The Function of the Photoreceptor Synaptic Ribbon - A Study From the Hibernating Ground Squirrel Retina

Abstract

Purpose: : Synaptic transmission of visual signals begins at the photoreceptor-bipolar cell synapse in the retina. A key presynaptic structure of photoreceptors and bipolar cells is the synaptic ribbon (SR), the function of which remains largely speculative. We set out to explore the function of the SR by studying the hibernating ground squirrel (GS) retina, in which the SRs undergo drastic morphological changes.

Methods: : Confocal and electron microscopy (EM) were used to characterize the structural alterations of the SR in the hibernating retina. Direct whole cell patch clamp paired-recordings were applied on cones and their connected bipolar cells in the hibernating retina to probe the synaptic activities of the altered ribbon synapse. ERG was performed to assess the function of the retina.

Results: : In hibernating GSs, confocal images show that a large amount of SRs disengage from the active zone and aggregate into a "large sphere" that resides several microns above the base of the cone terminal. EM images indicate that the "large sphere" is composed of many small ribbon fragments. Surprisingly though, when depolarizing voltage steps are applied to cones, large excitatory postsynaptic potentials (EPSCs) can still be elicited from the postsynaptic bipolar cells; even though immune-staining performed after the recording indicates that the labeling of the SR is greatly reduced. Quantal miniature EPSCs in hibernating GSs are comparable in size and kinetics with those in awake GSs, but are reduced in frequency. The size of the readily releasable pool (RRP) of vesicles at the hibernating cone ribbon synapse decreases significantly. The rate of vesicle replenishment, which is reflected by the recovery rate of the paired-pulse depression, is slower in the hibernating GSs compared with that in the awake GSs. Accordingly, in GSs that were just awaken from hibernation, photopic full-field flash ERG shows a normal waveform with a reduced amplitude and flicker ERG shows a decreased critical fusion frequency.

Conclusions: : Photoreceptor ribbon synapses maintain their basic synaptic functions despite seasonal structural alterations that significantly reduce the size of the ribbons at the synapse. The size of the RRP of the photoreceptor ribbon synapse is correlated to the size of the ribbon. SRs facilitate the turnover of synaptic vesicles to ensure high frequency synaptic signaling.

Keywords: synapse • photoreceptors • bipolar cells