Chemoreception Regulates Chemical Access to Mouse Vomeronasal Organ: Role of Solitary Chemosensory Cells
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{"title"=>"Chemoreception regulates chemical access to mouse vomeronasal organ: Role of solitary chemosensory cells", "type"=>"journal", "authors"=>[{"first_name"=>"Tatsuya", "last_name"=>"Ogura", "scopus_author_id"=>"7402985464"}, {"first_name"=>"Kurt", "last_name"=>"Krosnowski", "scopus_author_id"=>"36608254100"}, {"first_name"=>"Lana", "last_name"=>"Zhang", "scopus_author_id"=>"36609730300"}, {"first_name"=>"Mikhael", "last_name"=>"Bekkerman", "scopus_author_id"=>"36607398100"}, {"first_name"=>"Weihong", "last_name"=>"Lin", "scopus_author_id"=>"7406520379"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-77955630273", "pui"=>"359358276", "doi"=>"10.1371/journal.pone.0011924", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"77955630273", "pmid"=>"20689832"}, "id"=>"ed70015e-6889-3fe3-9770-60756ea87fa0", "abstract"=>"Controlling stimulus access to sensory organs allows animals to optimize sensory reception and prevent damage. The vomeronasal organ (VNO) detects pheromones and other semiochemicals to regulate innate social and sexual behaviors. This semiochemical detection generally requires the VNO to draw in chemical fluids, such as bodily secretions, which are complex in composition and can be contaminated. Little is known about whether and how chemical constituents are monitored to regulate the fluid access to the VNO. Using transgenic mice and immunolabeling, we found that solitary chemosensory cells (SCCs) reside densely at the entrance duct of the VNO. In this region, most of the intraepithelial trigeminal fibers innervate the SCCs, indicating that SCCs relay sensory information onto the trigeminal fibers. These SCCs express transient receptor potential channel M5 (TRPM5) and the phospholipase C (PLC) b2 signaling pathway. Additionally, the SCCs express choline acetyltransferase (ChAT) and vesicular acetylcholine transporter (VAChT) for synthesizing and packaging acetylcholine, a potential transmitter. In intracellular Ca 2+ imaging, the SCCs responded to various chemical stimuli including high concentrations of odorants and bitter compounds. The responses were suppressed significantly by a PLC inhibitor, suggesting involvement of the PLC pathway. Further, we developed a quantitative dye assay to show that the amount of stimulus fluid that entered the VNOs of behaving mice is inversely correlated to the concentration of odorous and bitter substances in the fluid. Genetic knockout and pharmacological inhibition of TRPM5 resulted in larger amounts of bitter compounds entering the VNOs. Our data uncovered that chemoreception of fluid constituents regulates chemical access to the VNO and plays an important role in limiting the access of non-specific irritating and harmful substances. Our results also provide new insight into the emerging role of SCCs in chemoreception and regulation of physiological actions.", "link"=>"http://www.mendeley.com/research/chemoreception-regulates-chemical-access-mouse-vomeronasal-organ-role-solitary-chemosensory-cells", "reader_count"=>41, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>6, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>2, "Student > Master"=>9, "Other"=>1, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>6, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>2, "Student > Master"=>9, "Other"=>1, "Student > Bachelor"=>2, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>27, "Medicine and Dentistry"=>1, "Neuroscience"=>4, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>4}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>27}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>2, "United Kingdom"=>1, "Germany"=>2, "Spain"=>1}, "group_count"=>0}

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  • {"files"=>["https://ndownloader.figshare.com/files/417434", "https://ndownloader.figshare.com/files/417451", "https://ndownloader.figshare.com/files/417467"], "description"=>"<div><p>Controlling stimulus access to sensory organs allows animals to optimize sensory reception and prevent damage. The vomeronasal organ (VNO) detects pheromones and other semiochemicals to regulate innate social and sexual behaviors. This semiochemical detection generally requires the VNO to draw in chemical fluids, such as bodily secretions, which are complex in composition and can be contaminated. Little is known about whether and how chemical constituents are monitored to regulate the fluid access to the VNO. Using transgenic mice and immunolabeling, we found that solitary chemosensory cells (SCCs) reside densely at the entrance duct of the VNO. In this region, most of the intraepithelial trigeminal fibers innervate the SCCs, indicating that SCCs relay sensory information onto the trigeminal fibers. These SCCs express transient receptor potential channel M5 (TRPM5) and the phospholipase C (PLC) β2 signaling pathway. Additionally, the SCCs express choline acetyltransferase (ChAT) and vesicular acetylcholine transporter (VAChT) for synthesizing and packaging acetylcholine, a potential transmitter. In intracellular Ca<sup>2+</sup> imaging, the SCCs responded to various chemical stimuli including high concentrations of odorants and bitter compounds. The responses were suppressed significantly by a PLC inhibitor, suggesting involvement of the PLC pathway. Further, we developed a quantitative dye assay to show that the amount of stimulus fluid that entered the VNOs of behaving mice is inversely correlated to the concentration of odorous and bitter substances in the fluid. Genetic knockout and pharmacological inhibition of TRPM5 resulted in larger amounts of bitter compounds entering the VNOs. Our data uncovered that chemoreception of fluid constituents regulates chemical access to the VNO and plays an important role in limiting the access of non-specific irritating and harmful substances. Our results also provide new insight into the emerging role of SCCs in chemoreception and regulation of physiological actions.</p></div>", "links"=>[], "tags"=>["chemoreception", "regulates", "vomeronasal", "solitary", "chemosensory", "cells"], "article_id"=>142400, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Tatsuya Ogura", "Kurt Krosnowski", "Lana Zhang", "Mikhael Bekkerman", "Weihong Lin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0011924.s001", "https://dx.doi.org/10.1371/journal.pone.0011924.s002", "https://dx.doi.org/10.1371/journal.pone.0011924.s003"], "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Chemoreception_Regulates_Chemical_Access_to_Mouse_Vomeronasal_Organ_Role_of_Solitary_Chemosensory_Cells/142400", "title"=>"Chemoreception Regulates Chemical Access to Mouse Vomeronasal Organ: Role of Solitary Chemosensory Cells", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-07-30 00:40:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/837684"], "description"=>"<p>A: Confocal image of a VNO epithelial strip from a TRPM5-GFP mouse, showing both PGP 9.5-labeled trigeminal nerve bundles (asterisks) at basal lamina and many fine intraepithelial fibers. Arrowheads point to varicosities found typically in peptidergic fibers. Arrow points to a branching nerve fiber. B: The GFP-fluorescence image overlaid with (A). All TRPM5-expressing SCCs are apposed or wrapped closely by one or a few intraepithelial nerve fibers. Arrows point to apexes of SCCs. C: immunolabeling of substance P in a section of the anterior non-sensory epithelium. Note that most of the labeled intraepithelial fibers appear to innervate SCCs. D: Percentages of intraepithelial fibers innervating SCCs. E and F: Confocal images of TRPM5-expressing SCCs (green) immunoreacted to antibodies against the ChAT and VAChT respectively (red). G: Whole-mount fluorescence image of the ChAT (GFP)-expressing cells taken from a VNO entrance duct of a ChAT(BAC)-eGFP mouse. H: CHAT (GFP)-expressing cells of the VNO immunolabeled by the anti-α-gustducin antibody (red). Scales: B, F, G, and H, 10 µm; C, 50 µm; E, 20 µm.</p>", "links"=>[], "tags"=>["innervation", "immuno-expression", "chat", "vacht", "ach", "synthesis", "packaging"], "article_id"=>508047, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Tatsuya Ogura", "Kurt Krosnowski", "Lana Zhang", "Mikhael Bekkerman", "Weihong Lin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011924.g002", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Trigeminal_innervation_and_immuno_expression_of_ChaT_and_VAChT_for_ACh_synthesis_and_packaging_in_SCCs_/508047", "title"=>"Trigeminal innervation and immuno-expression of ChaT and VAChT for ACh synthesis and packaging in SCCs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-30 02:14:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/837589"], "description"=>"<p>A: A schematic drawing of a mouse hemi-nose. MOE: main olfactory epithelium; OB: olfactory bulb. VNO: vomeronasal organ (blue). B: Luminal view of the entire non-sensory epithelium and entrance duct of a VNO from a TRPM5-GFP mouse. Bright spots are GFP-positive SCCs. Arrow points to the anterior opening. Anterior to the VNO, the cartilaginous stenonii canal channels external fluids to the VNO opening. C: Plot of SCC density at different regions as determined from horizontal VNO sections of four mice (Mean ± SEM), showing that the GFP-expressing SCCs preferentially reside at the entrance duct and adjacent 0.5 mm long anterior non-sensory epithelium. D: Confocal image of a typical GFP-expressing SCC. Arrowhead points to an apical microvillus. E: Immunolabeling of TRPM5 (red) in GFP-expressing cells (green) in a VNO section. F: Image taken from an epithelial strip from the entrance duct, showing that TRPM5 (GFP) expressing SCCs immunoreacted to an anti-α-gustducin antibody (red). Scales: B, 0.5 mm; D, 5 µm; E and F, 20 µm.</p>", "links"=>[], "tags"=>["preferentially", "duct", "vno", "chemosensory", "signaling"], "article_id"=>507952, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Tatsuya Ogura", "Kurt Krosnowski", "Lana Zhang", "Mikhael Bekkerman", "Weihong Lin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011924.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SCCs_preferentially_locate_at_the_entrance_duct_of_the_VNO_and_express_chemosensory_signaling_components_/507952", "title"=>"SCCs preferentially locate at the entrance duct of the VNO and express chemosensory signaling components.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-30 02:12:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/838040"], "description"=>"<p>The vomeronasal sensory neurons (VSN), which detect semiochemicals, are sequestered in the VNO, requiring chemical fluids to be drawn into the vomeronasal lumen via the anterior opening and entrance duct. SCCs reside densely at the entrance duct and detect odorous irritants and harmful substances in the stimulus fluids. Signal transduction in SCCs primarily involves the PLC signaling pathway, in which activation of PLC results in either an increase in intracellular Ca<sup>2+</sup> levels via the internal Ca<sup>2+</sup> stores, leading to activation of TRPM5 or activation of unknown effectors. PLC-independent pathway may also be involved in chemical responses. For sensory transduction of bitter compounds, the increase in intracellular Ca<sup>2+</sup> opens TRPM5 ion channels. Activation of SCCs leads to release of ACh, a potential transmitter onto the trigeminal nerve fibers and consequently regulating the access of chemical fluids.</p>", "links"=>[], "tags"=>["sensory", "regulating"], "article_id"=>508413, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Tatsuya Ogura", "Kurt Krosnowski", "Lana Zhang", "Mikhael Bekkerman", "Weihong Lin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011924.g006", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_view_of_a_novel_sensory_mechanism_regulating_chemical_access_to_the_VNO_/508413", "title"=>"Schematic view of a novel sensory mechanism regulating chemical access to the VNO.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-30 02:20:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/837767"], "description"=>"<p>A: Representative traces from three isolated SCCs responding to various stimuli with increases in intracellular Ca<sup>2+</sup> levels. Odorous stimuli, 0.5 mM or otherwise indicated. Mouse urine (1∶100 dilution). Horizontal bars indicate stimulation periods. Note stimulus- and concentration-dependence of the response amplitudes. Ethanol (EtOH, 0.5%): solvent for menthol, cold: 4°C saline. B: Percentage of SCCs responding to odorous stimuli (n = 4 to 22). C: Concentration-dependent responses to lilial. Each SCC was challenged by lilial from 0.025 to 0.5 mM. The responses were normalized to the peak response value of 0.5 mM (n = 4, mean ± SEM). Inset, response traces of lilial at two different concentrations. D: Typical intracellular Ca<sup>2+</sup> response traces to bitter-tasting compounds. DN: denatonium benzoate. E: Percentage of responding SCCs to bitter stimuli (n = 8 to 13). F: Concentration-dependent responses to denatonium (1, 3, 10 mM). The responses were normalized to the peak response value of 10 mM (n = 7, mean ± SEM). Inset, response traces of denatonium at three different concentrations. Vertical scales in A, C, D and F indicate percent changes from the resting Ca<sup>2+</sup> levels.</p>", "links"=>[], "tags"=>["stimuli-induced", "changes", "intracellular"], "article_id"=>508139, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Tatsuya Ogura", "Kurt Krosnowski", "Lana Zhang", "Mikhael Bekkerman", "Weihong Lin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011924.g003", "stats"=>{"downloads"=>0, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chemical_stimuli_induced_changes_in_intracellular_Ca_2_in_isolated_SCCs_/508139", "title"=>"Chemical stimuli-induced changes in intracellular Ca<sup>2<b>+</b></sup> in isolated SCCs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-30 02:15:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/837861"], "description"=>"<p>A and B: SCCs (green) of the VNO immunoreacted to antibodies against G-protein γ13 and PLCβ2 (red) respectively. Scales: 10 µm. C: The PLC inhibitor U73122 (5 µM), but not the negative control U73343 (5 µM), suppressed the denatonium (3 mM)-induced Ca<sup>2+</sup> increase. D: Summary of the inhibition. The concentration of denatonium and lilial were 3 mM and 0.5 mM respectively. The peak responses of single SCC obtained in the presence of U73122 or U73343 were normalized to the control responses. The U73122 inhibition of responses to denatonium and lilial was statistically significant as compared to the controls (marked by the asterisks; n = 9 for denatonium, 7 for lilial, and 4 for 0 Ca<sup>2+</sup> lilial).</p>", "links"=>[], "tags"=>["plc", "signaling"], "article_id"=>508229, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Tatsuya Ogura", "Kurt Krosnowski", "Lana Zhang", "Mikhael Bekkerman", "Weihong Lin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011924.g004", "stats"=>{"downloads"=>2, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Involvement_of_the_PLC_signaling_pathway_/508229", "title"=>"Involvement of the PLC signaling pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-30 02:17:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/837945"], "description"=>"<p>A: A representative fluorescence image of a hemi-nose taken after the dye assay, showing rhodamine fluorescence in the VNO and anterior nasal mucosa. Scale: 1mm. B, C, D, and E: Plots of averaged fluorescence intensity values in VNOs measured after the mixture applications (mean ± SEM). N = 5 to 14 animals for each group. Single asterisk: statistically significant as compared to the value of the lowest concentration of the same stimulus (B, C, and D) or to the control value (E). B: Applications of natural complex stimuli, synthetic pheromones and NaCl of 0.1 and 2M. C: Odorous stimuli applied at different concentrations, showing negative correlation between the intensity values and concentrations. Note very limited access of the dye-mixtures of capsaicin and mustard oil. These stimuli are known to directly stimulate trigeminal free nerve endings at the nostrils. D: Application of bitter-tasting stimuli. Denatonium (DN) was tested at three different concentrations, showing concentration-dependent mixture access. Note the significant differences between the WT and TRPM5 KO mice in the access of the bitter compounds at high concentrations (double asterisks). E: Changes in chemical access induced by local pharmacological inhibition of PLC and TRPM5. PLC inhibitor U73122 (10 µM) or TRPM5 inhibitor Ph<sub>3</sub>PO (100 µM) was applied to the VNOs using the delivery method in the dye assay. Inhibition of either PLC or TRPM5 significantly increased the access of bitter compounds to the VNOs in wild type animals. The access of dye-lilial mixture in both wild type and TRPM5 knockout mice was increased after U73122 treatment.</p>", "links"=>[], "tags"=>["vnos", "trpm5", "knockout"], "article_id"=>508307, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Tatsuya Ogura", "Kurt Krosnowski", "Lana Zhang", "Mikhael Bekkerman", "Weihong Lin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011924.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chemical_access_to_the_VNOs_of_wild_type_and_TRPM5_knockout_mice_/508307", "title"=>"Chemical access to the VNOs of wild type and TRPM5 knockout mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-30 02:18:27"}

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  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
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  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
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  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
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  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
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  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
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  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
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  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
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  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
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  • {"unique-ip"=>"15", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"17", "full-text"=>"16", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"11", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
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  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"1", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"11"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2021", "month"=>"1"}
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Relative Metric

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