Extrinsic determinants of retinal ganglion cell development in primates

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Abstract
As in all mammals studied to date, primate retina contains morphologically distinct classes of retinal ganglion cells (Polyak: The Retina. Chicago: University of Chicago Press, '41; Boycott and Dowling: Philos. Trans. R. Soc. Lond. [Biol.] 225:109–184, '69; Leventhal et al.: Science 213:1139–1142, '81; Perry et al.: Neuroscience 12:1101–1123, '84; Rodieck et al.: J. Comp. Neurol. 233:115–132, '85; Rodieck: In H.D. Steklis and J. Erwin (eds): Comparative Primate Biology, Volume 4: Neurosciences. New York: Alan R. Liss, Inc., pp. 203–278, '88). We have now studied the morphologies, central projections, and retinal distributions of the major morphological classes of ganglion cells in the normal adult monkey, the newborn monkey, and the adult monkey in which restricted regions of retina were depleted of ganglion cells at birth as a result of small lesions made around the perimeter of the optic disc. Both old‐world (Macaca fascicularis) and new‐world (Saimiri sciureus) monkeys were studied. Our results indicate that, at birth, the major morphological classes of monkey retinal ganglion cells are recognizable; cells in central regions are close to adult size whereas cells in peripheral regions are much smaller than in the adult. As in the adult (Stone et al.: J. Comp. Neurol. 150:333–348, '73), in newborn monkeys there is a very sharp division between ipsilaterally and contralaterally projecting retinal ganglion cells (nasotemporal division). Consistent with earlier work (Hendrickson and Kupfer: Invest. Ophthalmol. 15:746–756, '76) we find that the foveal pit in the neonate is immature and contains many more ganglion cells than in the adult. In the adult monkey in which the density of retinal ganglion cells in the central retina was reduced experimentally at birth, the fovea appeared immature, and an abnormally large number of retinal ganglion cells were distributed throughout the foveal pit. The cell bodies and dendritic fields of ganglion cells that developed within cell‐poor regions of the central retina were nearly ten times larger than normal. In peripheral regions the effects were smaller. The dendrites of the abnormally large foveal cells on the borders of cell‐poor zones were directed normally toward the foveal pit. They did not extend preferentially into the cell‐poor region as do the abnormally large cells on the borders of experimentally induced cell‐poor regions of cat central retina (Leventhal et al.: J. Neurosci. 8:1485–1499, '88) or, as we found here, in paracentral regions of primate retina. It is hypothesized that (1) competition for afferents as well as direct interactions among neighboring ganglion cells in the immature retina may contribute to the development of the structure of primate retinal ganglion cells, (2) other factors are also likely to be involved, and (3) foveal development can only proceed normally if the central retina contains an extremely high concentration of retinal ganglion cells.