A freeze-fracture study of photoreceptor presynaptic membranes during ribbon synapse formation

Abstract

The outer plexiform layer (OPL) of the developing chick retina from 11 embryonic days to 11/2 weeks posthatching has been studied by freeze-fracture to characterize changes in the membrane structure of photoreceptor terminals during synaptogenesis. At early stages, the undifferentiated photoreceptor synaptic base is characterized by a sparse distribution of intramembrane articles on the inner leaflet (P-face). Later, as the synaptic base begins to differentiate by extending filopodia into the OPL, numerous small aggregates of large particles appear between and on filopodial surfaces. Many of the aggregates occupy crater-like expressions, which are seen in cross-fractures through the underlying cytoplasm to be associated with vesicular invaginations of the presynaptic membrane. Corresponding thin sections through these regions at this time reveal immature arciform densities and coated vesicles fusing with the presynaptic membrane adjacent to these densities. At later stages, many of the particle aggregates on the photoreceptor membrane appear to have coalesced into longer arrays overlying ridges surrounded by numerous vesicle fusion sites. These intramembrane changes correlate with the formation of the mature arciform density-synaptic ribbon specialization in the photoreceptor presynaptic terminal and with physiological maturation of the chick retina.

Review: Fine structure of synaptogenesis in the vertebrate central nervous system

“…Later stages encompass the formation of presynaptic ribbons with associated accumulations of synaptic vesicles. More recent observations of photoreceptor synaptogenesis in conventional and freeze-fracture electron micrographs have led to the suggestions that 1) coated vesicles may be involved in an insertion of the intramembrane particles (IMPs) that are observed to accumulate in synaptic regions of photoreceptor membranes during synaptic differentiation, and 2) the IMPs coalesce into ridge-like arrays sur-rounded by vesicle fusion sites in correlation with the differentiation of presynaptic ribbons (McLaughlin and Reese, 1981). Similar freeze-fracture observations have been made in developing Xenopus retina, where there is also evidence that IMPs aggregate in presynaptic receptor membranes prior to postsynaptic horizontal cell membranes (Nagy and Witkovsky, 1981); but these investigators emphasize that close appositions between putative synaptic surfaces occur in advance of IMP aggregation in either preor postsynaptic membranes.…”

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