the retina overall, high central cell density is produced at the cost of lowered peripheral cell density. The developmental event that produces the fovea in other primates may extend over approximately twice as much embryonic retinal area in Alouatta, affecting only the distribution and not the generation of cells.

Keywords: retina • macula/fovea • color vision