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Development of the rhesus monkey retina: II. A three-dimensional analysis of the sequences of synaptic combinations
Abstract:
The inner plexiform layer (IPL) of the retina provides a useful model for ultrastructural analysis of synaptic development. In primates, the IPL consists of numerous combinations of neuronal contacts that assume the morphological configuration of either conventional or ribbon synapses. We have determined the sequential development of these combinations by analyzing serial electron microscopic sections from fetal rhesus monkeys. Our analysis reveals an orderly emergence of various pre- and postsynaptic elements: (1) patches of dense filamentous membrane first appear on the dendrites of ganglion (G) cells; (2) membrane densities on ganglion cell dendrites then become apposed to amacrine (A) cell processes still lacking their own membrane densities and synaptic vesicles; (3) amacrine cell processes acquire membrane specializations associated with vesicles at the sites apposing ganglion cell dendrites, thereby establishing the first morphologically complete, A----G subtype of conventional synapse; (4) pairs of amacrine cell processes form A----A subtypes of conventional synapses; (5) next, monad ribbon synapses are established between bipolar (B) and ganglion or amacrine cell processes (B----G; B----A); (6) the three subclasses of dyad ribbon synapses (B----GG; B----GA; B----AA) are subsequently formed by the introduction of additional amacrine or ganglion cell processes in the dyad synapse; (7) concurrently, processes of some amacrine and interplexiform (I) cells form a feedback circuit with bipolar cell axons (A----B; I----B), thereby completing the synaptic microcircuitry of the IPL. Present findings provide evidence that the sequence of synaptic differentiation in the IPL proceeds from the postsynaptic to the presynaptic site. Furthermore, lateral interactions (A----G and A----A) are established prior to the formation of the "straight signal" pathway from photoreceptors (P) via bipolar cells to ganglion cells (P----B----G). Observed developmental events provide new insight into the order of establishment of local neuronal circuits in the primate retina.