Synaptic size dynamics as an effectively stochastic process.

Long-term, repeated measurements of individual synaptic properties have revealed that synapses can undergo significant directed and spontaneous changes over time scales of minutes to weeks. These changes are presumably driven by a large number of activity-dependent and independent molecular processe...

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Main Authors: Adiel Statman, Maya Kaufman, Amir Minerbi, Noam E Ziv, Naama Brenner
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-10-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC4183425?pdf=render
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author Adiel Statman
Maya Kaufman
Amir Minerbi
Noam E Ziv
Naama Brenner
author_facet Adiel Statman
Maya Kaufman
Amir Minerbi
Noam E Ziv
Naama Brenner
author_sort Adiel Statman
collection DOAJ
description Long-term, repeated measurements of individual synaptic properties have revealed that synapses can undergo significant directed and spontaneous changes over time scales of minutes to weeks. These changes are presumably driven by a large number of activity-dependent and independent molecular processes, yet how these processes integrate to determine the totality of synaptic size remains unknown. Here we propose, as an alternative to detailed, mechanistic descriptions, a statistical approach to synaptic size dynamics. The basic premise of this approach is that the integrated outcome of the myriad of processes that drive synaptic size dynamics are effectively described as a combination of multiplicative and additive processes, both of which are stochastic and taken from distributions parametrically affected by physiological signals. We show that this seemingly simple model, known in probability theory as the Kesten process, can generate rich dynamics which are qualitatively similar to the dynamics of individual glutamatergic synapses recorded in long-term time-lapse experiments in ex-vivo cortical networks. Moreover, we show that this stochastic model, which is insensitive to many of its underlying details, quantitatively captures the distributions of synaptic sizes measured in these experiments, the long-term stability of such distributions and their scaling in response to pharmacological manipulations. Finally, we show that the average kinetics of new postsynaptic density formation measured in such experiments is also faithfully captured by the same model. The model thus provides a useful framework for characterizing synapse size dynamics at steady state, during initial formation of such steady states, and during their convergence to new steady states following perturbations. These findings show the strength of a simple low dimensional statistical model to quantitatively describe synapse size dynamics as the integrated result of many underlying complex processes.
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spelling doaj.art-4cbf05a80762403caa432ea77818cc412022-12-21T22:50:53ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582014-10-011010e100384610.1371/journal.pcbi.1003846Synaptic size dynamics as an effectively stochastic process.Adiel StatmanMaya KaufmanAmir MinerbiNoam E ZivNaama BrennerLong-term, repeated measurements of individual synaptic properties have revealed that synapses can undergo significant directed and spontaneous changes over time scales of minutes to weeks. These changes are presumably driven by a large number of activity-dependent and independent molecular processes, yet how these processes integrate to determine the totality of synaptic size remains unknown. Here we propose, as an alternative to detailed, mechanistic descriptions, a statistical approach to synaptic size dynamics. The basic premise of this approach is that the integrated outcome of the myriad of processes that drive synaptic size dynamics are effectively described as a combination of multiplicative and additive processes, both of which are stochastic and taken from distributions parametrically affected by physiological signals. We show that this seemingly simple model, known in probability theory as the Kesten process, can generate rich dynamics which are qualitatively similar to the dynamics of individual glutamatergic synapses recorded in long-term time-lapse experiments in ex-vivo cortical networks. Moreover, we show that this stochastic model, which is insensitive to many of its underlying details, quantitatively captures the distributions of synaptic sizes measured in these experiments, the long-term stability of such distributions and their scaling in response to pharmacological manipulations. Finally, we show that the average kinetics of new postsynaptic density formation measured in such experiments is also faithfully captured by the same model. The model thus provides a useful framework for characterizing synapse size dynamics at steady state, during initial formation of such steady states, and during their convergence to new steady states following perturbations. These findings show the strength of a simple low dimensional statistical model to quantitatively describe synapse size dynamics as the integrated result of many underlying complex processes.http://europepmc.org/articles/PMC4183425?pdf=render
spellingShingle Adiel Statman
Maya Kaufman
Amir Minerbi
Noam E Ziv
Naama Brenner
Synaptic size dynamics as an effectively stochastic process.
PLoS Computational Biology
title Synaptic size dynamics as an effectively stochastic process.
title_full Synaptic size dynamics as an effectively stochastic process.
title_fullStr Synaptic size dynamics as an effectively stochastic process.
title_full_unstemmed Synaptic size dynamics as an effectively stochastic process.
title_short Synaptic size dynamics as an effectively stochastic process.
title_sort synaptic size dynamics as an effectively stochastic process
url http://europepmc.org/articles/PMC4183425?pdf=render
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AT mayakaufman synapticsizedynamicsasaneffectivelystochasticprocess
AT amirminerbi synapticsizedynamicsasaneffectivelystochasticprocess
AT noameziv synapticsizedynamicsasaneffectivelystochasticprocess
AT naamabrenner synapticsizedynamicsasaneffectivelystochasticprocess