Kinetics of Synaptic Transmission at Ribbon Synapses of Rods and Cones

Abstract

The ribbon synapse is a specialized structure that allows photoreceptors to sustain the continuous release of vesicles for hours upon hours and years upon years but also respond rapidly to momentary changes in illumination. Light responses of cones are faster than those of rods and, mirroring this difference, synaptic transmission from cones is also faster than transmission from rods. This review evaluates the various factors that regulate synaptic kinetics and contribute to kinetic differences between rod and cone synapses. Presynaptically, the release of glutamate-laden synaptic vesicles is regulated by properties of the synaptic proteins involved in exocytosis, influx of calcium through calcium channels, calcium release from intracellular stores, diffusion of calcium to the release site, calcium buffering, and extrusion of calcium from the cytoplasm. The rate of vesicle replenishment also limits the ability of the synapse to follow changes in release. Post-synaptic factors include properties of glutamate receptors, dynamics of glutamate diffusion through the cleft, and glutamate uptake by glutamate transporters. Thus, multiple synaptic mechanisms help to shape the responses of second-order horizontal and bipolar cells. KeywordsPhotoreceptor; Synaptic transmission; Glutamate; Calcium; Vesicles; Retina Vision begins with the transduction of light into membrane potential changes as the result of an enzymatic cascade occurring in the outer segments of rod and cone photoreceptors [1,2]. Light-evoked membrane potential changes are modified by voltage-dependent currents in the inner segment [3] and transmitted to second order bipolar and horizontal cells by changes in release of the neurotransmitter, L-glutamate, from the synaptic terminals of both rods and cones. Because all of the visual information available to downstream retinal neurons must first pass through the photoreceptor synapse, synaptic transmission from photoreceptors has a considerable impact on visual perception. The focus of this review is on mechanisms that shape the kinetics of synaptic transmission at synapses of rods and cones. Additional information on other physiological and anatomical characteristics of photoreceptor ribbon synapses can be found in recent reviews [4][5][6]. Differences in Rod and Cone KineticsRod and cone photoreceptors are tonically depolarized in darkness with membrane potentials of −35 to −45 mV that allow continuous release of the neurotransmitter, L-glutamate. Light onset causes photoreceptors to hyperpolarize by as much as 30 mV, leading to a reduction in

Evidence That Vesicles Undergo Compound Fusion on the Synaptic Ribbon

“…2005; Thoreson, 2007). For example, a ribbon in a dissociated bipolar neuron, when strongly depolarized, can fuse ϳ500 vesicles s Ϫ1 (von Gersdorff et al, 1996), and similar rates were found in auditory hair cells (Parsons et al 1994).…”

Calmodulin Is a Functional Regulator of Cav1.4 L-type Ca2+ Channels

“…Glutamate release in these synapses is controlled via graded and sustained changes in membrane potential that are maintained throughout the duration of a light stimulus (1,2). In recent years, it became clear that Cav1.4 L-type Ca 2ϩ channels are the main channel subtype converting these analog input signals into corresponding permanent glutamate release (1,(3)(4)(5). In support of this mechanism, mutations in the Cav1.4 gene have been identified in patients suffering from congenital stationary night blindness type 2 and X-linked cone rod dystrophy (6 -8).…”

Retinal temporal resolution and contrast sensitivity in the parasitic lampreyMordacia mordaxand its non-parasitic derivativeM.praecox

“…Cones have faster light response kinetics than rods (Hestrin and Korenbrot, 1990;Thoreson, 2007), which allows them to have higher FFFs. Cones are, however, less sensitive to light, and their responses decline rapidly with decreasing light intensity Wolf, 1939, 1941;Hestrin and Korenbrot, 1990;Meneghini and Hamasaki, 1967).…”

“…This suggests that the response kinetics of the photoreceptor within Mordacia spp. are slow (Thoreson, 2007) and may be rod like.…”

“…The photoreceptors of both Mordacia species, however, show signs of saturation at the brightest light intensity examined, as the FFF started to plateau in M. praecox and actually decreased in M. mordax, adding further support for a rod-like physiology (Fitzpatrick, 2004). A decrease in FFF suggests that the visual pigment is being bleached and the post-stimulus recovery is slow (Aguilar and Stiles, 1954;Hestrin and Korenbrot, 1990;Thoreson, 2007).…”