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A pre-docking source for the power-law behavior of spontaneous quantal release: application to the analysis of LTP

In neurons, power-law behavior with different scaling exponents has been reported at many different levels, including fluctuations in membrane potentials, synaptic transmission up to neuronal network dynamics. Unfortunately in most cases the source of this non-linear feature remains controversial. H...

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Autores principales: Lamanna, Jacopo, Signorini, Maria G., Cerutti, Sergio, Malgaroli, Antonio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4332339/
https://www.ncbi.nlm.nih.gov/pubmed/25741239
http://dx.doi.org/10.3389/fncel.2015.00044
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author Lamanna, Jacopo
Signorini, Maria G.
Cerutti, Sergio
Malgaroli, Antonio
author_facet Lamanna, Jacopo
Signorini, Maria G.
Cerutti, Sergio
Malgaroli, Antonio
author_sort Lamanna, Jacopo
collection PubMed
description In neurons, power-law behavior with different scaling exponents has been reported at many different levels, including fluctuations in membrane potentials, synaptic transmission up to neuronal network dynamics. Unfortunately in most cases the source of this non-linear feature remains controversial. Here we have analyzed the dynamics of spontaneous quantal release at hippocampal synapses and characterized their power-law behavior. While in control conditions a fractal exponent greater than zero was rarely observed, its value was greatly increased by α-latrotoxin (α-LTX), a potent stimulator of spontaneous release, known to act at the very last step of vesicle fusion. Based on computer modeling, we confirmed that at an increase in fusion probability would unmask a pre-docking phenomenon with 1/f structure, where α estimated from the release series appears to sense the increase in release probability independently from the number of active sites. In the simplest scenario the pre-docking 1/f process could coincide with the Brownian diffusion of synaptic vesicles. Interestingly, when the effect of long-term potentiation (LTP) was tested, a ~200% long-lasting increase in quantal frequency was accompanied by a significant increase in the scaling exponent. The similarity between the action of LTP and of α-LTX suggests an increased contribution of high release probability sites following the induction of LTP. In conclusion, our results indicate that the source of the synaptic power-law behavior arises before synaptic vesicles dock to the active zone and that the fractal exponent α is capable of sensing a change in release probability independently from the number of active sites or synapses.
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spelling pubmed-43323392015-03-04 A pre-docking source for the power-law behavior of spontaneous quantal release: application to the analysis of LTP Lamanna, Jacopo Signorini, Maria G. Cerutti, Sergio Malgaroli, Antonio Front Cell Neurosci Neuroscience In neurons, power-law behavior with different scaling exponents has been reported at many different levels, including fluctuations in membrane potentials, synaptic transmission up to neuronal network dynamics. Unfortunately in most cases the source of this non-linear feature remains controversial. Here we have analyzed the dynamics of spontaneous quantal release at hippocampal synapses and characterized their power-law behavior. While in control conditions a fractal exponent greater than zero was rarely observed, its value was greatly increased by α-latrotoxin (α-LTX), a potent stimulator of spontaneous release, known to act at the very last step of vesicle fusion. Based on computer modeling, we confirmed that at an increase in fusion probability would unmask a pre-docking phenomenon with 1/f structure, where α estimated from the release series appears to sense the increase in release probability independently from the number of active sites. In the simplest scenario the pre-docking 1/f process could coincide with the Brownian diffusion of synaptic vesicles. Interestingly, when the effect of long-term potentiation (LTP) was tested, a ~200% long-lasting increase in quantal frequency was accompanied by a significant increase in the scaling exponent. The similarity between the action of LTP and of α-LTX suggests an increased contribution of high release probability sites following the induction of LTP. In conclusion, our results indicate that the source of the synaptic power-law behavior arises before synaptic vesicles dock to the active zone and that the fractal exponent α is capable of sensing a change in release probability independently from the number of active sites or synapses. Frontiers Media S.A. 2015-02-18 /pmc/articles/PMC4332339/ /pubmed/25741239 http://dx.doi.org/10.3389/fncel.2015.00044 Text en Copyright © 2015 Lamanna, Signorini, Cerutti and Malgaroli. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Lamanna, Jacopo
Signorini, Maria G.
Cerutti, Sergio
Malgaroli, Antonio
A pre-docking source for the power-law behavior of spontaneous quantal release: application to the analysis of LTP
title A pre-docking source for the power-law behavior of spontaneous quantal release: application to the analysis of LTP
title_full A pre-docking source for the power-law behavior of spontaneous quantal release: application to the analysis of LTP
title_fullStr A pre-docking source for the power-law behavior of spontaneous quantal release: application to the analysis of LTP
title_full_unstemmed A pre-docking source for the power-law behavior of spontaneous quantal release: application to the analysis of LTP
title_short A pre-docking source for the power-law behavior of spontaneous quantal release: application to the analysis of LTP
title_sort pre-docking source for the power-law behavior of spontaneous quantal release: application to the analysis of ltp
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4332339/
https://www.ncbi.nlm.nih.gov/pubmed/25741239
http://dx.doi.org/10.3389/fncel.2015.00044
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