Endocannabinoids differentially modulate synaptic plasticity in rat hippocampal CA1 pyramidal neurons.

<h4>Background</h4>Hippocampal CA1 pyramidal neurons receive two excitatory glutamatergic synaptic inputs: their most distal dendritic regions in the stratum lacunosum-moleculare (SLM) are innervated by the perforant path (PP), originating from layer III of the entorhinal cortex, while t...

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Autores principales: Jian-Yi Xu, Rongqing Chen, Jian Zhang, Chu Chen
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Publicado: Public Library of Science (PLoS) 2010
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spelling oai:doaj.org-article:9127dab5c92947f5a67365ca866aef352021-11-25T06:24:20ZEndocannabinoids differentially modulate synaptic plasticity in rat hippocampal CA1 pyramidal neurons.1932-620310.1371/journal.pone.0010306https://doaj.org/article/9127dab5c92947f5a67365ca866aef352010-04-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/20421986/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Hippocampal CA1 pyramidal neurons receive two excitatory glutamatergic synaptic inputs: their most distal dendritic regions in the stratum lacunosum-moleculare (SLM) are innervated by the perforant path (PP), originating from layer III of the entorhinal cortex, while their more proximal regions of the apical dendrites in the stratum radiatum (SR) are innervated by the Schaffer-collaterals (SC), originating from hippocampal CA3 neurons. Endocannabinoids (eCBs) are naturally occurring mediators capable of modulating both GABAergic and glutamatergic synaptic transmission and plasticity via the CB1 receptor. Previous work on eCB modulation of excitatory synapses in the CA1 region largely focuses on the SC pathway. However, little information is available on whether and how eCBs modulate glutamatergic synaptic transmission and plasticity at PP synapses.<h4>Methodology/principal findings</h4>By employing somatic and dendritic patch-clamp recordings, Ca(2+) uncaging, and immunostaining, we demonstrate that there are significant differences in low-frequency stimulation (LFS)- or DHPG-, an agonist of group I metabotropic glutamate receptors (mGluRs), induced long-term depression (LTD) of excitatory synaptic transmission between SC and PP synapses in the same pyramidal neurons. These differences are eliminated by pharmacological inhibition with selective CB1 receptor antagonists or genetic deletion of the CB1 receptor, indicating that these differences likely result from differential modulation via a CB1 receptor-dependent mechanism. We also revealed that depolarization-induced suppression of excitation (DSE), a form of short-term synaptic plasticity, and photolysis of caged Ca(2+)-induced suppression of Excitatory postsynaptic currents (EPSCs) were less at the PP than that at the SC. In addition, application of WIN55212 (WIN) induced a more pronounced inhibition of EPSCs at the SC when compared to that at the PP.<h4>Conclusions/significance</h4>Our results suggest that CB1 dependent LTD and DSE are differentially expressed at the PP versus SC synapses in the same neurons, which may have an impact on synaptic scaling, integration and plasticity of hippocampal CA1 pyramidal neurons.Jian-Yi XuRongqing ChenJian ZhangChu ChenPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 5, Iss 4, p e10306 (2010)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Jian-Yi Xu
Rongqing Chen
Jian Zhang
Chu Chen
Endocannabinoids differentially modulate synaptic plasticity in rat hippocampal CA1 pyramidal neurons.
description <h4>Background</h4>Hippocampal CA1 pyramidal neurons receive two excitatory glutamatergic synaptic inputs: their most distal dendritic regions in the stratum lacunosum-moleculare (SLM) are innervated by the perforant path (PP), originating from layer III of the entorhinal cortex, while their more proximal regions of the apical dendrites in the stratum radiatum (SR) are innervated by the Schaffer-collaterals (SC), originating from hippocampal CA3 neurons. Endocannabinoids (eCBs) are naturally occurring mediators capable of modulating both GABAergic and glutamatergic synaptic transmission and plasticity via the CB1 receptor. Previous work on eCB modulation of excitatory synapses in the CA1 region largely focuses on the SC pathway. However, little information is available on whether and how eCBs modulate glutamatergic synaptic transmission and plasticity at PP synapses.<h4>Methodology/principal findings</h4>By employing somatic and dendritic patch-clamp recordings, Ca(2+) uncaging, and immunostaining, we demonstrate that there are significant differences in low-frequency stimulation (LFS)- or DHPG-, an agonist of group I metabotropic glutamate receptors (mGluRs), induced long-term depression (LTD) of excitatory synaptic transmission between SC and PP synapses in the same pyramidal neurons. These differences are eliminated by pharmacological inhibition with selective CB1 receptor antagonists or genetic deletion of the CB1 receptor, indicating that these differences likely result from differential modulation via a CB1 receptor-dependent mechanism. We also revealed that depolarization-induced suppression of excitation (DSE), a form of short-term synaptic plasticity, and photolysis of caged Ca(2+)-induced suppression of Excitatory postsynaptic currents (EPSCs) were less at the PP than that at the SC. In addition, application of WIN55212 (WIN) induced a more pronounced inhibition of EPSCs at the SC when compared to that at the PP.<h4>Conclusions/significance</h4>Our results suggest that CB1 dependent LTD and DSE are differentially expressed at the PP versus SC synapses in the same neurons, which may have an impact on synaptic scaling, integration and plasticity of hippocampal CA1 pyramidal neurons.
format article
author Jian-Yi Xu
Rongqing Chen
Jian Zhang
Chu Chen
author_facet Jian-Yi Xu
Rongqing Chen
Jian Zhang
Chu Chen
author_sort Jian-Yi Xu
title Endocannabinoids differentially modulate synaptic plasticity in rat hippocampal CA1 pyramidal neurons.
title_short Endocannabinoids differentially modulate synaptic plasticity in rat hippocampal CA1 pyramidal neurons.
title_full Endocannabinoids differentially modulate synaptic plasticity in rat hippocampal CA1 pyramidal neurons.
title_fullStr Endocannabinoids differentially modulate synaptic plasticity in rat hippocampal CA1 pyramidal neurons.
title_full_unstemmed Endocannabinoids differentially modulate synaptic plasticity in rat hippocampal CA1 pyramidal neurons.
title_sort endocannabinoids differentially modulate synaptic plasticity in rat hippocampal ca1 pyramidal neurons.
publisher Public Library of Science (PLoS)
publishDate 2010
url https://doaj.org/article/9127dab5c92947f5a67365ca866aef35
work_keys_str_mv AT jianyixu endocannabinoidsdifferentiallymodulatesynapticplasticityinrathippocampalca1pyramidalneurons
AT rongqingchen endocannabinoidsdifferentiallymodulatesynapticplasticityinrathippocampalca1pyramidalneurons
AT jianzhang endocannabinoidsdifferentiallymodulatesynapticplasticityinrathippocampalca1pyramidalneurons
AT chuchen endocannabinoidsdifferentiallymodulatesynapticplasticityinrathippocampalca1pyramidalneurons
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