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A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons

A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons
A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons
Synapse-specific vesicle pools have been widely characterized at central terminals. Here, we demonstrate a vesicle pool that is not confined to a synapse but spans multiple terminals. Using fluorescence imaging, correlative electron microscopy, and modeling of vesicle dynamics, we show that some recycling pool vesicles at synapses form part of a larger vesicle "superpool." The vesicles within this superpool are highly mobile and are rapidly exchanged between terminals (turnover: approximately 4% of total pool/min), significantly changing vesicular composition at synapses over time. In acute hippocampal slices we show that the mobile vesicle pool is also a feature of native brain tissue. We also demonstrate that superpool vesicles are available to synapses during stimulation, providing an extension of the classical recycling pool. Experiments using focal BDNF application suggest the involvement of a local TrkB-receptor-dependent mechanism for synapse-specific regulation of presynaptic vesicle pools through control of vesicle release and capture to or from the extrasynaptic pool.
0896-6273
37-44
Staras, Kevin
9a6b1f6a-5d97-4541-a902-dfa050dbcda0
Branco, Tiago
54dc5f89-4c7b-4bab-a3b9-ed9c3b1ff3a8
Burden, Jemima J.
b4ae1812-bd80-4a46-b501-931fb2756062
Pozo, Karine
13587535-44f6-4722-85ee-fc82606c4607
Darcy, Kevin
604dc092-a1ee-4407-9092-b588effc66f9
Marra, Vincenzo
0d34b5f4-3145-4b25-ade3-801a5d45555c
Ratnayaka, Arjuna
002499b8-1a9f-45b6-9539-5ac145799dfd
Goda, Yukiko
051c94b4-4fc4-4712-8c5f-c14bff932c52
Staras, Kevin
9a6b1f6a-5d97-4541-a902-dfa050dbcda0
Branco, Tiago
54dc5f89-4c7b-4bab-a3b9-ed9c3b1ff3a8
Burden, Jemima J.
b4ae1812-bd80-4a46-b501-931fb2756062
Pozo, Karine
13587535-44f6-4722-85ee-fc82606c4607
Darcy, Kevin
604dc092-a1ee-4407-9092-b588effc66f9
Marra, Vincenzo
0d34b5f4-3145-4b25-ade3-801a5d45555c
Ratnayaka, Arjuna
002499b8-1a9f-45b6-9539-5ac145799dfd
Goda, Yukiko
051c94b4-4fc4-4712-8c5f-c14bff932c52

Staras, Kevin, Branco, Tiago, Burden, Jemima J., Pozo, Karine, Darcy, Kevin, Marra, Vincenzo, Ratnayaka, Arjuna and Goda, Yukiko (2010) A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron, 66 (1), 37-44. (doi:10.1016/j.neuron.2010.03.020). (PMID:20399727)

Record type: Article

Abstract

Synapse-specific vesicle pools have been widely characterized at central terminals. Here, we demonstrate a vesicle pool that is not confined to a synapse but spans multiple terminals. Using fluorescence imaging, correlative electron microscopy, and modeling of vesicle dynamics, we show that some recycling pool vesicles at synapses form part of a larger vesicle "superpool." The vesicles within this superpool are highly mobile and are rapidly exchanged between terminals (turnover: approximately 4% of total pool/min), significantly changing vesicular composition at synapses over time. In acute hippocampal slices we show that the mobile vesicle pool is also a feature of native brain tissue. We also demonstrate that superpool vesicles are available to synapses during stimulation, providing an extension of the classical recycling pool. Experiments using focal BDNF application suggest the involvement of a local TrkB-receptor-dependent mechanism for synapse-specific regulation of presynaptic vesicle pools through control of vesicle release and capture to or from the extrasynaptic pool.

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More information

Published date: April 2010
Organisations: Clinical & Experimental Sciences

Identifiers

Local EPrints ID: 352136
URI: http://eprints.soton.ac.uk/id/eprint/352136
ISSN: 0896-6273
PURE UUID: e670bb9b-cca5-4f5b-ac70-bac08cf02fbd
ORCID for Arjuna Ratnayaka: ORCID iD orcid.org/0000-0002-1027-6938

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Date deposited: 02 May 2013 13:42
Last modified: 15 Mar 2024 03:47

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Contributors

Author: Kevin Staras
Author: Tiago Branco
Author: Jemima J. Burden
Author: Karine Pozo
Author: Kevin Darcy
Author: Vincenzo Marra
Author: Yukiko Goda

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