Role of the synaptic ribbon in transmitting the cone light response

Skyler Jackman, Sue Yeon Choi, Wallace B. Thoreson, Katalin Rabl, Theodore M. Bartoletti, Richard H. Kramer

Research output: Contribution to journalArticle

108 Scopus citations

Abstract

Cone photoreceptors distinguish small changes in light intensity while operating over a wide dynamic range. The cone synapse encodes intensity by modulating tonic neurotransmitter release, but precise encoding is limited by the quantal nature of synaptic vesicle exocytosis. Cones possess synaptic ribbons, structures that are thought to accelerate the delivery of vesicles for tonic release. Here we show that the synaptic ribbon actually constrains vesicle delivery, resulting in a maintained state of synaptic depression in darkness. Electron microscopy of cones from the lizard Anolis segrei revealed that depression is caused by the depletion of vesicles on the ribbon, indicating that resupply, not fusion, is the rate-limiting step that controls release. Responses from postsynaptic retinal neurons from the salamander Ambystoma tigrinum showed that the ribbon behaves like a capacitor, charging with vesicles in light and discharging in a phasic burst at light offset. Phasic release extends the operating range of the cone synapse to more accurately encode changes in light intensity, accentuating features that are salient to photopic vision.

Original languageEnglish (US)
Pages (from-to)303-310
Number of pages8
JournalNature Neuroscience
Volume12
Issue number3
DOIs
Publication statusPublished - Mar 1 2009
Externally publishedYes

    Fingerprint

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Jackman, S., Choi, S. Y., Thoreson, W. B., Rabl, K., Bartoletti, T. M., & Kramer, R. H. (2009). Role of the synaptic ribbon in transmitting the cone light response. Nature Neuroscience, 12(3), 303-310. https://doi.org/10.1038/nn.2267