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

101 Citations (Scopus)

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
StatePublished - Mar 1 2009
Externally publishedYes

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Light
Synapses
Ambystoma
Retinal Cone Photoreceptor Cells
Retinal Neurons
Urodela
Color Vision
Lizards
Synaptic Vesicles
Darkness
Exocytosis
Neurotransmitter Agents
Electron Microscopy
Depression

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

Role of the synaptic ribbon in transmitting the cone light response. / Jackman, Skyler; Choi, Sue Yeon; Thoreson, Wallace B.; Rabl, Katalin; Bartoletti, Theodore M.; Kramer, Richard H.

In: Nature Neuroscience, Vol. 12, No. 3, 01.03.2009, p. 303-310.

Research output: Contribution to journalArticle

Jackman, S, Choi, SY, Thoreson, WB, Rabl, K, Bartoletti, TM & Kramer, RH 2009, 'Role of the synaptic ribbon in transmitting the cone light response', Nature Neuroscience, vol. 12, no. 3, pp. 303-310. https://doi.org/10.1038/nn.2267
Jackman S, Choi SY, Thoreson WB, Rabl K, Bartoletti TM, Kramer RH. Role of the synaptic ribbon in transmitting the cone light response. Nature Neuroscience. 2009 Mar 1;12(3):303-310. https://doi.org/10.1038/nn.2267
Jackman, Skyler ; Choi, Sue Yeon ; Thoreson, Wallace B. ; Rabl, Katalin ; Bartoletti, Theodore M. ; Kramer, Richard H. / Role of the synaptic ribbon in transmitting the cone light response. In: Nature Neuroscience. 2009 ; Vol. 12, No. 3. pp. 303-310.
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