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

Acta Physiol (Oxf). 2019 Jun;226(2):e13241. doi: 10.1111/apha.13241. Epub 2019 Jan 12.

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 Ca2+ 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 Cav 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.

Keywords: Bassoon; cone photoreceptor; horizontal cell; retina; ribbon synapse; signal transmission.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Exocytosis / physiology
  • Mice
  • Patch-Clamp Techniques / methods
  • Retina / physiology*
  • Retinal Cone Photoreceptor Cells / physiology*
  • Synapses / physiology*
  • Synaptic Transmission / physiology*