Signal transmission at invaginating cone photoreceptor synaptic contacts following deletion of the presynaptic cytomatrix protein Bassoon in mouse retina

Abstract

Abstract Aim A key feature of the mammalian retina is the segregation of visual information in parallel pathways, starting at the photoreceptor terminals. Cone photoreceptors establish synaptic contacts with On bipolar and horizontal cells at invaginating, ribbon‐containing synaptic sites, whereas Off bipolar cells form flat, non‐ribbon‐containing contacts. The cytomatrix protein Bassoon anchors ribbons at the active zone, and its absence induces detachment of ribbons from the active zone. In this study we investigate the impact of a missing Bassoon on synaptic transmission at the first synapse of the visual system. Methods Release properties of cone photoreceptors were studied in wild‐type and mutant mouse retinae with a genetic disruption of the presynaptic cytomatrix protein Bassoon using whole‐cell voltage‐clamp recordings. Light and electron microscopy revealed the distribution of Ca 2+ channels and synaptic vesicles, respectively, in both mouse lines. Results Whole‐cell recordings from postsynaptic horizontal cells of the two mouse lines showed that the presence of Bassoon (and a ribbon) enhanced the rate of exocytosis during tonic and evoked release by increasing synaptic vesicle pool size and replenishment rate, while at the same time slowing synaptic vesicle release. Furthermore, the number of Ca v 1.4 channels and synaptic vesicles was significantly higher at wild‐type than at Bassoon mutant synaptic sites. Conclusion The results of our study demonstrate that glutamate release from cone photoreceptor terminals can occur independent of a synaptic ribbon, but seems restricted to active zones, and they show the importance of a the synaptic ribbon in sustained and spatially and temporally synchronized neurotransmitter release.