Nicotine Uses Neuron-Glia Communication to Enhance Hippocampal Synaptic Transmission and Long-term Memory
Publication Date
November 21, 2012
Journal
PLOS ONE
Authors
Mónica López Hidalgo, Karla Salgado Puga, Reynaldo Alvarado Martínez, Andrea Cristina Medina, et al
Volume
7
Issue
11
Pages
e49998
DOI
https://dx.plos.org/10.1371/journal.pone.0049998
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0049998
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23185511
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3503711
Europe PMC
http://europepmc.org/abstract/MED/23185511
Web of Science
000311821000161
Scopus
84869777978
Mendeley
http://www.mendeley.com/research/nicotine-uses-neuronglia-communication-enhance-hippocampal-synaptic-transmission-longterm-memory
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Mendeley | Further Information

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/289445", "https://ndownloader.figshare.com/files/289485", "https://ndownloader.figshare.com/files/289534"], "description"=>"<div><p>Nicotine enhances synaptic transmission and facilitates long-term memory. Now it is known that bi-directional glia-neuron interactions play important roles in the physiology of the brain. However, the involvement of glial cells in the effects of nicotine has not been considered until now. In particular, the gliotransmitter D-serine, an endogenous co-agonist of NMDA receptors, enables different types of synaptic plasticity and memory in the hippocampus. Here, we report that hippocampal long-term synaptic plasticity induced by nicotine was annulled by an enzyme that degrades endogenous D-serine, or by an NMDA receptor antagonist that acts at the D-serine binding site. Accordingly, both effects of nicotine: the enhancement of synaptic transmission and facilitation of long-term memory were eliminated by impairing glial cells with fluoroacetate, and were restored with exogenous D-serine. Together, these results show that glial D-serine is essential for the long-term effects of nicotine on synaptic plasticity and memory, and they highlight the roles of glial cells as key participants in brain functions.</p> </div>", "links"=>[], "tags"=>["nicotine", "uses", "neuron-glia", "hippocampal", "synaptic", "memory"], "article_id"=>116996, "categories"=>["Neuroscience", "Cell Biology"], "users"=>["Mónica López-Hidalgo", "Karla Salgado-Puga", "Reynaldo Alvarado-Martínez", "Andrea Cristina Medina", "Roberto A. Prado-Alcalá", "Jesús García-Colunga"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0049998.s001", "https://dx.doi.org/10.1371/journal.pone.0049998.s002", "https://dx.doi.org/10.1371/journal.pone.0049998.s003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Nicotine_Uses_Neuron_Glia_Communication_to_Enhance_Hippocampal_Synaptic_Transmission_and_Long_term_Memory__/116996", "title"=>"Nicotine Uses Neuron-Glia Communication to Enhance Hippocampal Synaptic Transmission and Long-term Memory", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-11-21 01:56:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/538453"], "description"=>"<p>A, Experimental arrangement for recording the evoked field potential (EFP) using a stimulation electrode (Stim) located in Schaffer collaterals (SC). B, the EFP slope before, during, and after nicotine administration (Nic; 1 µM, 7 min). The numerals in B (1, 2 and 3) indicate the time at which the representative traces (insets) were taken. The color of the numeral correlates with the color o the trace. The same code was used for the subsequent figures. C, The PPR and representative traces from experiments in B, before (Control, brown), during (black), and after nicotine administration (15 min, orange; 60 min, green). Columns represent the mean ± S.E.M. of results in each condition. Connected circles correspond to individual experiments. Effects on the EFP slope of nicotine combined with mecamylamine, a non-selective antagonist of nAChRs, (D, Mec; 50 µM); with AP5, an antagonist of NMDA receptors (E, F, AP5; 50 µM); or in the presence of fluoroacetate (G, FAC; 5 mM). Insets, for this and subsequent figures, they show representative traces for EFP responses before (brown) and after nicotine administration (early, orange; late, green) in the absence and presence of the test drug. Horizontal bars indicate the timing of drug application. H, Summary of the experiments in B, D–G. For this and subsequent figures, the results are the mean ± S.E.M. of the EFP slope expressed as percent of baseline.10–20 min (early, orange) and 50–60 min (late, green) after nicotine administration, in the absence or presence of the test drug. The dashed line indicates the normalized basal level in each condition (*p<0.05, **p<0.01, one-way repeated-measures ANOVA, <i>post hoc</i> Fisher test).</p>", "links"=>[], "tags"=>["potentiation", "synaptic", "depends", "glial"], "article_id"=>208941, "categories"=>["Neuroscience", "Cell Biology"], "users"=>["Mónica López-Hidalgo", "Karla Salgado-Puga", "Reynaldo Alvarado-Martínez", "Andrea Cristina Medina", "Roberto A. Prado-Alcalá", "Jesús García-Colunga"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0049998.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nicotine_potentiation_of_synaptic_transmission_depends_of_glial_cell_activity_/208941", "title"=>"Nicotine potentiation of synaptic transmission depends of glial cell activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-21 02:29:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/538583"], "description"=>"<p>The EFP slope as a function of time before and after administration of nicotine (Nic, 1 µM) in combination with: D-serine (A, D-ser, 20 µM); DCKA (B, 200 nM), an antagonist of NMDA receptors at the glycine-binding site; DAAO (C, 0.1 U/ml), a specific enzyme that degrades D-serine; or D-serine in the presence of FAC (D, 5 mM). Insets, representative traces with the indicated drugs (see Fig. 1 for details). E, Summary of the experiments in A–D; data represent the mean ± S.E.M. of the EFP slope (as percent of control), after nicotine administration (see Fig. 1 for details), (*p<0.05, **p<0.01, one-way repeated-measures ANOVA, <i>post hoc</i> Fisher test).</p>", "links"=>[], "tags"=>["d-serine", "nicotine", "potentiation", "synaptic"], "article_id"=>209074, "categories"=>["Neuroscience", "Cell Biology"], "users"=>["Mónica López-Hidalgo", "Karla Salgado-Puga", "Reynaldo Alvarado-Martínez", "Andrea Cristina Medina", "Roberto A. Prado-Alcalá", "Jesús García-Colunga"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0049998.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Glial_D_serine_is_necessary_for_nicotine_potentiation_of_synaptic_transmission_/209074", "title"=>"Glial D-serine is necessary for nicotine potentiation of synaptic transmission.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-21 02:31:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/538677"], "description"=>"<p>Training (gray columns) and escape (black columns) latencies of rats that had been treated with: A, different doses of nicotine (Nic); or C, Nic (0.4 mg/kg, same data as in A), AP5 (50 mM), or a combination of both drugs. Retention latency in the inhibitory avoidance task: B, at different doses of Nic; or D, with Nic (0.4 mg/kg, same data as in A) and 50 mM AP5 alone or in combination. For this and Figs. 4, 5, median and interquartile ranges of latency scores are depicted. *p≤0.05 vs. Control, Kruskal-Wallis, <i>post hoc</i> U-Mann-Whitnney.</p>", "links"=>[], "tags"=>["facilitation", "depends", "nmda"], "article_id"=>209172, "categories"=>["Neuroscience", "Cell Biology"], "users"=>["Mónica López-Hidalgo", "Karla Salgado-Puga", "Reynaldo Alvarado-Martínez", "Andrea Cristina Medina", "Roberto A. Prado-Alcalá", "Jesús García-Colunga"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0049998.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nicotine_facilitation_of_long_term_memory_depends_on_NMDA_receptors_/209172", "title"=>"Nicotine facilitation of long-term memory depends on NMDA receptors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-21 02:32:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/538786"], "description"=>"<p>Retention latency in the inhibitory-avoidance task at: B, different concentrations of FAC; or D, with FAC (10 mM, same data as in A), D-serine alone, and D-serine in combination with 10 mM FAC. *p≤0.05, Kruskal-Wallis, <i>post hoc</i> U-Mann-Whitnney.</p>", "links"=>[], "tags"=>["depends", "glial", "d-serine", "latencies", "concentrations", "fac", "100"], "article_id"=>209272, "categories"=>["Neuroscience", "Cell Biology"], "users"=>["Mónica López-Hidalgo", "Karla Salgado-Puga", "Reynaldo Alvarado-Martínez", "Andrea Cristina Medina", "Roberto A. Prado-Alcalá", "Jesús García-Colunga"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0049998.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Long_term_memory_depends_on_glial_D_serine_Training_gray_columns_and_escape_black_columns_latencies_at_A_different_concentrations_of_FAC_or_C_with_FAC_10_mM_same_data_as_in_A_D_serine_alone_D_ser_100_181_M_or_in_combination_/209272", "title"=>"Long-term memory depends on glial D-serine Training (gray columns) and escape (black columns) latencies at: A, different concentrations of FAC; or C, with FAC (10 mM, same data as in A), D-serine alone (D-ser, 100 µM), or in combination.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-21 02:34:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/538880"], "description"=>"<p>A, Training (gray columns) and escape (black columns) latencies with nicotine (Nic, 0.4 mg/kg, same data as in Fig. 3A), Nic and FAC (10 mM), D-serine (D-ser, 100 µM), and Nic, FAC and D-ser. B, Retention latency in the inhibitory-avoidance task in rats subjected to the same experimental conditions as in A. *p≤0.05, Kruskal-Wallis, <i>post hoc</i> U-Mann-Whitnney.</p>", "links"=>[], "tags"=>["facilitated", "nicotine", "depends", "glial"], "article_id"=>209369, "categories"=>["Neuroscience", "Cell Biology"], "users"=>["Mónica López-Hidalgo", "Karla Salgado-Puga", "Reynaldo Alvarado-Martínez", "Andrea Cristina Medina", "Roberto A. Prado-Alcalá", "Jesús García-Colunga"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0049998.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Long_term_memory_facilitated_by_nicotine_depends_on_glial_D_serine_/209369", "title"=>"Long-term memory facilitated by nicotine depends on glial D-serine.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-21 02:36:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/538965"], "description"=>"<p>Due to the electrical stimuli and nicotine activation of nAChRs, the Schaffer collateral terminal releases glutamate that could interact with postsynaptic AMPA and NMDA receptors (AMPAR and NMDAR) in the CA1 pyramidal neuron. At the same time, nicotine activates Ca<sup>2+</sup>-permeable nAChRs <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0049998#pone.0049998-Fucile1\" target=\"_blank\">[106]</a> located in the postsynaptic neuron (helping of the removal of Mg<sup>2+</sup> ions for the NMDA receptor <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0049998#pone.0049998-Mayer1\" target=\"_blank\">[82]</a> and in astrocytes <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0049998#pone.0049998-Sharma1\" target=\"_blank\">[30]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0049998#pone.0049998-Shen1\" target=\"_blank\">[38]</a> thereby promoting the Ca<sup>2+</sup>-dependent release of D-serine. These brain cells and events would participate in concert to allow nicotine to enhance both NMDA receptor-dependent synaptic transmission and memory.</p>", "links"=>[], "tags"=>["cell biology", "neuroscience"], "article_id"=>209462, "categories"=>["Neuroscience", "Cell Biology"], "users"=>["Mónica López-Hidalgo", "Karla Salgado-Puga", "Reynaldo Alvarado-Martínez", "Andrea Cristina Medina", "Roberto A. Prado-Alcalá", "Jesús García-Colunga"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0049998.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Scheme_accounting_for_the_long_term_effect_of_nicotine_/209462", "title"=>"Scheme accounting for the long-term effect of nicotine.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-21 02:37:42"}

PMC Usage Stats | Further Information

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Relative Metric

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