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{"title"=>"Transmission of stress-induced learning impairment and associated brain gene expression from parents to offspring in chickens", "type"=>"journal", "authors"=>[{"first_name"=>"Christina", "last_name"=>"Lindqvist", "scopus_author_id"=>"8575018100"}, {"first_name"=>"Andrew M.", "last_name"=>"Janczak", "scopus_author_id"=>"6603465993"}, {"first_name"=>"Daniel", "last_name"=>"Nätt", "scopus_author_id"=>"57190948409"}, {"first_name"=>"Izabella", "last_name"=>"Baranowska", "scopus_author_id"=>"22949788900"}, {"first_name"=>"Niclas", "last_name"=>"Lindqvist", "scopus_author_id"=>"6603938408"}, {"first_name"=>"Anette", "last_name"=>"Wichman", "scopus_author_id"=>"14032306300"}, {"first_name"=>"Joakim", "last_name"=>"Lundeberg", "scopus_author_id"=>"7004756744"}, {"first_name"=>"Johan", "last_name"=>"Lindberg", "scopus_author_id"=>"14012660900"}, {"first_name"=>"Peter A.", "last_name"=>"Torjesen", "scopus_author_id"=>"7005142383"}, {"first_name"=>"Per", "last_name"=>"Jensen", "scopus_author_id"=>"7402088701"}], "year"=>2007, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-35549009579", "sgr"=>"35549009579", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0000364", "pmid"=>"17426812", "isbn"=>"1932-6203 (Electronic)", "pui"=>"352618174"}, "id"=>"4c216602-80f5-3a1c-b89a-4b2de0602338", "abstract"=>"BACKGROUND: Stress influences many aspects of animal behaviour and is a major factor driving populations to adapt to changing living conditions, such as during domestication. Stress can affect offspring through non-genetic mechanisms, but recent research indicates that inherited epigenetic modifications of the genome could possibly also be involved. METHODOLOGY/PRINCIPAL FINDINGS: Red junglefowl (RJF, ancestors of modern chickens) and domesticated White Leghorn (WL) chickens were raised in a stressful environment (unpredictable light-dark rhythm) and control animals in similar pens, but on a 12/12 h light-dark rhythm. WL in both treatments had poorer spatial learning ability than RJF, and in both populations, stress caused a reduced ability to solve a spatial learning task. Offspring of stressed WL, but not RJF, raised without parental contact, had a reduced spatial learning ability compared to offspring of non-stressed animals in a similar test as that used for their parents. Offspring of stressed WL were also more competitive and grew faster than offspring of non-stressed parents. Using a whole-genome cDNA microarray, we found that in WL, the same changes in hypothalamic gene expression profile caused by stress in the parents were also found in the offspring. In offspring of stressed WL, at least 31 genes were up- or down-regulated in the hypothalamus and pituitary compared to offspring of non-stressed parents. CONCLUSIONS/SIGNIFICANCE: Our results suggest that, in WL the gene expression response to stress, as well as some behavioural stress responses, were transmitted across generations. The ability to transmit epigenetic information and behaviour modifications between generations may therefore have been favoured by domestication. The mechanisms involved remain to be investigated; epigenetic modifications could either have been inherited or acquired de novo in the specific egg environment. In both cases, this would offer a novel explanation to rapid evolutionary adaptation of a population.", "link"=>"http://www.mendeley.com/research/transmission-stressinduced-learning-impairment-associated-brain-gene-expression-parents-offspring-ch", "reader_count"=>83, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>8, "Researcher"=>14, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>1, "Student > Master"=>7, "Student > Bachelor"=>9, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>8}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>8, "Researcher"=>14, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>1, "Student > Master"=>7, "Student > Bachelor"=>9, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>8}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>68, "Medicine and Dentistry"=>4, "Neuroscience"=>2, "Veterinary Science and Veterinary Medicine"=>1, "Psychology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Neuroscience"=>{"Neuroscience"=>2}, "Psychology"=>{"Psychology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>68}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>2}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Netherlands"=>1, "Sweden"=>2, "Austria"=>1, "United States"=>2, "Brazil"=>2, "Italy"=>1, "United Kingdom"=>3, "France"=>1, "Spain"=>1}, "group_count"=>4}

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• {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/576", "title"=>"Incorrect data analysis", "body"=>"Apparently, the paper exhibits at least four flaws, which render the authors’ conclusions invalid.\r\n\r\nFirst, in the microarray study, M-values were calculated to estimate differential expression due to treatment. Data from each group of 8 birds (same generation and population) were collapsed, because the observations were not matched individually, but groupwise. In this way, all information on the relative expression of genes in individual birds is lost and the variation between experimental units (the basis of statistical inference) cannot be estimated. In the analysis that follows, the observations are pairwise M-values from the different spots, but there is only one group of animals, i.e. essentially one single observation, behind all data-points. Instead of using M-values, it would probably be wise to keep the raw values of relative expression as the outcome trait, thus utilizing information from each bird.\r\n\r\nSecond, correlation analysis, as in the study of associations between M-values in parents and offspring, requires that observations are independent. It is very reasonable to assume that there is some dependence between M-values of different spots, i.e. that the expressions of different genes are related to each other. Hence, the observed association probably reflects the degree of dependence among spots more than anything else.\r\n\r\nThird, sub-samples of the 9,033 spots were selected randomly to calculate a mean correlation coefficient and a standard error of that mean. However, the sub-samples are not independent either, primarily because of dependence among spots, but also because some sub-samples even share the same spots. The number of sub-samples is of course arbitrary; nevertheless, it is crucial when calculating standard errors and drawing further inferences. Therefore, the sub-sampling approach does not solve anything – it only makes things worse.\r\n\r\nFourth, learning ability was tested and the cumulative proportion of successful birds at each test round was compared between treatment and control groups by chi-square analysis. No adjustment was made for multiple comparisons at different tests. The graphs in Figure 1 allow us to reconstruct raw data with a fair degree of accuracy and re-run the analysis with such an adjustment. Alternatively, considering the time-to-event type of data, it seems more straightforward to test the effect of treatment using the log-rank test. With either analytical approach (both were tried by me), there is no significant difference between treated and control White Leghorn offspring (P>>0.05), as the authors claim. I did not check the learning ability results of the parental generation.\r\n\r\nCheers,\r\nJan Hultgren\r\n", "isRemoved"=>false, "created"=>"2007-05-07T07:45:20Z", "lastModified"=>"2007-05-07T07:45:20Z", "creator"=>{"userId"=>"87137"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0000364", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>2, "mostRecentActivity"=>"2007-11-13T21:04:55Z", "replies"=>[{"type"=>"REPLY", "parentID"=>7957, "annotationUri"=>"info:doi/10.1371/reply/171", "title"=>"RE: Incorrect data analysis", "body"=>"We thank Jan Hultgren for his important and stimulating comments on our paper, and would like to offer the following responses:\n\n1. I am afraid we do not fully understand the objection here. Underlying the M-values are of course data on the relative expression level of each spot from each individual. For every individual (4 per treatment group), one microarray (plus technical replicates) were run. The M-value, by definition, estimates the difference in average expression between two treatments or groups of animals. The statistical analysis developed for microarray analysis is based on the variation between experimental units (biological replicates), and we therefore continue to believe that the analysis we have done is the most appropriate one. \n\n2. Hultgren is correct in stating that the spots on one micro-array are inter-dependent, since regulatory networks will affect many genes in the same way. However, the main point of the correlation analysis is that there is a dependency of M-values (which, as already said, estimate the average differential expression) between generations, something which is not biologically obvious. The important message here is that this dependency was only seen in the population of birds where we simultaneously saw a phenotypic effect.\n\n3. The randomization procedure used for calculating an average coefficient of correlation does of course not render independent datasets, as Hultgren rightly points out. However, we think this was the best available type of analysis for our purpose. We could have simply calculated a correlation coefficient based on all 9033 pairs of M-values from the two generations, but this would be a biased analysis with an inflated p-value due to the facts that there were so many data-points, and that most of them had small absolute M-values. We could also have decided to look at only the most differentially expressed genes (those shown in the fig), but again this would have rendered a biased r. We therefore used a randomization procedure and picked random subsets of M-values as described in the paper. Even if the randomly generated datasets are not independent, they do provide a clear indication that the M-values of the two generations are correlated. However, we agree that the SD and the actual p-value of the t-test must be treated with care.\n\n4. As we do say in the paper, there was no overall effect of treatment on the average (or median) number of tests needed to reach the learning criterium in the offspring, which is probably why Hultgren does not find any significant result in his analysis. However, by visual inspection, it is obvious that the learning curves appear quite different between Leghorn offspring of stressed and control birds. After 5,6 and 7 rounds of testing, the differences between treatment groups were visually striking, and we therefore decided to test the differences in proportion of birds having solved the task at the points which appeared different. We did not apply a correction for multiple testing, because we only tested three data-points in the offspring, and in the parental generation, the differences were already shown by an ANOVA. We admit that the effects are small in the offspring, but still clearly discernible.\n\nCheers,\nPer Jensen, on behalf on the authors.\n", "isRemoved"=>false, "created"=>"2007-05-24T07:58:01Z", "lastModified"=>"2007-05-24T07:58:01Z", "creator"=>{"userId"=>"78119"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0000364", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>1, "mostRecentActivity"=>"2007-11-13T21:04:55Z", "replies"=>[{"type"=>"REPLY", "parentID"=>37397, "annotationUri"=>"info:doi/10.1371/reply/7ee25ec2-abb9-4efa-8f0e-39f97a15898d", "title"=>"RE: RE: Incorrect data analysis", "body"=>"I have read this paper with great interest, and we actually used it in a seminar about evolutionary biology at the Department of Ecology in Lund. The students and myself found the paper interesting and the results suggestive. Hopefully, this paper will stimulate further research in this area and this study is a first step.\n\nHowever, one of the students pointed out that the experiment was not replicated, i. e. all individual parents subject to stress-treatment were in one batch. If this criticism is correct, I believe it is a serious statistical problem with the current study. This problem could easily have been avoided if the the treatments had been replicated, but according to my reading of the paper, they have not. It is possible that this is a misunderstanding on my part, but I do not think so, at least when reading through the paper.", "isRemoved"=>false, "created"=>"2007-11-13T21:04:55Z", "lastModified"=>"2007-11-13T21:04:55Z", "creator"=>{"userId"=>"82923"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0000364", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2007-11-13T21:04:55Z", "replies"=>[]}]}]}
• {"type"=>"COMMENT", "annotationUri"=>"info:doi/10.1371/annotation/27b1af47-a885-4eb2-b997-0af0edde86f7", "title"=>"Interesting and suggestive", "body"=>"May be problem with lack of replication of treatments, see Discussion around this article.", "isRemoved"=>false, "created"=>"2007-11-13T21:08:05Z", "lastModified"=>"2007-11-13T21:08:05Z", "creator"=>{"userId"=>"82923"}, "highlightedText"=>"", "competingInterestStatement"=>{"creatorWasPrompted"=>false, "hasCompetingInterests"=>false}, "parentArticle"=>{"doi"=>"info:doi/10.1371/journal.pone.0000364", "state"=>"published", "journals"=>{"PLoSONE"=>{"journalKey"=>"PLoSONE", "eIssn"=>"1932-6203", "title"=>"PLOS ONE"}}}, "replyTreeSize"=>0, "mostRecentActivity"=>"2007-11-13T21:08:05Z", "replies"=>[]}

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• {"id"=>"781550213311848448", "text"=>"Here's a link to the great Swedish chicken epidgenetics study: https://t.co/elY8bQB86F", "created_at"=>"2016-09-29T17:44:26Z", "user"=>"MICROUVic", "user_name"=>"Doug Briant", "user_profile_image"=>"http://pbs.twimg.com/profile_images/2508233308/67sd78kwxvakdfvk0vmn_normal.jpeg"}

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Figshare

• {"files"=>["https://ndownloader.figshare.com/files/951205"], "description"=>"<p>M-value is the log₂ of the difference in expression level, and B-value is the log odds ratio of expression levels; the B-value estimates the certainty of DE vs non-certainty of DE. Common criteria for significant expression is that M>1 and B>0.</p>", "links"=>[], "tags"=>["genes", "parents", "offspring", "brains", "differential", "caused", "applied"], "article_id"=>621515, "categories"=>["Evolutionary Biology", "Infectious Diseases"], "users"=>["Christina Lindqvist", "Andrew M. Janczak", "Daniel Nätt", "Izabella Baranowska", "Niclas Lindqvist", "Anette Wichman", "Joakim Lundeberg", "Johan Lindberg", "Peter A. Torjesen", "Per Jensen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000364.t003", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Numbers_of_genes_in_parents_and_offspring_brains_showing_differential_expression_caused_by_stress_applied_to_parents_/621515", "title"=>"Numbers of genes in parents and offspring brains showing differential expression caused by stress applied to parents.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 12:37:04"}
• {"files"=>["https://ndownloader.figshare.com/files/951269"], "description"=>"<p>Birds were weighed within an hour after hatching and at eight days of age. Food competition capacity was estimated as the percentage of time in which each individual occupied the feeder in a pair-wise competition test. The data were analysed with ANOVA, using breed and parental treatment as fixed independent variables. Data (LS Means±SEM) with different superscripts in the table differ significantly at p<0.05.</p>", "links"=>[], "tags"=>["evolutionary biology/animal behavior", "evolutionary biology/genomics"], "article_id"=>621589, "categories"=>["Evolutionary Biology", "Infectious Diseases"], "users"=>["Christina Lindqvist", "Andrew M. Janczak", "Daniel Nätt", "Izabella Baranowska", "Niclas Lindqvist", "Anette Wichman", "Joakim Lundeberg", "Johan Lindberg", "Peter A. Torjesen", "Per Jensen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000364.t001", "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Weight_and_food_competition_capacity_in_offspring_/621589", "title"=>"Weight and food competition capacity in offspring", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 12:37:32"}
• {"files"=>["https://ndownloader.figshare.com/files/951097"], "description"=>"<p>Correlations between magnitude of differential expression of genes between parents and offspring. Diagrams show M-values for the differential expression (comparing stressed vs control parents, and offspring of stressed vs offspring of control parents) of the 500 most differentially expressed genes (largest log₂ difference caused by stress in parents) in (a) red junglefowl, and (b) White Leghorns. Each point represents one spot on the microarray. Positive M-values indicate upregulation and negative downregulation by stress (or by having stressed parents). The average correlation line is shown in both comparisons.</p>", "links"=>[], "tags"=>["evolutionary biology/animal behavior", "evolutionary biology/genomics"], "article_id"=>621414, "categories"=>["Evolutionary Biology", "Infectious Diseases"], "users"=>["Christina Lindqvist", "Andrew M. Janczak", "Daniel Nätt", "Izabella Baranowska", "Niclas Lindqvist", "Anette Wichman", "Joakim Lundeberg", "Johan Lindberg", "Peter A. Torjesen", "Per Jensen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000364.g002", "stats"=>{"downloads"=>3, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_2_/621414", "title"=>"Figure 2", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:36:31"}
• {"files"=>["https://ndownloader.figshare.com/files/951165"], "description"=>"<p>Because of the low number of biological replicates, no valid p-values could be estimated, so a gene with M>1 was considered to be differentially expressed in this analysis. All genes with M>1 showed the same direction of regulation (up or down-regulated by stress treatment) as on the microarray. The nine genes were selected based on their high M- and B-values in the microarray analysis. Relative expression levels (M-values) were estimated using β-actin as an internal control. Negative M-values indicate that the expression level was higher in control than in stress birds.</p>", "links"=>[], "tags"=>["rt-pcr", "genes", "verification", "microarray"], "article_id"=>621475, "categories"=>["Evolutionary Biology", "Infectious Diseases"], "users"=>["Christina Lindqvist", "Andrew M. Janczak", "Daniel Nätt", "Izabella Baranowska", "Niclas Lindqvist", "Anette Wichman", "Joakim Lundeberg", "Johan Lindberg", "Peter A. Torjesen", "Per Jensen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000364.t004", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Real_time_RT_PCR_data_for_nine_genes_selected_for_verification_of_microarray_results_/621475", "title"=>"Real-time RT-PCR data for nine genes selected for verification of microarray results", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 12:36:50"}
• {"files"=>["https://ndownloader.figshare.com/files/950972"], "description"=>"<p>Spatial learning in White Leghorn parents and their non-stressed offspring. Each panel shows cumulative proportion of tested birds which had solved the spatial learning task at successive test instances; the criterion for solving the task was five correct choices out of six successive tests, so the smallest number of required tests was five. a, White Leghorn parents. b, Red junglefowl parents. c, White Leghorn offspring. d, Red junglefowl offspring. The differences in cumulative proportions of birds from different treatments solving the task were tested with χ² –analysis after five test rounds and onwards, and significant differences are indicated (p<0.05).</p>", "links"=>[], "tags"=>["evolutionary biology/animal behavior", "evolutionary biology/genomics"], "article_id"=>621282, "categories"=>["Evolutionary Biology", "Infectious Diseases"], "users"=>["Christina Lindqvist", "Andrew M. Janczak", "Daniel Nätt", "Izabella Baranowska", "Niclas Lindqvist", "Anette Wichman", "Joakim Lundeberg", "Johan Lindberg", "Peter A. Torjesen", "Per Jensen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000364.g001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_1_/621282", "title"=>"Figure 1", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:35:39"}
• {"files"=>["https://ndownloader.figshare.com/files/951234"], "description"=>"<p>The table shows the 10 genes with highest differential expression in WL offspring, out of those which were among the 100 most differentially expressed genes in both WL parents and offspring. Negative M-values indicate that the expression level was higher in control than in stress birds.</p>", "links"=>[], "tags"=>["differentially", "leghorn", "parents"], "article_id"=>621547, "categories"=>["Evolutionary Biology", "Infectious Diseases"], "users"=>["Christina Lindqvist", "Andrew M. Janczak", "Daniel Nätt", "Izabella Baranowska", "Niclas Lindqvist", "Anette Wichman", "Joakim Lundeberg", "Johan Lindberg", "Peter A. Torjesen", "Per Jensen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0000364.t002", "stats"=>{"downloads"=>3, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genes_differentially_expressed_both_in_White_Leghorn_parents_and_offspring_/621547", "title"=>"Genes differentially expressed both in White Leghorn parents and offspring.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 12:37:19"}

PMC Usage Stats | Further Information

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• {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"18", "unique-ip"=>"13", "pdf"=>"4", "year"=>"2010", "figure"=>"12", "scanned-summary"=>"0", "supp-data"=>"0"}
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• {"scanned-page-browse"=>"0", "month"=>"7", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"3", "unique-ip"=>"5", "pdf"=>"2", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
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• {"scanned-page-browse"=>"0", "month"=>"9", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"9", "unique-ip"=>"12", "pdf"=>"4", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"10", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"3", "year"=>"2010", "pdf"=>"1", "unique-ip"=>"5", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"11", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"4", "unique-ip"=>"4", "pdf"=>"3", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"12", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "year"=>"2010", "pdf"=>"1", "unique-ip"=>"3", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"8", "unique-ip"=>"8", "pdf"=>"1", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"2", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"4", "year"=>"2011", "pdf"=>"4", "unique-ip"=>"5", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"6", "unique-ip"=>"8", "pdf"=>"5", "year"=>"2011", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "year"=>"2011", "pdf"=>"2", "unique-ip"=>"3", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"3", "unique-ip"=>"5", "pdf"=>"2", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"2", "year"=>"2011", "pdf"=>"0", "unique-ip"=>"4", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"7", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"5", "unique-ip"=>"6", "pdf"=>"0", "year"=>"2011", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"8", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"5", "year"=>"2011", "pdf"=>"2", "unique-ip"=>"6", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"9", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "unique-ip"=>"6", "pdf"=>"2", "year"=>"2011", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"10", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"4", "year"=>"2011", "pdf"=>"2", "unique-ip"=>"4", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"11", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"12", "unique-ip"=>"10", "pdf"=>"1", "year"=>"2011", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"0"}
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• {"month"=>"2", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"6", "year"=>"2012", "pdf"=>"2", "unique-ip"=>"5", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"4", "unique-ip"=>"4", "pdf"=>"0", "year"=>"2012", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "year"=>"2012", "pdf"=>"0", "unique-ip"=>"4", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "unique-ip"=>"2", "pdf"=>"2", "year"=>"2012", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"4", "scanned-page-browse"=>"31", "cited-by"=>"1", "abstract"=>"0", "full-text"=>"1", "year"=>"2007", "pdf"=>"0", "unique-ip"=>"1", "figure"=>"102", "scanned-summary"=>"69", "supp-data"=>"79"}
• {"scanned-page-browse"=>"25", "month"=>"5", "cited-by"=>"2", "abstract"=>"0", "full-text"=>"3", "unique-ip"=>"3", "pdf"=>"0", "year"=>"2007", "figure"=>"90", "scanned-summary"=>"59", "supp-data"=>"57"}
• {"scanned-page-browse"=>"5", "month"=>"7", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"1", "unique-ip"=>"0", "pdf"=>"0", "year"=>"2007", "figure"=>"21", "scanned-summary"=>"15", "supp-data"=>"16"}
• {"month"=>"8", "scanned-page-browse"=>"5", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"1", "year"=>"2007", "pdf"=>"0", "unique-ip"=>"0", "figure"=>"18", "scanned-summary"=>"12", "supp-data"=>"12"}
• {"scanned-page-browse"=>"9", "month"=>"9", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "unique-ip"=>"0", "pdf"=>"0", "year"=>"2007", "figure"=>"33", "scanned-summary"=>"22", "supp-data"=>"19"}
• {"month"=>"10", "scanned-page-browse"=>"13", "cited-by"=>"1", "abstract"=>"0", "full-text"=>"2", "year"=>"2007", "pdf"=>"0", "unique-ip"=>"1", "figure"=>"42", "scanned-summary"=>"26", "supp-data"=>"26"}
• {"scanned-page-browse"=>"12", "month"=>"11", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"0", "unique-ip"=>"2", "pdf"=>"0", "year"=>"2007", "figure"=>"46", "scanned-summary"=>"32", "supp-data"=>"25"}
• {"month"=>"12", "scanned-page-browse"=>"10", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "year"=>"2007", "pdf"=>"0", "unique-ip"=>"1", "figure"=>"34", "scanned-summary"=>"21", "supp-data"=>"20"}
• {"scanned-page-browse"=>"6", "month"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"1", "unique-ip"=>"0", "pdf"=>"0", "year"=>"2008", "figure"=>"26", "scanned-summary"=>"19", "supp-data"=>"18"}
• {"month"=>"2", "scanned-page-browse"=>"10", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"0", "year"=>"2008", "pdf"=>"0", "unique-ip"=>"0", "figure"=>"44", "scanned-summary"=>"34", "supp-data"=>"30"}
• {"scanned-page-browse"=>"4", "month"=>"3", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"0", "unique-ip"=>"0", "pdf"=>"0", "year"=>"2008", "figure"=>"17", "scanned-summary"=>"13", "supp-data"=>"13"}
• {"month"=>"4", "scanned-page-browse"=>"5", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"0", "year"=>"2008", "pdf"=>"0", "unique-ip"=>"0", "figure"=>"15", "scanned-summary"=>"10", "supp-data"=>"12"}
• {"scanned-page-browse"=>"4", "month"=>"5", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"0", "unique-ip"=>"2", "pdf"=>"0", "year"=>"2008", "figure"=>"16", "scanned-summary"=>"10", "supp-data"=>"11"}
• {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"16", "year"=>"2008", "pdf"=>"1", "unique-ip"=>"12", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"7", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"19", "unique-ip"=>"17", "pdf"=>"5", "year"=>"2008", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"8", "scanned-page-browse"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"1", "year"=>"2008", "pdf"=>"0", "unique-ip"=>"0", "figure"=>"7", "scanned-summary"=>"5", "supp-data"=>"6"}
• {"scanned-page-browse"=>"0", "month"=>"9", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"13", "unique-ip"=>"14", "pdf"=>"6", "year"=>"2008", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"10", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "year"=>"2008", "pdf"=>"3", "unique-ip"=>"5", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"11", "cited-by"=>"1", "abstract"=>"1", "full-text"=>"8", "unique-ip"=>"9", "pdf"=>"4", "year"=>"2008", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"12", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"13", "year"=>"2008", "pdf"=>"3", "unique-ip"=>"12", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"1", "cited-by"=>"1", "abstract"=>"1", "full-text"=>"13", "unique-ip"=>"12", "pdf"=>"6", "year"=>"2009", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"2", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"11", "year"=>"2009", "pdf"=>"8", "unique-ip"=>"12", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"15", "unique-ip"=>"14", "pdf"=>"7", "year"=>"2009", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"5", "year"=>"2009", "pdf"=>"4", "unique-ip"=>"8", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"4", "unique-ip"=>"5", "pdf"=>"2", "year"=>"2009", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "year"=>"2009", "pdf"=>"2", "unique-ip"=>"4", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"7", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"5", "unique-ip"=>"6", "pdf"=>"2", "year"=>"2009", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"8", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"3", "year"=>"2009", "pdf"=>"2", "unique-ip"=>"4", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"9", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"6", "unique-ip"=>"5", "pdf"=>"4", "year"=>"2009", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"10", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"2", "year"=>"2009", "pdf"=>"1", "unique-ip"=>"3", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"11", "cited-by"=>"1", "abstract"=>"1", "full-text"=>"36", "unique-ip"=>"16", "pdf"=>"8", "year"=>"2009", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"12", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"3", "full-text"=>"8", "year"=>"2009", "pdf"=>"3", "unique-ip"=>"11", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"scanned-page-browse"=>"0", "month"=>"6", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"3", "unique-ip"=>"3", "pdf"=>"2", "year"=>"2012", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
• {"month"=>"6", "scanned-page-browse"=>"13", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"2", "year"=>"2007", "pdf"=>"0", "unique-ip"=>"0", "figure"=>"40", "scanned-summary"=>"25", "supp-data"=>"30"}
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• {"unique-ip"=>"5", "full-text"=>"9", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
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• {"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"=>"8"}
• {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
• {"unique-ip"=>"6", "full-text"=>"5", "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"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"11"}
• {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"12"}
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Relative Metric

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F1000Prime