A Well-Defined Readily Releasable Pool with Fixed Capacity for Storing Vesicles at Calyx of Held.

The readily releasable pool (RRP) of vesicles is a core concept in studies of presynaptic function. However, operating principles lack consensus definition and the utility for quantitative analysis has been questioned. Here we confirm that RRPs at calyces of Held from 14 to 21 day old mice have a fi...

Full description

Saved in:
Bibliographic Details
Main Authors: Kashif Mahfooz, Mahendra Singh, Robert Renden, John F Wesseling
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-04-01
Series:PLoS Computational Biology
Online Access:https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1004855&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849419317778579456
author Kashif Mahfooz
Mahendra Singh
Robert Renden
John F Wesseling
author_facet Kashif Mahfooz
Mahendra Singh
Robert Renden
John F Wesseling
author_sort Kashif Mahfooz
collection DOAJ
description The readily releasable pool (RRP) of vesicles is a core concept in studies of presynaptic function. However, operating principles lack consensus definition and the utility for quantitative analysis has been questioned. Here we confirm that RRPs at calyces of Held from 14 to 21 day old mice have a fixed capacity for storing vesicles that is not modulated by Ca2+. Discrepancies with previous studies are explained by a dynamic flow-through pool, established during heavy use, containing vesicles that are released with low probability despite being immediately releasable. Quantitative analysis ruled out a posteriori explanations for the vesicles with low release probability, such as Ca2+-channel inactivation, and established unexpected boundary conditions for remaining alternatives. Vesicles in the flow-through pool could be incompletely primed, in which case the full sequence of priming steps downstream of recruitment to the RRP would have an average unitary rate of at least 9/s during heavy use. Alternatively, vesicles with low and high release probability could be recruited to distinct types of release sites; in this case the timing of recruitment would be similar at the two types, and the downstream transition from recruited to fully primed would be much faster. In either case, further analysis showed that activity accelerates the upstream step where vesicles are initially recruited to the RRP. Overall, our results show that the RRP can be well defined in the mathematical sense, and support the concept that the defining mechanism is a stable group of autonomous release sites.
format Article
id doaj-art-df1797d56dbb4c6fa1249d8a4e4e897f
institution Kabale University
issn 1553-734X
1553-7358
language English
publishDate 2016-04-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Computational Biology
spelling doaj-art-df1797d56dbb4c6fa1249d8a4e4e897f2025-08-20T03:32:09ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582016-04-01124e100485510.1371/journal.pcbi.1004855A Well-Defined Readily Releasable Pool with Fixed Capacity for Storing Vesicles at Calyx of Held.Kashif MahfoozMahendra SinghRobert RendenJohn F WesselingThe readily releasable pool (RRP) of vesicles is a core concept in studies of presynaptic function. However, operating principles lack consensus definition and the utility for quantitative analysis has been questioned. Here we confirm that RRPs at calyces of Held from 14 to 21 day old mice have a fixed capacity for storing vesicles that is not modulated by Ca2+. Discrepancies with previous studies are explained by a dynamic flow-through pool, established during heavy use, containing vesicles that are released with low probability despite being immediately releasable. Quantitative analysis ruled out a posteriori explanations for the vesicles with low release probability, such as Ca2+-channel inactivation, and established unexpected boundary conditions for remaining alternatives. Vesicles in the flow-through pool could be incompletely primed, in which case the full sequence of priming steps downstream of recruitment to the RRP would have an average unitary rate of at least 9/s during heavy use. Alternatively, vesicles with low and high release probability could be recruited to distinct types of release sites; in this case the timing of recruitment would be similar at the two types, and the downstream transition from recruited to fully primed would be much faster. In either case, further analysis showed that activity accelerates the upstream step where vesicles are initially recruited to the RRP. Overall, our results show that the RRP can be well defined in the mathematical sense, and support the concept that the defining mechanism is a stable group of autonomous release sites.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1004855&type=printable
spellingShingle Kashif Mahfooz
Mahendra Singh
Robert Renden
John F Wesseling
A Well-Defined Readily Releasable Pool with Fixed Capacity for Storing Vesicles at Calyx of Held.
PLoS Computational Biology
title A Well-Defined Readily Releasable Pool with Fixed Capacity for Storing Vesicles at Calyx of Held.
title_full A Well-Defined Readily Releasable Pool with Fixed Capacity for Storing Vesicles at Calyx of Held.
title_fullStr A Well-Defined Readily Releasable Pool with Fixed Capacity for Storing Vesicles at Calyx of Held.
title_full_unstemmed A Well-Defined Readily Releasable Pool with Fixed Capacity for Storing Vesicles at Calyx of Held.
title_short A Well-Defined Readily Releasable Pool with Fixed Capacity for Storing Vesicles at Calyx of Held.
title_sort well defined readily releasable pool with fixed capacity for storing vesicles at calyx of held
url https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1004855&type=printable
work_keys_str_mv AT kashifmahfooz awelldefinedreadilyreleasablepoolwithfixedcapacityforstoringvesiclesatcalyxofheld
AT mahendrasingh awelldefinedreadilyreleasablepoolwithfixedcapacityforstoringvesiclesatcalyxofheld
AT robertrenden awelldefinedreadilyreleasablepoolwithfixedcapacityforstoringvesiclesatcalyxofheld
AT johnfwesseling awelldefinedreadilyreleasablepoolwithfixedcapacityforstoringvesiclesatcalyxofheld
AT kashifmahfooz welldefinedreadilyreleasablepoolwithfixedcapacityforstoringvesiclesatcalyxofheld
AT mahendrasingh welldefinedreadilyreleasablepoolwithfixedcapacityforstoringvesiclesatcalyxofheld
AT robertrenden welldefinedreadilyreleasablepoolwithfixedcapacityforstoringvesiclesatcalyxofheld
AT johnfwesseling welldefinedreadilyreleasablepoolwithfixedcapacityforstoringvesiclesatcalyxofheld