The mammalian rod synaptic ribbon is essential for Cav channel facilitation and ultrafast synaptic vesicle fusion

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Abstract

Rod photoreceptors (PRs) use ribbon synapses to transmit visual information. To signal 'no light detected' they release glutamate continually to activate post-synaptic receptors. When light is detected glutamate release pauses. How a rod's individual ribbon enables this process was studied here by recording evoked changes in whole-cell membrane capacitance from wild type and ribbonless (Ribeye-ko) mice. Wild type rods filled with high (10 mM) or low (0.5 mM) concentrations of the Ca²⁺-buffer EGTA created a readily releasable pool (RRP) of 87 synaptic vesicles (SVs) that emptied as a single kinetic phase with a τ < 0.4 msec. The lower concentration of EGTA accelerated Ca_v channel opening and facilitated release kinetics. In contrast, ribbonless rods created a much smaller RRP of 22 SVs, and they lacked Ca_v channel facilitation; however, Ca²⁺ channel-release coupling remained tight. These release deficits caused a sharp attenuation of rod-driven light responses. We conclude that the synaptic ribbon facilitates Ca²⁺-influx and establishes a large RRP of SVs.

Data availability

All analytic tools are described in the Methods section, and they are commercially available. All data and statistical analyses are described throughout the manuscript and in the Methods.

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Author details

Chad Paul Grabner

Synaptic Nanophysiology, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany

For correspondence
chadgrabner@gmail.com

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7885-7627
Tobias Moser

Institute for Auditory Neuroscience, University Medical Center Göttingen, Göttingen, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7145-0533

Funding

Deutsche Forschungsgemeinschaft (Leibniz Award)

Tobias Moser

Deutsche Forschungsgemeinschaft (ExC 2067)

Tobias Moser

Deutsche Forschungsgemeinschaft (CRC 1286,project C08)

Tobias Moser

Deutsche Forschungsgemeinschaft (Multiscale Bioimaging Cluster of Excellence,ExC 2067)

Tobias Moser

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments complied with national animal care guidelines and were approved by the University of Götingen Board for Animal Welfare and the Animal Welfare Office of the State of Lower Saxony (permit number: 14-1391).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.