A Reinforcing Circuit Action of Extrasynaptic GABAA Receptor Modulators on Cerebellar Granule Cell Inhibition
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{"title"=>"A reinforcing circuit action of extrasynaptic GABA<inf>A</inf> receptor modulators on cerebellar granule cell inhibition", "type"=>"journal", "authors"=>[{"first_name"=>"Vijayalakshmi", "last_name"=>"Santhakumar", "scopus_author_id"=>"6701846585"}, {"first_name"=>"Pratap", "last_name"=>"Meera", "scopus_author_id"=>"6701308179"}, {"first_name"=>"Movses H.", "last_name"=>"Karakossian", "scopus_author_id"=>"8847291900"}, {"first_name"=>"Thomas S.", "last_name"=>"Otis", "scopus_author_id"=>"6603915468"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"604820792", "sgr"=>"84894105979", "pmid"=>"23977374", "scopus"=>"2-s2.0-84894105979", "doi"=>"10.1371/journal.pone.0072976", "issn"=>"19326203"}, "id"=>"84cdd170-4100-36ee-a920-a026efe5c380", "abstract"=>"GABAA receptors (GABARs) are the targets of a wide variety of modulatory drugs which enhance chloride flux through GABAR ion channels. Certain GABAR modulators appear to acutely enhance the function of δ subunit-containing GABAR subtypes responsible for tonic forms of inhibition. Here we identify a reinforcing circuit mechanism by which these drugs, in addition to directly enhancing GABAR function, also increase GABA release. Electrophysiological recordings in cerebellar slices from rats homozygous for the ethanol-hypersensitive (α6100Q) allele show that modulators and agonists selective for δ-containing GABARs such as THDOC, ethanol and THIP (gaboxadol) increased the frequency of spontaneous inhibitory postsynaptic currents (sIPSCs) in granule cells. Ethanol fails to augment granule cell sIPSC frequency in the presence of glutamate receptor antagonists, indicating that circuit mechanisms involving granule cell output contribute to ethanol-enhancement of synaptic inhibition. Additionally, GABAR antagonists decrease ethanol-induced enhancement of Golgi cell firing. Consistent with a role for glutamatergic inputs, THIP-induced increases in Golgi cell firing are abolished by glutamate receptor antagonists. Moreover, THIP enhances the frequency of spontaneous excitatory postsynaptic currents in Golgi cells. Analyses of knockout mice indicate that δ subunit-containing GABARs are required for enhancing GABA release in the presence of ethanol and THIP. The limited expression of the GABAR δ subunit protein within the cerebellar cortex suggests that an indirect, circuit mechanism is responsible for stimulating Golgi cell GABA release by drugs selective for extrasynaptic isoforms of GABARs. Such circuit effects reinforce direct actions of these positive modulators on tonic GABAergic inhibition and are likely to contribute to the potent effect of these compounds as nervous system depressants.", "link"=>"http://www.mendeley.com/research/reinforcing-circuit-action-extrasynaptic-gabainfainf-receptor-modulators-cerebellar-granule-cell-inh", "reader_count"=>19, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>2, "Researcher"=>6, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>2, "Researcher"=>6, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>12, "Medicine and Dentistry"=>1, "Neuroscience"=>4, "Psychology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>4}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}}, "reader_count_by_country"=>{"Austria"=>1, "United States"=>3, "United Kingdom"=>1, "Germany"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1174696"], "description"=>"<p><i>A.</i> Schematic of the connectivity between cerebellar granule cells and Golgi cells including the inhibitory connections between Golgi cells identified in recent studies <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0072976#pone.0072976-Hull1\" target=\"_blank\">[33]</a>. Location of extrasynaptic GABARs in granule cell somata and parallel fiber axons is illustrated. Prediction (right panel), illustrates the proposed changes in neuronal activity in the circuit following increased activation of parallel fiber GABARs. <i>B</i>. Hypothesized effect of GluR antagonists on circuit activity following increase in activation of granule cell extrasynaptic GABARs. Red X indicates blocked glutamatergic synapses. <i>C</i>. Predicted effects of GABAR antagonists on granule and Golgi cell activity following increased activation of granule cell extrasynaptic GABARs. Red X indicates blocked GABA synapses and orange X denotes block of both somato-dendritic and axonal extrasynaptic GABARs.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "electrophysiology", "Model organisms", "Animal models", "mouse", "rat", "neuroscience", "Cellular neuroscience", "ion channels", "neurophysiology", "Central nervous system", "synapses", "Motor systems", "neurotransmitters", "Cell physiology", "anesthesiology", "Anesthetic mechanisms", "neurology", "Cerebellar disorders", "Neuropharmacology", "circuit", "ethanol-enhancement", "synaptic", "gaba", "golgi"], "article_id"=>776229, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Vijayalakshmi Santhakumar", "Pratap Meera", "Movses H. Karakossian", "Thomas S. Otis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0072976.g001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_of_the_circuit_hypothesis_for_ethanol_enhancement_of_synaptic_GABA_release_from_Golgi_neurons_/776229", "title"=>"Schematic of the circuit hypothesis for ethanol-enhancement of synaptic GABA release from Golgi neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-19 03:33:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1174697"], "description"=>"<p><i>A.</i> Representative granule cell current traces recorded in ACSF (CON, left panel) and during perfusion of 50 mM ethanol (EtOH, middle panel). Cumulative probability plots (right panel) compare the frequency of individual sIPSC in ACSF (CON) and after perfusion of 50 mM ethanol (same number of events from <i>n</i> = 5 cells; <i>p</i><0.05 by K-S test). <i>B</i>. Granule cell current traces recorded in the presence of the GluR antagonists 20 µM APV and 25 µM DNQX (CON, left panel) and after inclusion of 50 mM ethanol (EtOH, middle panel). Cumulative probability plots (right panel) show the frequency distribution of individual sIPSCs in APV/DNQX (CON) and after addition of 50 mM ethanol (identical number of events from <i>n</i> = 6 cells; <i>p</i><0.05 by K-S test). <i>C</i>. Summary data of the sIPSC frequency averaged over 30 second periods in control conditions before addition of ethanol (CON) and in the presence 50 mM ethanol. The frequency of sIPSCs recorded in ACSF is compared with the effect observed in DNQX/APV (# indicates p<0.05 by two-way repeated measures ANOVA followed by post-hoc analyses by Holm-Sidak method). <i>D</i>. Summary data of the sIPSC frequency averaged over 30 second periods in control conditions before addition of ethanol (CON) and in the presence 10 mM ethanol. Individual data points are represented by open circles connected by dotted lines. (** indicates p<0.05 by Wilcoxon Signed Rank test). <i>F</i>. Summary histogram of the sIPSC frequency in ethanol, normalized to frequency in the same cell prior to perfusion of ethanol (n.s. denotes p>0.05, * indicates p<0.05 by paired <i>t</i>-test and ## indicates p<0.05 by one-way ANOVA followed by post-hoc analyses by Holm-Sidak method).</p>", "links"=>[], "tags"=>["Anatomy and physiology", "electrophysiology", "Model organisms", "Animal models", "mouse", "rat", "neuroscience", "Cellular neuroscience", "ion channels", "neurophysiology", "Central nervous system", "synapses", "Motor systems", "neurotransmitters", "Cell physiology", "anesthesiology", "Anesthetic mechanisms", "neurology", "Cerebellar disorders", "Neuropharmacology", "glutamatergic", "abolishes", "ethanol-effects", "granule", "sipsc"], "article_id"=>776230, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Vijayalakshmi Santhakumar", "Pratap Meera", "Movses H. Karakossian", "Thomas S. Otis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0072976.g002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Blocking_glutamatergic_transmission_abolishes_ethanol_effects_on_granule_cell_sIPSC_frequency_/776230", "title"=>"Blocking glutamatergic transmission abolishes ethanol-effects on granule cell sIPSC frequency.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-19 03:33:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1174699"], "description"=>"<p><i>A.</i> Overlay of normalized granule cell sIPSC traces recorded in ACSF show that there was no difference in the IPSC kinetics under control conditions (black) and in 50mM ethanol (gray). <i>B.</i> Overlay of normalized granule cell sIPSC traces recorded in DNQX (25 µM) and APV (20 µM) show no difference in IPSC kinetics in the absence (black) and in 50mM ethanol (gray). <i>C</i>. Summary plots of sIPSC amplitude before and during ethanol perfusion illustrate the lack of ethanol-modulation both in ACSF and in GluR antagonists (DNQX/APV). <i>D</i>. Histogram of the weighted τ<sub>decay</sub> of granule cell sIPSCs in ACSF in GluR antagonists (DNQX/APV) recorded before and during ethanol perfusion.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "electrophysiology", "Model organisms", "Animal models", "mouse", "rat", "neuroscience", "Cellular neuroscience", "ion channels", "neurophysiology", "Central nervous system", "synapses", "Motor systems", "neurotransmitters", "Cell physiology", "anesthesiology", "Anesthetic mechanisms", "neurology", "Cerebellar disorders", "Neuropharmacology", "modulate", "sipsc", "amplitude"], "article_id"=>776232, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Vijayalakshmi Santhakumar", "Pratap Meera", "Movses H. Karakossian", "Thomas S. Otis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0072976.g003", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ethanol_does_not_modulate_sIPSC_amplitude_or_decay_/776232", "title"=>"Ethanol does not modulate sIPSC amplitude or decay.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-19 03:33:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1174701"], "description"=>"<p><i>A</i>. Voltage clamp recordings from a granule cell illustrates the effect of ethanol (50 mM) on synaptic and tonic GABA currents recorded in the presence of the GluR antagonists APV (20 µM) and kynurenic acid (KyA, 3 mM). To the right are histograms of all points in each segment. Tonic GABA currents were measured as the baseline current blocked by GABAR antagonist gabazine (10 µM). Gaussian fits to the positive half of the current trace under each condition are superimposed (right panel). The dashed lines indicate the mean current from these fits and difference currents are noted. <i>B</i>. Plot illustrates the time course of changes in baseline currents, averaged over 100 ms time intervals, during perfusion of ethanol (50 mM) and subsequent washout of ethanol. Baseline current averages during gabazine perfusion at the end of the recordings were used to measure tonic GABA current amplitude. Segments of representative current traces in A and baseline currents in B were obtained from the same recordings <i>C.</i> Summary plot of the effect of ethanol on granule cell sIPSC frequency in the presence of ACSF and in KyA/APV. In each case, sIPSC frequency was averaged over a 30 second recording periods. <i>C</i>. Histogram shows that the amplitude of tonic GABA currents in ethanol (50 mM) normalized to the tonic GABA current amplitude in the same cell prior to perfusion of ethanol, both in ACSF and in KyA/APV. * indicates p<0.05 by paired <i>t</i>-test.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "electrophysiology", "Model organisms", "Animal models", "mouse", "rat", "neuroscience", "Cellular neuroscience", "ion channels", "neurophysiology", "Central nervous system", "synapses", "Motor systems", "neurotransmitters", "Cell physiology", "anesthesiology", "Anesthetic mechanisms", "neurology", "Cerebellar disorders", "Neuropharmacology", "tonic", "gaba", "currents", "sipsc", "glutamate", "receptor"], "article_id"=>776234, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Vijayalakshmi Santhakumar", "Pratap Meera", "Movses H. Karakossian", "Thomas S. Otis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0072976.g004", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ethanol_enhances_tonic_GABA_currents_without_increasing_sIPSC_frequency_in_the_presence_of_glutamate_receptor_antagonists_/776234", "title"=>"Ethanol enhances tonic GABA currents without increasing sIPSC frequency in the presence of glutamate receptor antagonists.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-19 03:33:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1174703"], "description"=>"<p><i>A.</i> Representative current traces illustrate enhancement of sIPSC frequency and tonic GABA currents by THIP (1 µM). To the right are histograms of all points in each segment. Tonic GABA currents were measured as the baseline current blocked by GABAR antagonist gabazine (10 µM). Gaussian fits to current trace under each condition are superimposed (right panel). Dashed lines indicate the mean baseline currents and the difference in baseline currents measured as tonic GABA currents are noted. <i>B.</i> Summary data show the effect of 500 nM and 1 µM THIP on granule cell sIPSC frequency. <i>C.</i> Histogram shows the amplitude of tonic GABA currents in ACSF, 500 nM and 1 µM THIP measured simultaneously during the recordings in B. * indicates p<0.05 by paired <i>t</i>-test, # indicates p<0.05 by one-way repeated measures ANOVA followed by post-hoc analyses by Holm-Sidak method.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "electrophysiology", "Model organisms", "Animal models", "mouse", "rat", "neuroscience", "Cellular neuroscience", "ion channels", "neurophysiology", "Central nervous system", "synapses", "Motor systems", "neurotransmitters", "Cell physiology", "anesthesiology", "Anesthetic mechanisms", "neurology", "Cerebellar disorders", "Neuropharmacology", "selective", "agonist", "thip", "sipsc"], "article_id"=>776236, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Vijayalakshmi Santhakumar", "Pratap Meera", "Movses H. Karakossian", "Thomas S. Otis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0072976.g005", "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GABAR_948_subunit_selective_agonist_THIP_increases_sIPSC_frequency_/776236", "title"=>"GABAR δ-subunit selective agonist THIP increases sIPSC frequency.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-19 03:33:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1174705"], "description"=>"<p>A. Voltage clamp recordings from granule cells illustrate the relatively low frequency of synaptic events in granule cells recorded in control conditions (upper trace) and the increase in the number of synaptic events following perfusion of 10 nM THDOC (lower trace). <i>B-C</i>. Plots show the effect of THDOC (10 nM) on the frequency of sIPSCs (<i>B</i>) and amplitude of tonic GABA current (<i>C</i>) recorded in the same cells. Individual data points are represented by open circles connected by dotted lines. Synaptic events were completely abolished in 10 µM gabazine. Amplitude of tonic GABA currents was measured as the baseline current blocked by 10 µM gabazine. * indicates p<0.05 by paired <i>t</i>-test, <i>D-E</i>. Histogram demonstrates the lack of THDOC (10 nM) modulation of granule cell sIPSC amplitude (<i>B</i>) and weighted τ<sub>decay</sub> (<i>D</i>).</p>", "links"=>[], "tags"=>["Anatomy and physiology", "electrophysiology", "Model organisms", "Animal models", "mouse", "rat", "neuroscience", "Cellular neuroscience", "ion channels", "neurophysiology", "Central nervous system", "synapses", "Motor systems", "neurotransmitters", "Cell physiology", "anesthesiology", "Anesthetic mechanisms", "neurology", "Cerebellar disorders", "Neuropharmacology", "induce", "parallel", "granule", "sipsc", "tonic", "gaba"], "article_id"=>776238, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Vijayalakshmi Santhakumar", "Pratap Meera", "Movses H. Karakossian", "Thomas S. Otis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0072976.g006", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Neurosteroids_induce_parallel_increases_in_granule_cell_sIPSC_frequency_and_tonic_GABA_currents_/776238", "title"=>"Neurosteroids induce parallel increases in granule cell sIPSC frequency and tonic GABA currents.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-19 03:33:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1174707"], "description"=>"<p><i>A.</i> Example trace of loose-patch cell-attached recordings from a Golgi cell illustrates the spontaneous firing in ACSF (upper panel) and the increase in firing in the presence of 50 mM ethanol (lower panel). <i>B.</i> Golgi cell firing recorded in the presence of gabazine (10 µM) in loose-patch mode before (upper panel) and during application of 50 mM ethanol (lower panel). <i>C</i>. Summary plots of the frequency of Golgi cell firing in 50 mM ethanol, normalized to the firing frequency before ethanol perfusion in ACSF (white bar) and in gabazine (black bar). <i>D</i>. Summary plots of the frequency of Golgi cell firing in 1 µM THIP, normalized to the firing frequency before THIP perfusion in ACSF (white bar) and in 3 mM kynurenic acid and 20 µM APV (black bar). * indicates p<0.05 by paired <i>t</i>-test.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "electrophysiology", "Model organisms", "Animal models", "mouse", "rat", "neuroscience", "Cellular neuroscience", "ion channels", "neurophysiology", "Central nervous system", "synapses", "Motor systems", "neurotransmitters", "Cell physiology", "anesthesiology", "Anesthetic mechanisms", "neurology", "Cerebellar disorders", "Neuropharmacology", "gaba", "glutamate", "receptors", "enhancement", "golgi", "firing", "extrasynaptic", "gabar"], "article_id"=>776240, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Vijayalakshmi Santhakumar", "Pratap Meera", "Movses H. Karakossian", "Thomas S. Otis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0072976.g007", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Blocking_GABA_or_glutamate_receptors_reduces_enhancement_of_Golgi_cell_firing_by_extrasynaptic_GABAR_agonists_/776240", "title"=>"Blocking GABA or glutamate receptors reduces enhancement of Golgi cell firing by extrasynaptic GABAR agonists.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-19 03:33:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1174710"], "description"=>"<p><i>A.</i> Representative Golgi cell current recordings obtained with a low chloride internal solution at a holding potential of –70 mV. Recordings in control ACSF (upper panel) and after perfusion of 1 µM THIP (lower panel) illustrate the increase in frequency of spontaneous excitatory synaptic events in THIP. <i>B</i>. Summary plot shows the effect of THIP on Golgi cell sEPSC frequency. Individual data points are represented by open circles connected by dotted lines. * indicates p<0.05 by paired <i>t</i>-test.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "electrophysiology", "Model organisms", "Animal models", "mouse", "rat", "neuroscience", "Cellular neuroscience", "ion channels", "neurophysiology", "Central nervous system", "synapses", "Motor systems", "neurotransmitters", "Cell physiology", "anesthesiology", "Anesthetic mechanisms", "neurology", "Cerebellar disorders", "Neuropharmacology", "golgi", "sepsc"], "article_id"=>776243, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Vijayalakshmi Santhakumar", "Pratap Meera", "Movses H. Karakossian", "Thomas S. Otis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0072976.g008", "stats"=>{"downloads"=>2, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_THIP_increases_Golgi_cell_sEPSC_frequency_/776243", "title"=>"THIP increases Golgi cell sEPSC frequency.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-19 03:33:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1174712"], "description"=>"<p><i>A-B.</i> Current traces recorded in cerebellar granule cells from wild-type (<i>A</i>) and <i>Gabrd</i>–<i>/</i>– mice (<i>B</i>) in the presence of 50mM and 100 mM ethanol. Both synaptic and tonic GABA currents are blocked by gabazine (10 µM). Gaussian fits to current traces superimposed on histograms of all points in each segment (right panel). Dashed lines indicate the mean current from the fits used to measure tonic GABA current amplitude (difference in baseline current blocked by gabazine). <i>C</i>. sIPSC frequency in ethanol normalized to frequency prior to ethanol perfusion in wild-type (WT) and <i>Gabrd</i>–<i>/</i>– mice (δ<sup>−/−</sup>). <i>D</i>. Granule cell tonic GABA current amplitudes in wild-type (WT) and <i>Gabrd</i>–<i>/</i>– (δ<sup>−/−</sup>) measured in control ACSF and in the presence of 50 and 100 mM ethanol. <i>E</i>. Summary plot of the effect of THIP (500 nM) on granule cell sIPSC frequency in wild-type (WT) mice, in ACSF and in the presence of KyA/APV. In each case, sIPSC frequency was averaged over a 30 second recording period. <i>F</i>. Effect of THIP (500 nM) on granule cell tonic GABA current amplitude in wild-type (WT) mice measured in control ACSF and in the presence of KyA/APV. * indicates p<0.05 by paired <i>t</i>-test within genotype and # indicates p<0.05 by two-way repeated measures ANOVA followed by post hoc pairwise comparison using Holm-Sidak method. <i>G</i>. Effect of THIP (1 µM) on granule cell tonic GABA current amplitude in <i>Gabrd</i>–<i>/</i>– mice measured in control ACSF. Individual data points are represented by open circles connected by dotted lines.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "electrophysiology", "Model organisms", "Animal models", "mouse", "rat", "neuroscience", "Cellular neuroscience", "ion channels", "neurophysiology", "Central nervous system", "synapses", "Motor systems", "neurotransmitters", "Cell physiology", "anesthesiology", "Anesthetic mechanisms", "neurology", "Cerebellar disorders", "Neuropharmacology", "granule", "sipsc", "ethanol", "thip", "gabar", "glutamatergic", "synaptic"], "article_id"=>776245, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Vijayalakshmi Santhakumar", "Pratap Meera", "Movses H. Karakossian", "Thomas S. Otis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0072976.g009", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increase_in_granule_cell_sIPSC_frequency_by_ethanol_and_THIP_require_the_presence_of_GABAR_948_8211_subunits_and_intact_glutamatergic_synaptic_transmission_/776245", "title"=>"Increase in granule cell sIPSC frequency by ethanol and THIP require the presence of GABAR δ–subunits and intact glutamatergic synaptic transmission.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-08-19 03:33:32"}

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Relative Metric

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