The Neuroglial Potassium Cycle during Neurotransmission: Role of Kir4.1 Channels
Publication Date
March 31, 2015
Journal
PLOS Computational Biology
Authors
Jérémie Sibille, Khanh Dao Duc, David Holcman & Nathalie Rouach
Volume
11
Issue
3
Pages
e1004137
DOI
https://dx.plos.org/10.1371/journal.pcbi.1004137
Publisher URL
http://journals.plos.org/ploscompbiol/article?id=10.1371%2Fjournal.pcbi.1004137
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/25826753
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4380507
Europe PMC
http://europepmc.org/abstract/MED/25826753
Web of Science
000352195700033
Scopus
84926311570
Mendeley
http://www.mendeley.com/research/neuroglial-potassium-cycle-during-neurotransmission-role-kir41-channels
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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/2000476", "https://ndownloader.figshare.com/files/2000477"], "description"=>"<div><p>Neuronal excitability relies on inward sodium and outward potassium fluxes during action potentials. To prevent neuronal hyperexcitability, potassium ions have to be taken up quickly. However, the dynamics of the activity-dependent potassium fluxes and the molecular pathways underlying extracellular potassium homeostasis remain elusive. To decipher the specific and acute contribution of astroglial K<sub>ir</sub>4.1 channels in controlling potassium homeostasis and the moment to moment neurotransmission, we built a tri-compartment model accounting for potassium dynamics between neurons, astrocytes and the extracellular space. We here demonstrate that astroglial K<sub>ir</sub>4.1 channels are sufficient to account for the slow membrane depolarization of hippocampal astrocytes and crucially contribute to extracellular potassium clearance during basal and high activity. By quantifying the dynamics of potassium levels in neuron-glia-extracellular space compartments, we show that astrocytes buffer within 6 to 9 seconds more than 80% of the potassium released by neurons in response to basal, repetitive and tetanic stimulations. Astroglial K<sub>ir</sub>4.1 channels directly lead to recovery of basal extracellular potassium levels and neuronal excitability, especially during repetitive stimulation, thereby preventing the generation of epileptiform activity. Remarkably, we also show that K<sub>ir</sub>4.1 channels strongly regulate neuronal excitability for slow 3 to 10 Hz rhythmic activity resulting from probabilistic firing activity induced by sub-firing stimulation coupled to Brownian noise. Altogether, these data suggest that astroglial K<sub>ir</sub>4.1 channels are crucially involved in extracellular potassium homeostasis regulating theta rhythmic activity.</p></div>", "links"=>[], "tags"=>["hippocampal astrocytes", "tetanic stimulations", "Action potentials", "extracellular potassium homeostasis", "basal extracellular potassium levels", "potassium fluxes", "potassium ions", "moment neurotransmission", "astrocytes buffer", "potassium levels", "10 Hz", "membrane depolarization", "potassium homeostasis", "Kir 4.1 channels", "epileptiform activity", "astroglial Kir 4.1 channels", "potassium dynamics", "Neuroglial Potassium Cycle", "Brownian noise", "Extracellular space", "extracellular potassium clearance", "Kir 4.1 Channels Neuronal excitability", "9 seconds"], "article_id"=>1363432, "categories"=>["Uncategorised"], "users"=>["Jérémie Sibille", "Khanh Dao Duc", "David Holcman", "Nathalie Rouach"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1004137.s001", "https://dx.doi.org/10.1371/journal.pcbi.1004137.s002"], "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Neuroglial_Potassium_Cycle_during_Neurotransmission_Role_of_Kir4_1_Channels_/1363432", "title"=>"The Neuroglial Potassium Cycle during Neurotransmission: Role of Kir4.1 Channels", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-03-31 04:01:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/2000474"], "description"=>"<p>Parameters.</p>", "links"=>[], "tags"=>["hippocampal astrocytes", "tetanic stimulations", "Action potentials", "extracellular potassium homeostasis", "basal extracellular potassium levels", "potassium fluxes", "potassium ions", "moment neurotransmission", "astrocytes buffer", "potassium levels", "10 Hz", "membrane depolarization", "potassium homeostasis", "Kir 4.1 channels", "epileptiform activity", "astroglial Kir 4.1 channels", "potassium dynamics", "Neuroglial Potassium Cycle", "Brownian noise", "Extracellular space", "extracellular potassium clearance", "Kir 4.1 Channels Neuronal excitability", "9 seconds"], "article_id"=>1363430, "categories"=>["Uncategorised"], "users"=>["Jérémie Sibille", "Khanh Dao Duc", "David Holcman", "Nathalie Rouach"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1004137.t001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Parameters_/1363430", "title"=>"Parameters.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-03-31 04:01:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/2000471"], "description"=>"<p>Comparison of simulated [K<sup>+</sup>]<sub>o</sub> (<b><i>A</i>,<i>E I</i></b>) or neuronal firing (<b><i>C</i>,<i>G</i>,<i>K</i></b>) in control conditions (blue, Ctrl) and during inhibition of K<sub>ir</sub>4.1 channels (light blue) following single (<b><i>A-D</i></b>), tetanic (100 Hz, 1 s) <b><i>(E-H)</i></b> and repetitive (10 Hz, 30 s) (<b><i>I-L</i></b>) stimulations, respectively. Quantification of kinetics of extracellular K<sup>+</sup> transients (<b><i>B</i>,<i>F</i>,<i>J</i></b>) and neuronal firing (<b><i>D</i>,<i>H</i>,<i>L</i></b>) evoked by single, tetanic and repetitive stimulations, respectively.</p>", "links"=>[], "tags"=>["hippocampal astrocytes", "tetanic stimulations", "Action potentials", "extracellular potassium homeostasis", "basal extracellular potassium levels", "potassium fluxes", "potassium ions", "moment neurotransmission", "astrocytes buffer", "potassium levels", "10 Hz", "membrane depolarization", "potassium homeostasis", "Kir 4.1 channels", "epileptiform activity", "astroglial Kir 4.1 channels", "potassium dynamics", "Neuroglial Potassium Cycle", "Brownian noise", "Extracellular space", "extracellular potassium clearance", "Kir 4.1 Channels Neuronal excitability", "9 seconds"], "article_id"=>1363427, "categories"=>["Uncategorised"], "users"=>["Jérémie Sibille", "Khanh Dao Duc", "David Holcman", "Nathalie Rouach"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1004137.g004", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Acute_contribution_of_astroglial_K_ir_4_1_channels_to_the_dynamics_of_neuronal_firing_and_extracellular_potassium_levels_/1363427", "title"=>"Acute contribution of astroglial K<sub>ir</sub>4.1 channels to the dynamics of neuronal firing and extracellular potassium levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-31 04:01:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/2000470"], "description"=>"<p><b><i>A-I</i></b>, K<sup>+</sup> redistribution between neurons, extracellular space and astrocytes induced by single (<b><i>A-C</i></b>), tetanic (100 Hz, 1 s) (<b><i>D-F</i></b>) and repetitive (10 Hz, 30 s) (<b><i>G-I</i></b>) stimulations. For all regimes of activity, neuronal K<sup>+</sup> (red) is released, increasing K<sup>+</sup> in the extracellular space (black) during the stimulation initiated at time t = 0 (phase 0, t = 0 to t1), and is then cleared by the astrocyte (blue) (phase 1, t1 to t2). K<sup>+</sup> levels are illustrated for the different regimes in each compartment (<b><i>A</i>,<i>D</i>,<i>G</i></b>) and are normalized to basal [K<sup>+</sup>]<sub>o</sub> (<b><i>B</i>,<i>E</i>,<i>H</i></b>) or to the total amount of released K<sup>+</sup> by neurons (<b><i>C</i>,<i>F</i>,<i>I</i></b>). Finally, the buffered K<sup>+</sup> is slowly redistributed back to neurons, which ends the <b>K</b><sup>+</sup> cycle (phase 2, t2 to end). t1 represents the time point where neuronal release of K<sup>+</sup> stops, whereas t2 is the time point where astroglial K<sup>+</sup> uptake peaks.</p>", "links"=>[], "tags"=>["hippocampal astrocytes", "tetanic stimulations", "Action potentials", "extracellular potassium homeostasis", "basal extracellular potassium levels", "potassium fluxes", "potassium ions", "moment neurotransmission", "astrocytes buffer", "potassium levels", "10 Hz", "membrane depolarization", "potassium homeostasis", "Kir 4.1 channels", "epileptiform activity", "astroglial Kir 4.1 channels", "potassium dynamics", "Neuroglial Potassium Cycle", "Brownian noise", "Extracellular space", "extracellular potassium clearance", "Kir 4.1 Channels Neuronal excitability", "9 seconds"], "article_id"=>1363426, "categories"=>["Uncategorised"], "users"=>["Jérémie Sibille", "Khanh Dao Duc", "David Holcman", "Nathalie Rouach"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1004137.g003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_potassium_cycle_between_neuronal_astroglial_and_extracellular_space_compartments_during_basal_and_trains_of_stimulations_/1363426", "title"=>"The potassium cycle between neuronal, astroglial and extracellular space compartments during basal and trains of stimulations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-31 04:01:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/2000473"], "description"=>"<p><b><i>A-E</i></b>, To induce probabilistic firing, a periodic sub-firing 5 Hz stimulation (5 ms squared stimulus) was set as the input of our tri-compartment model (<b><i>A</i></b>). Moreover, a Brownian source of amplitude <b>σ</b> = <b>0.68 <i>pA</i></b><sup><b>2</b></sup><b>.<i>ms</i></b><sup><b>-1</b></sup> was added to induce a neuronal membrane potential noise of 1 mV amplitude (Inset in <b><i>B</i></b>). Corresponding neuronal firing (<b><i>B</i></b>), [K<sup>+</sup>]<sub>o</sub> (<b><i>C</i></b>) and estimated firing probability (number of action potentials (AP) per second/stimulation frequency) obtained by one simulation (<b><i>D</i></b>) are illustrated below for a 5 Hz stimulation during 15 seconds. <b><i>E</i></b>, Quantification of the average firing probability computed over 100 numerical simulations for 5 Hz stimulation during 15 seconds in control condition. <b><i>F-K</i></b>, Same quantification over time as in (<b><i>E</i></b>) in control (Ctrl, blue) and inhibited K<sub>ir</sub>4.1 channel (light blue) conditions illustrated for 0.1 Hz (<b><i>F</i></b>), 1 Hz (<b><i>G</i></b>), 3 Hz (<b><i>H</i></b>), 5 Hz (<b><i>I</i></b>), 10 Hz (<b><i>J</i></b>) and 50 Hz (<b><i>K</i></b>) stimulations.</p>", "links"=>[], "tags"=>["hippocampal astrocytes", "tetanic stimulations", "Action potentials", "extracellular potassium homeostasis", "basal extracellular potassium levels", "potassium fluxes", "potassium ions", "moment neurotransmission", "astrocytes buffer", "potassium levels", "10 Hz", "membrane depolarization", "potassium homeostasis", "Kir 4.1 channels", "epileptiform activity", "astroglial Kir 4.1 channels", "potassium dynamics", "Neuroglial Potassium Cycle", "Brownian noise", "Extracellular space", "extracellular potassium clearance", "Kir 4.1 Channels Neuronal excitability", "9 seconds"], "article_id"=>1363429, "categories"=>["Uncategorised"], "users"=>["Jérémie Sibille", "Khanh Dao Duc", "David Holcman", "Nathalie Rouach"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1004137.g005", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Involvement_of_K_ir_4_1_channels_in_firing_probability_induced_by_Brownian_noise_and_sub_firing_stimulation_/1363429", "title"=>"Involvement of K<sub>ir</sub>4.1 channels in firing probability induced by Brownian noise and sub-firing stimulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-31 04:01:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/2000469"], "description"=>"<div><p>comparison of simulations and experiments <b><i>A</i>,<i>E</i>,<i>I</i></b>, Numerical simulation of the applied current (I<sub><i>app</i></sub>, blue) induced by single (<b><i>A</i></b>), tetanic (100 Hz, 1 s) (<b><i>E</i></b>) and repetitive (10 Hz, 30 s) (<b><i>I</i></b>) stimulations generated by the depression-facilitation model with inputs <b><i>f(t)</i> = <i>f<sub>S</sub>(t)</i></b> (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1004137#pcbi.1004137.e010\" target=\"_blank\">Equation 4</a>), <b><i>f(t)</i> = <i>f<sub>TT</sub>(t)</i></b> (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1004137#pcbi.1004137.e010\" target=\"_blank\">Equation 5</a>) and <b><i>f(t)</i> = <i>f<sub>RS</sub>(t)</i></b> (<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1004137#pcbi.1004137.e010\" target=\"_blank\">Equation 6</a>), respectively. <i>B</i>,<i>F</i>,<i>J</i>, Representative electrophysiological recordings of synaptic transmission (field excitatory postsynaptic potential, fEPSP, black) induced by single (<b><i>B</i></b>), tetanic (100 Hz, 1 s) (<b><i>F</i></b>) and repetitive (10 Hz, 30 s) (<b><i>J</i></b>) stimulations of Schaffer collaterals in acute hippocampal slices.</p>\n<p>Inset in panel B is a magnification of the simulated applied current (I<sub><i>app</i></sub>) illustrated in (<b><i>A</i></b>) and the corresponding experimental field excitatory postsynaptic potential (fEPSP) shown in (<b><i>B</i></b>). <b><i>C</i>, <i>G</i>, <i>K</i></b>, Superimposition of astrocytic membrane potential dynamics obtained by electrophysiological recordings (black) and numerical simulations (blue) generated by <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1004137#pcbi.1004137.e029\" target=\"_blank\">equation 23</a> during single (<b><i>C</i></b>), tetanic (<b><i>G</i></b>) and repetitive stimulations (<b><i>K</i></b>). Inset in panel C is a magnification of the simulated and experimentally recorded astrocytic membrane potentials <b><i>D</i>,<i>H</i>,<i>L</i></b>, Quantification of astrocytic membrane potential kinetics extracted from experimental data (black) and numerical simulations (blue). The rise and decay times are computed between 20% and 80% of the maximal peak amplitude response.</p></div>", "links"=>[], "tags"=>["hippocampal astrocytes", "tetanic stimulations", "Action potentials", "extracellular potassium homeostasis", "basal extracellular potassium levels", "potassium fluxes", "potassium ions", "moment neurotransmission", "astrocytes buffer", "potassium levels", "10 Hz", "membrane depolarization", "potassium homeostasis", "Kir 4.1 channels", "epileptiform activity", "astroglial Kir 4.1 channels", "potassium dynamics", "Neuroglial Potassium Cycle", "Brownian noise", "Extracellular space", "extracellular potassium clearance", "Kir 4.1 Channels Neuronal excitability", "9 seconds"], "article_id"=>1363425, "categories"=>["Uncategorised"], "users"=>["Jérémie Sibille", "Khanh Dao Duc", "David Holcman", "Nathalie Rouach"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1004137.g002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dynamics_of_astroglial_membrane_potential_induced_by_single_tetanic_and_repetitive_stimulations_/1363425", "title"=>"Dynamics of astroglial membrane potential induced by single, tetanic and repetitive stimulations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-31 04:01:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/2000467"], "description"=>"<p>A, Schematic representation of the tri-compartment model: neuronal activity induces the release of K<sup>+</sup> in the extracellular space, which is taken up by astrocytes. B, Reduction of the tri-compartment model to ionic fluxes exchanges between a generic postsynaptic neuron, astrocyte and extracellular space. The model includes channels and pumps carrying K<sup>+</sup> and Na<sup>+</sup> ions. C, Current-Voltage relationship (I-V curve) of K<sub>ir</sub>4.1 channels. We identify the free parameters in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1004137#pcbi.1004137.e028\" target=\"_blank\">equation 22</a> by fitting the simulated IV curve (light blue) to experimental recordings performed in isolated astrocytes (sampling data, black rectangles) [<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1004137#pcbi.1004137.ref065\" target=\"_blank\">65</a>]. Using <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1004137#pcbi.1004137.e028\" target=\"_blank\">equation 22</a>, we plot the I-V curve for different ratios of extracellular to intracellular astrocytic K<sup>+</sup> concentrations (2.5/135 (light blue), 5/135 (blue) and 10/135 (dark blue). At resting membrane potential (-80 mV) and resting [K<sup>+</sup>]<sub>o</sub> (2.5 mM), the K<sub>ir</sub>4.1 current is outward, but as illustrated here, it reverses by increasing [K<sup>+</sup>]<sub>o</sub>.</p>", "links"=>[], "tags"=>["hippocampal astrocytes", "tetanic stimulations", "Action potentials", "extracellular potassium homeostasis", "basal extracellular potassium levels", "potassium fluxes", "potassium ions", "moment neurotransmission", "astrocytes buffer", "potassium levels", "10 Hz", "membrane depolarization", "potassium homeostasis", "Kir 4.1 channels", "epileptiform activity", "astroglial Kir 4.1 channels", "potassium dynamics", "Neuroglial Potassium Cycle", "Brownian noise", "Extracellular space", "extracellular potassium clearance", "Kir 4.1 Channels Neuronal excitability", "9 seconds"], "article_id"=>1363423, "categories"=>["Uncategorised"], "users"=>["Jérémie Sibille", "Khanh Dao Duc", "David Holcman", "Nathalie Rouach"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1004137.g001", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tri_compartment_model_of_the_potassium_cycle_between_the_neuron_the_extracellular_space_and_the_astrocyte_/1363423", "title"=>"Tri-compartment model of the potassium cycle between the neuron, the extracellular space and the astrocyte.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-31 04:01:54"}

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  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"17", "full-text"=>"17", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
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  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"15", "full-text"=>"15", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"14", "full-text"=>"14", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"24", "full-text"=>"31", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"24", "full-text"=>"28", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"21", "full-text"=>"27", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"23", "full-text"=>"25", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"151", "full-text"=>"167", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"169", "full-text"=>"187", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"61", "full-text"=>"59", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"50", "full-text"=>"48", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"54", "full-text"=>"60", "pdf"=>"10", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"110", "full-text"=>"114", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"74", "full-text"=>"81", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"39", "full-text"=>"41", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"40", "full-text"=>"42", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"48", "full-text"=>"52", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"118", "full-text"=>"127", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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