Development of the rhesus monkey retina. I. Emergence of the inner plexiform layer and its synapses

Abstract

The emergence and differentiation of the inner plexiform layer (IPL) and the establishment of its synapses were analyzed in retinae of 18 rhesus monkeys ranging in age from the 55th embryonic day (E55) to 10 years. The IPL becomes recognizable by E65 as a thin acellular zone consisting of immature neurites and growth cones scattered within large extracellular spaces. In each specimen, apposing paired membrane specializations were classified as junctions without synaptic vesicles, conventional synapses, ribbon synapses, or gap junctions. Initially, at E65, the IPL consists of variety of immature cell processes that are interconnected exclusively by junctions without synaptic vesicles, at a density of 4.7/100 μm². By E73, the IPL becomes more distinct and wider and contains 7.8 such junctions/100 μm². Conventional synapses develop by the addition of vesicles to initially vesiclefree junctions. The first conventional synapses appear at E78. They increase in density from 1.5 to 3.2/100 μm² between E78 and E84 and reach a density of 7.9/100 μm² by E99. A rapid burst in synaptogenesis occurs in the IPL between E99 and E114; a density of 16.5/100 μm² is reached, mainly due to accretion of conventional synapses. Ribbon synapses first become recognizable at E99, almost 3 weeks after the emergence of conventional synapses. By E114 they account for about 7% of all synaptic contacts in the IPL. The rate of synaptogenesis slows down during the last quarter of gestation; the adult level of about 24 contacts/100 μm² is reached between E130 and E149. Of these, 72.2% are of conventional type, 15.4% are ribbon synapses, and 12.4% are junctions without vesicles. However, in the adult the density of junction without vesicles is only about one‐half that found at E149. Gap junctions are absent during the initial and rapid phases of synaptogenesis; they appear abruptly, between E130 and E149, only after the density of chemical synapses in the IPL has reached the adult level. In the rhesus monkey, synaptogenesis begins several weeks later in the IPL than in its primary targets–the dorsal lateral geniculate nucleus and the superior colliculus (Hendrickson and Rakic, '77; Cooper and Rakic, '83). However, the rapid increase in density of conventional synapses in the IPL coincides with the segregation of retinal projections from right and left eyes in the geniculate nucleus (Rakic, '76) and with the elimination of the large surplus of retinal ganglion cell axons (Rakic and Reley, '83).