Sustained increase of spontaneous input and spike transfer in the CA3-CA1 pathway following long term potentiation in vivo

Long term potentiation (LTP) is commonly used to study synaptic plasticity but the associated changes in the spontaneous activity of individual neurons or the computational properties of neural networks in vivo remain largely unclear. The multisynaptic origin of spontaneous spikes makes difficult es...

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Main Authors: Oscar eHerreras, Valeri eMakarov, Antonio eFernández-Ruiz
Format: Article
Language:English
Published: Frontiers Media S.A. 2012-10-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fncir.2012.00071/full
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spelling doaj-1777137871cc455ba2fe227cf10630702020-11-24T20:51:48ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102012-10-01610.3389/fncir.2012.0007133760Sustained increase of spontaneous input and spike transfer in the CA3-CA1 pathway following long term potentiation in vivoOscar eHerreras0Valeri eMakarov1Antonio eFernández-Ruiz2Consejo Superior de Investigaciones Científicas (CSIC)Universidad Complutense de MadridConsejo Superior de Investigaciones Científicas (CSIC)Long term potentiation (LTP) is commonly used to study synaptic plasticity but the associated changes in the spontaneous activity of individual neurons or the computational properties of neural networks in vivo remain largely unclear. The multisynaptic origin of spontaneous spikes makes difficult estimating the impact of a particular potentiated input. Accordingly, we adopted an approach that isolates pathway-specific postsynaptic activity from raw local field potentials (LFPs) in the rat hippocampus in order to study the effects of LTP on ongoing spike transfer between cell pairs in the CA3-CA1 pathway. CA1 Schaffer-specific LFPs elicited by spontaneous clustered firing of CA3 pyramidal cells involved a regular succession of elementary micro-field-EPSPs (gamma-frequency) that fired spikes in CA1 units. LTP increased the amplitude but not the frequency of these ongoing excitatory quanta. Also, the proportion of Schaffer-driven spikes in both CA1 pyramidal cells and interneurons increased in a cell-specific manner only in previously connected CA3-CA1 cell pairs, i.e., when the CA3 pyramidal cell had shown pre-LTP significant correlation with firing of a CA1 unit and potentiated spike-triggered average of Schaffer LFPs following LTP. Moreover, LTP produced subtle reorganization of presynaptic CA3 cell assemblies. These findings show effective enhancement of pathway specific ongoing activity which leads to increased spike transfer in potentiated segments of a network. These indicate that plastic phenomena induced by external protocols may intensify spontaneous information flow across specific channels as proposed in transsynaptic propagation of plasticity and synfire chain hypotheses that may be the substrate for different types of memory involving multiple brain structures.http://journal.frontiersin.org/Journal/10.3389/fncir.2012.00071/fulllong term potentiationsynaptic plasticitysynfire chainIndependent Component AnalysisLocal Field Potentialsspontaneous activity
collection DOAJ
language English
format Article
sources DOAJ
author Oscar eHerreras
Valeri eMakarov
Antonio eFernández-Ruiz
spellingShingle Oscar eHerreras
Valeri eMakarov
Antonio eFernández-Ruiz
Sustained increase of spontaneous input and spike transfer in the CA3-CA1 pathway following long term potentiation in vivo
Frontiers in Neural Circuits
long term potentiation
synaptic plasticity
synfire chain
Independent Component Analysis
Local Field Potentials
spontaneous activity
author_facet Oscar eHerreras
Valeri eMakarov
Antonio eFernández-Ruiz
author_sort Oscar eHerreras
title Sustained increase of spontaneous input and spike transfer in the CA3-CA1 pathway following long term potentiation in vivo
title_short Sustained increase of spontaneous input and spike transfer in the CA3-CA1 pathway following long term potentiation in vivo
title_full Sustained increase of spontaneous input and spike transfer in the CA3-CA1 pathway following long term potentiation in vivo
title_fullStr Sustained increase of spontaneous input and spike transfer in the CA3-CA1 pathway following long term potentiation in vivo
title_full_unstemmed Sustained increase of spontaneous input and spike transfer in the CA3-CA1 pathway following long term potentiation in vivo
title_sort sustained increase of spontaneous input and spike transfer in the ca3-ca1 pathway following long term potentiation in vivo
publisher Frontiers Media S.A.
series Frontiers in Neural Circuits
issn 1662-5110
publishDate 2012-10-01
description Long term potentiation (LTP) is commonly used to study synaptic plasticity but the associated changes in the spontaneous activity of individual neurons or the computational properties of neural networks in vivo remain largely unclear. The multisynaptic origin of spontaneous spikes makes difficult estimating the impact of a particular potentiated input. Accordingly, we adopted an approach that isolates pathway-specific postsynaptic activity from raw local field potentials (LFPs) in the rat hippocampus in order to study the effects of LTP on ongoing spike transfer between cell pairs in the CA3-CA1 pathway. CA1 Schaffer-specific LFPs elicited by spontaneous clustered firing of CA3 pyramidal cells involved a regular succession of elementary micro-field-EPSPs (gamma-frequency) that fired spikes in CA1 units. LTP increased the amplitude but not the frequency of these ongoing excitatory quanta. Also, the proportion of Schaffer-driven spikes in both CA1 pyramidal cells and interneurons increased in a cell-specific manner only in previously connected CA3-CA1 cell pairs, i.e., when the CA3 pyramidal cell had shown pre-LTP significant correlation with firing of a CA1 unit and potentiated spike-triggered average of Schaffer LFPs following LTP. Moreover, LTP produced subtle reorganization of presynaptic CA3 cell assemblies. These findings show effective enhancement of pathway specific ongoing activity which leads to increased spike transfer in potentiated segments of a network. These indicate that plastic phenomena induced by external protocols may intensify spontaneous information flow across specific channels as proposed in transsynaptic propagation of plasticity and synfire chain hypotheses that may be the substrate for different types of memory involving multiple brain structures.
topic long term potentiation
synaptic plasticity
synfire chain
Independent Component Analysis
Local Field Potentials
spontaneous activity
url http://journal.frontiersin.org/Journal/10.3389/fncir.2012.00071/full
work_keys_str_mv AT oscareherreras sustainedincreaseofspontaneousinputandspiketransferintheca3ca1pathwayfollowinglongtermpotentiationinvivo
AT valeriemakarov sustainedincreaseofspontaneousinputandspiketransferintheca3ca1pathwayfollowinglongtermpotentiationinvivo
AT antonioefernandezruiz sustainedincreaseofspontaneousinputandspiketransferintheca3ca1pathwayfollowinglongtermpotentiationinvivo
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