Rapid synaptic vesicle endocytosis in cone photoreceptors of salamander retina

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

Following synaptic vesicle exocytosis, neurons retrieve the fused membrane by a process of endocytosis to provide a supply of vesicles for subsequent release and maintain the presynaptic active zone. Rod and cone photoreceptors use a specialized structure called the synaptic ribbon that enables them to sustain high rates of neurotransmitter release. They must also employ mechanisms of synaptic vesicle endocytosis capable of keeping up with release. While much is known about endocytosis at another retinal ribbon synapse, that of the goldfish Mb1 bipolar cell, less is known about endocytosis in photoreceptors. We used capacitance recording techniques to measure vesicle membrane fusion and retrieval in photoreceptors from salamander retinal slices. We found that application of brief depolarizing steps (<100 ms) to cones evoked exocytosis followed by rapid endocytosis with a time constant ~250 ms. In some cases, the capacitance trace overshot the baseline, indicating excess endocytosis. Calcium had no effect on the time constant, but enhanced excess endocytosis resulting in a faster rate of membrane retrieval. Surprisingly, endocytosis was unaffected by blockers of dynamin, suggesting that cone endocytosis is dynamin independent. This contrasts with synaptic vesicle endocytosis in rods, which was inhibited by the dynamin inhibitor dynasore and GTPγS introduced through the patch pipette, suggesting that the two photoreceptor types employ distinct pathways for vesicle retrieval. The fast kinetics of synaptic vesicle endocytosis in photoreceptors likely enables these cells to maintain a high rate of transmitter release, allowing them to faithfully signal changes in illumination to second-order neurons.

Original languageEnglish (US)
Pages (from-to)18112-18123
Number of pages12
JournalJournal of Neuroscience
Volume32
Issue number50
DOIs
StatePublished - Dec 12 2012

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Retinal Cone Photoreceptor Cells
Urodela
Synaptic Vesicles
Endocytosis
Retina
Dynamins
Vertebrate Photoreceptor Cells
Exocytosis
Retinal Rod Photoreceptor Cells
Neurons
Goldfish
Membrane Fusion
Membranes
Lighting
Synapses
Neurotransmitter Agents

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Rapid synaptic vesicle endocytosis in cone photoreceptors of salamander retina. / Van Hook, Matthew; Thoreson, Wallace B.

In: Journal of Neuroscience, Vol. 32, No. 50, 12.12.2012, p. 18112-18123.

Research output: Contribution to journalArticle

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