Plasticity of retinal ribbon synapses

Abstract

Ribbon synapses differ from conventional chemical synapses in that they contain, within the cloud of synaptic vesicles (SV's), a specialized synaptic body, most often termed synaptic ribbon (SR). This body assumes various forms. Reconstructions reveal that what appear as rod‐ or ribbon‐like profiles in sections are in fact rectangular or horseshoe‐shaped plates. Moreover, spherical, T‐shaped, table‐shaped, and highly pleomorphic bodies may be present. In mammals, ribbon synapses are present in afferent synapses of photoreceptors, bipolar nerve cells, and hair cells of both the organ of Corti and the vestibular organ. Synaptic ribbons (SR's) are also found in the intrinsic cells of the third eye, the pineal gland, and in the lateral line system. The precise function of SR's is enigmatic. The prevailing concept is that SR's function as conveyor belts to channel SV's to the presynaptic membrane for neurotransmitter release by means of exocytosis. The present article reviews the evidence that speaks for a plasticity of these organelles in the retina and the third eye, as reflected in changes in number, size, shape, location, and grouping pattern. SR plasticity is especially pronounced in the mammalian and submammalian pineal gland and in cones and bipolar cells of teleost fishes. Here, SR number and size wax and wane according to the environmental lighting conditions. In the pineal SR numbers increase at night and decrease during the day. In teleost cones, SR's are in their prime during daytime and decrease or disappear at night, when transmitter release is enhanced. In addition to numerical changes, SR's may also exhibit changes in size, shape, grouping pattern, and location. In the mammalian retina of adults, in contrast to the developing retina, the reported signs of SR plasticity are subtle and not always consistent. They may reflect changes in function or may represent signs of degradation. To distinguish between the two, more detailed studies under selected experimental conditions are required. Probably the strongest evidence for SR plasticity in the mammalian retina is that in hibernating squirrels SR's leave the synaptic site and accumulate in areas as far as 5 μm from the synapse. Changes in shape include the occurrence of club‐shaped SR's and round SR's or synaptic spheres (SS's). SS's may represent a special type of synaptic body, yet belonging to the family of SR's, or may be related to the catabolism of SR's. SR number is regulated by Ca2+ in teleost cones, whereas in the mammalian pineal gland cGMP is involved. An interesting biochemical feature of ribbon synapses is that they lack synapsins. The presently reviewed results suggest to us that SR's do not primarily function as conveyor belts, but are devices to immobilize SV's in inactive ribbon synapses. © 1996 Wiley‐Liss, Inc.

The expression of L‐type voltage‐gated calcium channels in retinal photoreceptors is under circadian control

“…In sensory synapses, synaptic ribbons mediate continuous neurotransmitter release in response to graded depolarization, and the shape and number of photoreceptor synaptic ribbons are under circadian control (Vollrath and Spiwoks-Becker 1996;Hull et al 2006). In mice lacking the b 2 subunit of the L-type VGCCs, the photoreceptor ribbons become unanchored or disorganized (Ball et al 2002).…”

Components and connections of the circadian timing system in mammals

“…Vollrath 1981). Well-known examples are the distinct rhythms of melatonin synthesis, of spontaneous electrical activity and of "synaptic" bodies probably involved in intercellular communication (for reviews, see McNulty and Fox 1992;Reuss 1987;Sugden 1989;Vollrath 1981;Vollrath and Spiwoks 1996). A considerable number of studies indicate that these rhythms are driven by the SCN and predominantly are mediated by the sympathetic system.…”

Synaptic transmission at retinal ribbon synapses

“…1. As reviewed elsewhere (Vollrath and Spiwoks-Becker, 1996), photoreceptor ribbons exhibit diurnal changes in shape and size. However, in turtle cones where the ribbon surface area decreases almost two-fold in darkness, there is a compensatory two-fold increase in synaptic vesicle density on the ribbon face suggesting that the number of tethered vesicles remains nearly constant despite considerable changes in ribbon size (Pierantoni and McCann, 1981).…”