Variation in the Large-Scale Organization of Gene Expression Levels in the Hippocampus Relates to Stable Epigenetic Variability in Behavior
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{"title"=>"Variation in the large-scale organization of gene expression levels in the hippocampus relates to stable epigenetic variability in behavior", "type"=>"journal", "authors"=>[{"first_name"=>"Mark D.", "last_name"=>"Alter", "scopus_author_id"=>"7103262211"}, {"first_name"=>"Daniel B.", "last_name"=>"Rubin", "scopus_author_id"=>"36986490600"}, {"first_name"=>"Keri", "last_name"=>"Ramsey", "scopus_author_id"=>"57201541885"}, {"first_name"=>"Rebecca", "last_name"=>"Halpern", "scopus_author_id"=>"25227696700"}, {"first_name"=>"Dietrich A.", "last_name"=>"Stephan", "scopus_author_id"=>"35238808400"}, {"first_name"=>"L. F.", "last_name"=>"Abbott", "scopus_author_id"=>"24517161100"}, {"first_name"=>"Rene", "last_name"=>"Hen", "scopus_author_id"=>"7005852886"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pui"=>"352493523", "sgr"=>"53749104645", "doi"=>"10.1371/journal.pone.0003344", "scopus"=>"2-s2.0-53749104645", "pmid"=>"18836535"}, "id"=>"8ffc8390-817f-3d1a-8f6e-efb06b83669b", "abstract"=>"BACKGROUND: Despite sharing the same genes, identical twins demonstrate substantial variability in behavioral traits and in their risk for disease. Epigenetic factors-DNA and chromatin modifications that affect levels of gene expression without affecting the DNA sequence-are thought to be important in establishing this variability. Epigenetically-mediated differences in the levels of gene expression that are associated with individual variability traditionally are thought to occur only in a gene-specific manner. We challenge this idea by exploring the large-scale organizational patterns of gene expression in an epigenetic model of behavioral variability.\\n\\nMETHODOLOGY/FINDINGS: To study the effects of epigenetic influences on behavioral variability, we examine gene expression in genetically identical mice. Using a novel approach to microarray analysis, we show that variability in the large-scale organization of gene expression levels, rather than differences in the expression levels of specific genes, is associated with individual differences in behavior. Specifically, increased activity in the open field is associated with increased variance of log-transformed measures of gene expression in the hippocampus, a brain region involved in open field activity. Early life experience that increases adult activity in the open field also similarly modifies the variance of gene expression levels. The same association of the variance of gene expression levels with behavioral variability is found with levels of gene expression in the hippocampus of genetically heterogeneous outbred populations of mice, suggesting that variation in the large-scale organization of gene expression levels may also be relevant to phenotypic differences in outbred populations such as humans. We find that the increased variance in gene expression levels is attributable to an increasing separation of several large, log-normally distributed families of gene expression levels. We also show that the presence of these multiple log-normal distributions of gene expression levels is a universal characteristic of gene expression in eurkaryotes. We use data from the MicroArray Quality Control Project (MAQC) to demonstrate that our method is robust and that it reliably detects biological differences in the large-scale organization of gene expression levels.\\n\\nCONCLUSIONS: Our results contrast with the traditional belief that epigenetic effects on gene expression occur only at the level of specific genes and suggest instead that the large-scale organization of gene expression levels provides important insights into the relationship of gene expression with behavioral variability. Understanding the epigenetic, genetic, and environmental factors that regulate the large-scale organization of gene expression levels, and how changes in this large-scale organization influences brain development and behavior will be a major future challenge in the field of behavioral genomics.", "link"=>"http://www.mendeley.com/research/variation-largescale-organization-gene-expression-levels-hippocampus-relates-stable-epigenetic-varia", "reader_count"=>66, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>9, "Librarian"=>1, "Researcher"=>23, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>4, "Other"=>4, "Student > Master"=>2, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>10}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>9, "Librarian"=>1, "Researcher"=>23, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>4, "Other"=>4, "Student > Master"=>2, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>10}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>46, "Medicine and Dentistry"=>5, "Neuroscience"=>6, "Psychology"=>3, "Social Sciences"=>1, "Computer Science"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Neuroscience"=>{"Neuroscience"=>6}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>46}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>4, "Japan"=>2, "Brazil"=>2, "Italy"=>1, "France"=>1, "Germany"=>1, "India"=>1}, "group_count"=>5}

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/919579"], "description"=>"<p>Postnatal handling resulted in an increased variance of log-transformed gene expression levels in the same direction and magnitude as in high activity mice. Changes in gene expression organization were accompanied by increased activity in the open field (supplemental <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003344#pone.0003344.s002\" target=\"_blank\">figure S2</a>) and increased activity in the light compartment in the light-dark paradigm (supplemental <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003344#pone.0003344.s003\" target=\"_blank\">figure S3</a>).</p>", "links"=>[], "tags"=>["log-transformed", "levels", "ca1", "hippocampus", "affected", "postnatal"], "article_id"=>590029, "categories"=>["Genetics", "Neuroscience"], "users"=>["Mark D. Alter", "Daniel B. Rubin", "Keri Ramsey", "Rebecca Halpern", "Dietrich A. Stephan", "L. F. Abbott", "Rene Hen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003344.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Variance_of_log_transformed_gene_expression_levels_in_the_CA1_of_the_hippocampus_is_affected_by_postnatal_handling_/590029", "title"=>"Variance of log-transformed gene expression levels in the CA1 of the hippocampus is affected by postnatal handling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-10-06 00:00:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/919742"], "description"=>"<p>We find, in all cases where variance is increased, that a corresponding increase in the distance between log-normal distributions is present. The distance is measured between peaks in natural logs. We present the data normalized to the less active group of animals and converted into linear fold change of expression levels. For example, if the distance between the high and low expression groups of genes was 1 natural log greater in more active animals, then the difference would be the natural exponent taken to the power of 1 or 2.718. This would mean that when compared to the low expression group of genes that the high expression group of genes is up-regulated on average 2.718-fold. Significant differences in separation were found between the low and middle, middle and high, and high and low distributions in all cases. Importantly, significant differences in separation of distributions were found in the hippocampus but not in the amygdala between high and low freezing mice. This is consistent with the findings for the variance (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003344#pone-0003344-g003\" target=\"_blank\">figure 3</a>).</p>", "links"=>[], "tags"=>["variance", "mice", "relates", "moving", "log-normal"], "article_id"=>590190, "categories"=>["Genetics", "Neuroscience"], "users"=>["Mark D. Alter", "Daniel B. Rubin", "Keri Ramsey", "Rebecca Halpern", "Dietrich A. Stephan", "L. F. Abbott", "Rene Hen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003344.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_variance_in_gene_expression_in_more_active_mice_relates_to_a_moving_apart_of_log_normal_distributions_/590190", "title"=>"Increased variance in gene expression in more active mice relates to a moving apart of log-normal distributions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-10-06 00:03:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/919638"], "description"=>"<p>Gene expression data was downloaded from the Gene Expression Omnibus public repository (GSE4034 & GSE4035 (supplemental <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003344#pone.0003344.s004\" target=\"_blank\">figure S4</a>)). Mice for these experiments were selected over multiple generations after an inter-strain cross of a high anxiety (DBA or A/J) and low anxiety (C57/B6) strain of mice. We found that variance of log-transformed gene expression levels in the hippocampus but not amygdala was significantly increased in low freezing mice. In this study low freezing mice were found to have increased activity in the open-field similar to high activity and handled mice <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003344#pone.0003344-Ponder1\" target=\"_blank\">[14]</a>.</p>", "links"=>[], "tags"=>["log-transformed", "levels", "hippocampus", "amygdala", "contextual", "genetically", "heterogeneous"], "article_id"=>590082, "categories"=>["Genetics", "Neuroscience"], "users"=>["Mark D. Alter", "Daniel B. Rubin", "Keri Ramsey", "Rebecca Halpern", "Dietrich A. Stephan", "L. F. Abbott", "Rene Hen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003344.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Variance_of_log_transformed_gene_expression_levels_in_the_hippocampus_but_not_the_amygdala_is_associated_with_contextual_fear_and_present_in_genetically_heterogeneous_mice_/590082", "title"=>"Variance of log-transformed gene expression levels in the hippocampus but not the amygdala is associated with contextual fear and present in genetically heterogeneous mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-10-06 00:01:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/919903"], "description"=>"<p>To validate our approach to microarray analysis, we analyzed an independent publicly available dataset from the MicroArray Quality Control Project. Here two commercially available samples (Sample A = Stratagene Universal Human Reference RNA (UHRR, Catalog #740000), Sample B = Ambion Human Brain Reference RNA (HBRR, Catalog #6050)) were sent to six independent testing sites that ran 5 technical replicates for each sample. At all testing sites sample A had a greater variance of log-transformed gene expression levels than sample B. In all cases this was accompanied by a moving apart of gene expression distributions. A strongly significant effect of testing site on all measurements was also present. The effects of sample and site did not interact.</p>", "links"=>[], "tags"=>["differences", "patterns", "robustly"], "article_id"=>590352, "categories"=>["Genetics", "Neuroscience"], "users"=>["Mark D. Alter", "Daniel B. Rubin", "Keri Ramsey", "Rebecca Halpern", "Dietrich A. Stephan", "L. F. Abbott", "Rene Hen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003344.g007", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Global_differences_in_gene_expression_patterns_are_robustly_detected_at_multiple_testing_sites_/590352", "title"=>"Global differences in gene expression patterns are robustly detected at multiple testing sites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-10-06 00:05:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/919521"], "description"=>"<p>Gene expression was log-transformed to reduce normally distributed noise and because of a recognized skewing of gene expression data to low expression values. Variance of log-transformed gene expression levels was significantly increased in mice selected for stable high activity in the open field.</p>", "links"=>[], "tags"=>["log-transformed", "levels", "hippocampus", "differences"], "article_id"=>589966, "categories"=>["Genetics", "Neuroscience"], "users"=>["Mark D. Alter", "Daniel B. Rubin", "Keri Ramsey", "Rebecca Halpern", "Dietrich A. Stephan", "L. F. Abbott", "Rene Hen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003344.g001", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Variance_of_log_transformed_gene_expression_levels_in_the_hippocampus_is_associated_with_individual_differences_in_activity_in_the_open_field_/589966", "title"=>"Variance of log-transformed gene expression levels in the hippocampus is associated with individual differences in activity in the open field.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-10-06 02:46:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/919687"], "description"=>"<p>We found that the distribution log-transformed gene expression levels can be described by three log-normal curves. Three normal distributions were fit to log-transformed Affymetrix micro-array data that was processed and summarized using MAS 5.0. The fit error in all cases was minimal and could not be improved significantly by adding additional log-normal curves, whereas trying to fit data to one or two log-normal distributions significantly increased error. Matlab fitting algorithms perform well across a wide range of distribution patterns (supplemental <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003344#pone.0003344.s006\" target=\"_blank\">figure S6</a>).</p>", "links"=>[], "tags"=>["log-normal"], "article_id"=>590140, "categories"=>["Genetics", "Neuroscience"], "users"=>["Mark D. Alter", "Daniel B. Rubin", "Keri Ramsey", "Rebecca Halpern", "Dietrich A. Stephan", "L. F. Abbott", "Rene Hen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003344.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Global_gene_expression_is_described_by_three_log_normal_distributions_/590140", "title"=>"Global gene expression is described by three log-normal distributions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-10-06 00:02:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/919865"], "description"=>"<p>Data sets from S. cerviciae (GSE4135), C. elegans (GSE8004), and humans (GSE8853) were examined. The distribution of log-transformed gene expression levels was described by 3-log-normal distributions in all species examined (A–D). A human sample was examined with RNAseq. Approximately 23 thousand unique tags produced 17 million sequences. The distribution of log-transformed sequence tag counts was fit by 3-log normal distributions (E).</p>", "links"=>[], "tags"=>["log-normal", "distributions"], "article_id"=>590318, "categories"=>["Genetics", "Neuroscience"], "users"=>["Mark D. Alter", "Daniel B. Rubin", "Keri Ramsey", "Rebecca Halpern", "Dietrich A. Stephan", "L. F. Abbott", "Rene Hen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003344.g006", "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_presence_of_3_log_normal_gene_expression_distributions_is_a_universal_feature_of_gene_expression_in_eukaryots_/590318", "title"=>"The presence of 3 log-normal gene expression distributions is a universal feature of gene expression in eukaryots.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-10-06 00:05:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/455895", "https://ndownloader.figshare.com/files/456199", "https://ndownloader.figshare.com/files/456418", "https://ndownloader.figshare.com/files/456610", "https://ndownloader.figshare.com/files/456857", "https://ndownloader.figshare.com/files/457121"], "description"=>"<div><h3>Background</h3><p>Despite sharing the same genes, identical twins demonstrate substantial variability in behavioral traits and in their risk for disease. Epigenetic factors–DNA and chromatin modifications that affect levels of gene expression without affecting the DNA sequence–are thought to be important in establishing this variability. Epigenetically-mediated differences in the levels of gene expression that are associated with individual variability traditionally are thought to occur only in a gene-specific manner. We challenge this idea by exploring the large-scale organizational patterns of gene expression in an epigenetic model of behavioral variability.</p><h3>Methodology/Findings</h3><p>To study the effects of epigenetic influences on behavioral variability, we examine gene expression in genetically identical mice. Using a novel approach to microarray analysis, we show that variability in the large-scale organization of gene expression levels, rather than differences in the expression levels of specific genes, is associated with individual differences in behavior. Specifically, increased activity in the open field is associated with increased variance of log-transformed measures of gene expression in the hippocampus, a brain region involved in open field activity. Early life experience that increases adult activity in the open field also similarly modifies the variance of gene expression levels. The same association of the variance of gene expression levels with behavioral variability is found with levels of gene expression in the hippocampus of genetically heterogeneous outbred populations of mice, suggesting that variation in the large-scale organization of gene expression levels may also be relevant to phenotypic differences in outbred populations such as humans. We find that the increased variance in gene expression levels is attributable to an increasing separation of several large, log-normally distributed families of gene expression levels. We also show that the presence of these multiple log-normal distributions of gene expression levels is a universal characteristic of gene expression in eurkaryotes. We use data from the MicroArray Quality Control Project (MAQC) to demonstrate that our method is robust and that it reliably detects biological differences in the large-scale organization of gene expression levels.</p><h3>Conclusions</h3><p>Our results contrast with the traditional belief that epigenetic effects on gene expression occur only at the level of specific genes and suggest instead that the large-scale organization of gene expression levels provides important insights into the relationship of gene expression with behavioral variability. Understanding the epigenetic, genetic, and environmental factors that regulate the large-scale organization of gene expression levels, and how changes in this large-scale organization influences brain development and behavior will be a major future challenge in the field of behavioral genomics.</p></div>", "links"=>[], "tags"=>["large-scale", "levels", "hippocampus", "relates", "epigenetic", "variability"], "article_id"=>149797, "categories"=>["Genetics", "Neuroscience"], "users"=>["Mark D. Alter", "Daniel B. Rubin", "Keri Ramsey", "Rebecca Halpern", "Dietrich A. Stephan", "L. F. Abbott", "Rene Hen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0003344.s001", "https://dx.doi.org/10.1371/journal.pone.0003344.s002", "https://dx.doi.org/10.1371/journal.pone.0003344.s003", "https://dx.doi.org/10.1371/journal.pone.0003344.s004", "https://dx.doi.org/10.1371/journal.pone.0003344.s005", "https://dx.doi.org/10.1371/journal.pone.0003344.s006"], "stats"=>{"downloads"=>7, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Variation_in_the_Large_Scale_Organization_of_Gene_Expression_Levels_in_the_Hippocampus_Relates_to_Stable_Epigenetic_Variability_in_Behavior/149797", "title"=>"Variation in the Large-Scale Organization of Gene Expression Levels in the Hippocampus Relates to Stable Epigenetic Variability in Behavior", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-10-06 02:43:17"}

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  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"12", "cited-by"=>"1", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"7"}
  • {"unique-ip"=>"12", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"8"}
  • {"unique-ip"=>"11", "full-text"=>"4", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2014", "month"=>"9"}
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  • {"unique-ip"=>"17", "full-text"=>"8", "pdf"=>"9", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"11"}
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  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"4"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"2", "full-text"=>"0", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
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  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"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"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
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  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"10", "full-text"=>"12", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"10", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"10", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
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Relative Metric

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