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.

Fig. 1

Examples of EPSCs evoked in horizontal cells by presynaptic stimulation of cones (a) and rods (b, c). The cone-driven EPSC is faster and more transient than the rod-driven EPSCs, but there is also a fast cone-like initial component evident in the rod-driven response shown in b (arrow). Salamander photoreceptors were stimulated by depolarizing voltage steps from −70 to −10 mV, and horizontal cells were voltage-clamped at −50 mV

Fig. 2

Ryanodine (1 μM) stimulates Ca²⁺ increases in rods and cones from a salamander retinal slice loaded with the calcium-sensitive dye, fluo-4. Images are stacks of five confocal sections taken at 1-μm intervals. Image acquisition time was 125 ms/confocal slice. The somas of a rod and cone are labeled in the figure. Bath application of ryanodine for 3 min stimulated a Ca²⁺ increase in both the soma and synaptic terminal (horizontal arrow) of the rod. Ryanodine also caused a Ca²⁺ increase in the soma of the cone, but not the synaptic region at the base of soma (vertical arrow) showed little change. Scale bar=10 μm

Fig. 3

Upon returning to a holding potential of −70 mV after a step to −40 mV, the EPSC evoked in a salamander horizontal cell by presynaptic stimulation of a cone (a) decayed more rapidly than the EPSC evoked in the same horizontal cell (HC) by rod stimulation (b). c Average data from five horizontal cells in which presynaptic test pulses were applied to both a rod and a cone. The EPSCs evoked by cone stimulation (τ=18.9 ms) decayed at a significantly (P=0.01) more rapid rate than those evoked in the same horizontal cells by stimulation of rods (τ=30.2 ms). Horizontal cells were voltage-clamped at −50 mV