Structure of the synaptic membranes in the inner plexiform layer of the retina: A freeze‐fracture study in monkeys and rabbits

Abstract

The internal structure of the synaptic membranes in the inner plexiform layer (IPL) of the retina of monkeys and rabbits was studied with the freeze-fracturing technique. In ribbon synapses, the presynaptic active zone is characterized by an aggregate of P-face particles, images of synaptic vesicle exocytosis, and forming coated vesicles which occupy distinct, contiguous membrane domains from apex to base of the synaptic ridge. The postsynaptic membrane contains a prominent aggregate of homogeneous particles which remain associated with the E-face. In the presynaptic membrane of conventional synapses, images of synaptic vesicle exocytosis are intermingled with large P-face particles, whereas forming coated vesicles surround the active zone. Three types of internal organization characterize the postsynaptic membrane of conventional synapses. Usually, the postsynaptic membrane exhibits the same internal structure as the surrounding nonjunctional plasmalemma. A second, less common type of conventional synapse contains a loose aggregate of heterogeneous particles which remain associated with the P-face. Finally, synapses were exceptionally found which are macular in shape and contain an aggregate of E-free particles within the postsynaptic membrane. The freeze-fracture evidence suggests that the axonal endings of bipolar cells--or at least some of them--make excitatory synapses, whereas the vast majority of amacrine cell dendrites make inhibitory synapses. Additional specializations of the cell surface in the IPL include gap junctions, puncta adhaerentia, subsurface cisterns, and cell corner aggregates.

Excitatory dyad synapse in rabbit retina.

“…Furthermore, the postsynaptic membranes are decorated by symmetric layers of fluffy cytoplasmic material. With the freeze-fracturing technique it is very difficult to identify the origin of the processes that display synaptic specializations; however, all dyad synapses observed so far in the IPL of the rabbit conform to the pattern that was described previously (8): the membrane of both postsynaptic dendrites contains an aggregate of large particles that remain associated with the outer leaflet ofthe fractured membrane or E face (Fig. 2).…”

“…Furthermore, it is in turn presynaptic to the rod bipolar ending at conventional synaptic junctions, characterized by clustering of vesicles at the presynaptic active zone. Freeze-fracturing shows that no particle aggregate within the membrane of the rod bipolar ending marks the site of these feedback synapses (8).…”

“…The specimen was subsequently reembedded, serially sectioned, and examined with a Jeol 100B electron microscope. Freeze-fracturing was carried out according to the method described in a previous paper (8).…”

“…The results of both pharmacological experiments with a synaptic blocking agent (7) and a freeze-fracture study of the internal structure of the postsynaptic membranes (8) suggest that dyad synapses can be excitatory. In the cat retina, however, light seems to induce hyperpolarization of rod bipolars and depolarization of two of the amacrine cells that are postsynaptic to them (5, 6, 9, 10).…”

Visualizing synaptic vesicle turnover and pool refilling driven by calcium nanodomains at presynaptic active zones of ribbon synapses

“…The concentration of Ca 2+ at the ribbon active zone should rise rapidly to high levels to drive fusion of synaptic vesicles at the speed achieved during the ultrafast component. A variety of lines of evidence indicate that Ca 2+ channels cluster in the plasma membrane at ribbon locations in bipolar cell synaptic terminals (17)(18)(19)(20)(21), and Ca 2+ influx has been shown to occur preferentially at ribbons (19,22). Therefore, nanodomains of high Ca 2+ at the ribbon are likely to be involved in triggering vesicle fusion (19,(22)(23)(24)(25), a conclusion also supported by blockade of the fast component by 1,2-bis(o-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid (BAPTA) but not EGTA (4).…”