Neural systems are necessarily the adaptive products of natural selection, but a neural system, dedicated to any particular function in a complex brain, may be composed of components that covary with functionally unrelated systems, owing to constraints beyond immediate functional requirements. Some studies support a modular or mosaic organization of the brain, whereas others emphasize coordination and covariation. To contrast these views, we have analysed the retina, striate cortex (V1) and extrastriate cortex (V2, V3, MT, etc.) in 30 mammals, examining the area of the neocortex and individual neocortical areas and the relative numbers of rods and cones. Controlling for brain size and species relatedness, the sizes of visual cortical areas (striate, extrastriate) within the brains of nocturnal and diurnal mammals are not statistically different from one another. The relative sizes of all cortical areas, visual, somatosensory and auditory, are best predicted by the total size of the neocortex. In the sensory periphery, the retina is clearly specialized for niche. New data on rod and cone numbers in various New World primates confirm that rod and cone complements of the retina vary substantially between nocturnal and diurnal species. Although peripheral specializations or receptor surfaces may be highly susceptible to niche-specific selection pressures, the areal divisions of the cerebral cortex are considerably more conservative.

To better understand the evolution of spatial and color vision, the number and spatial distributions of cones, rods, and optic nerve axon numbers were assessed in seven New World primates (Cebus apella,Saimiri ustius,Saguinus midas niger,Alouatta caraya,Aotus azarae, Calllithrix jacchus, andCallicebus moloch). The spatial distribution and number of rods and cones was determined from counts of retinal whole mounts. Optic axon number was determined from optic nerve sections by electron microscopy. These data were amassed with existing data on retinal cell number and distribution in Old World primates, and the scaling of relative densities and numbers with respect to retinal area, eye and brain sizes, and foveal specializations were evaluated. Regular scaling of all cell types was observed, with the exceptionally large, rod-enriched retina of the nocturnal owl monkeyAotus azarae, and the unusually high cone density of the fovea of the trichromatic howler monkeyAlouatta carayapresenting interesting variations on this basic plan. Over all species, the lawful scaling of rods, cones, and retinal ganglion cell number is hypothesized to result from a conserved sequence of cell generation that defends retinal acuity and sensitivity over a large range of eye sizes.

The foveal specializations of five New World monkeys, the marmoset, Callithrix jacchus; the golden-handed tamarin, Saguinus midas niger; the squirrel monkey, Saimiri ustius; the capuchin monkey, Cebus apella; and the howler monkey, Alouatta caraya were compared. Although retinal area varies by over a factor of two in these monkeys, the area of the fovea does not covary with retinal area and remains approximately the same absolute size, as measured by the dimensions of the high density region of cones, or the rod-free region. This constancy in foveal size also holds for rhesus monkeys and humans, bringing the variation in retinal area to a factor of five. Alouatta caraya is unusual, distinguished by a very high central cone density and a small rod-free zone. Physiological constraints that might limit foveal area over a wide range of eye sizes are considered.