The Perilipin Homologue, Lipid Storage Droplet 2, Regulates Sleep Homeostasis and Prevents Learning Impairments Following Sleep Loss
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{"title"=>"The Perilipin homologue, Lipid storage droplet 2, regulates sleep homeostasis and prevents learning impairments following sleep loss", "type"=>"journal", "authors"=>[{"first_name"=>"Matthew S.", "last_name"=>"Thimgan", "scopus_author_id"=>"36960670600"}, {"first_name"=>"Yasuko", "last_name"=>"Suzuki", "scopus_author_id"=>"55724542200"}, {"first_name"=>"Laurent", "last_name"=>"Seugnet", "scopus_author_id"=>"6506143969"}, {"first_name"=>"Laura", "last_name"=>"Gottschalk", "scopus_author_id"=>"24478741100"}, {"first_name"=>"Paul J.", "last_name"=>"Shaw", "scopus_author_id"=>"7401651687"}], "year"=>2010, "source"=>"PLoS Biology", "identifiers"=>{"issn"=>"15449173", "scopus"=>"2-s2.0-77956854713", "pui"=>"359586885", "doi"=>"10.1371/journal.pbio.1000466", "isbn"=>"1545-7885 (Electronic)\\r1544-9173 (Linking)", "sgr"=>"77956854713", "pmid"=>"20824166"}, "id"=>"325c6b78-7a19-300e-a814-f04e0a5543af", "abstract"=>"Extended periods of waking result in physiological impairments in humans, rats, and flies. Sleep homeostasis, the increase in sleep observed following sleep loss, is believed to counter the negative effects of prolonged waking by restoring vital biological processes that are degraded during sleep deprivation. Sleep homeostasis, as with other behaviors, is influenced by both genes and environment. We report here that during periods of starvation, flies remain spontaneously awake but, in contrast to sleep deprivation, do not accrue any of the negative consequences of prolonged waking. Specifically, the homeostatic response and learning impairments that are a characteristic of sleep loss are not observed following prolonged waking induced by starvation. Recently, two genes, brummer (bmm) and Lipid storage droplet 2 (Lsd2), have been shown to modulate the response to starvation. bmm mutants have excess fat and are resistant to starvation, whereas Lsd2 mutants are lean and sensitive to starvation. Thus, we hypothesized that bmm and Lsd2 may play a role in sleep regulation. Indeed, bmm mutant flies display a large homeostatic response following sleep deprivation. In contrast, Lsd2 mutant flies, which phenocopy aspects of starvation as measured by low triglyceride stores, do not exhibit a homeostatic response following sleep loss. Importantly, Lsd2 mutant flies are not learning impaired after sleep deprivation. These results provide the first genetic evidence, to our knowledge, that lipid metabolism plays an important role in regulating the homeostatic response and can protect against neuronal impairments induced by prolonged waking.", "link"=>"http://www.mendeley.com/research/perilipin-homologue-lipid-storage-droplet-2-regulates-sleep-homeostasis-prevents-learning-impairment", "reader_count"=>73, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>5, "Researcher"=>17, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>24, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>9, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>5, "Researcher"=>17, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>24, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>9, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>48, "Medicine and Dentistry"=>3, "Neuroscience"=>11, "Psychology"=>1, "Social Sciences"=>1, "Veterinary Science and Veterinary Medicine"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>11}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>48}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>3}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>2}}, "reader_count_by_country"=>{"United States"=>3, "China"=>1, "France"=>1}, "group_count"=>5}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/414803", "https://ndownloader.figshare.com/files/414824", "https://ndownloader.figshare.com/files/414840", "https://ndownloader.figshare.com/files/414857", "https://ndownloader.figshare.com/files/414873", "https://ndownloader.figshare.com/files/414880"], "description"=>"<div><p>Extended periods of waking result in physiological impairments in humans, rats, and flies. Sleep homeostasis, the increase in sleep observed following sleep loss, is believed to counter the negative effects of prolonged waking by restoring vital biological processes that are degraded during sleep deprivation. Sleep homeostasis, as with other behaviors, is influenced by both genes and environment. We report here that during periods of starvation, flies remain spontaneously awake but, in contrast to sleep deprivation, do not accrue any of the negative consequences of prolonged waking. Specifically, the homeostatic response and learning impairments that are a characteristic of sleep loss are not observed following prolonged waking induced by starvation. Recently, two genes, <em>brummer</em> (<em>bmm</em>) and <em>Lipid storage droplet 2</em> (<em>Lsd2</em>), have been shown to modulate the response to starvation. <em>bmm</em> mutants have excess fat and are resistant to starvation, whereas <em>Lsd2</em> mutants are lean and sensitive to starvation. Thus, we hypothesized that <em>bmm</em> and <em>Lsd2</em> may play a role in sleep regulation. Indeed, <em>bmm</em> mutant flies display a large homeostatic response following sleep deprivation. In contrast, <em>Lsd2</em> mutant flies, which phenocopy aspects of starvation as measured by low triglyceride stores, do not exhibit a homeostatic response following sleep loss. Importantly, <em>Lsd2</em> mutant flies are not learning impaired after sleep deprivation. These results provide the first genetic evidence, to our knowledge, that lipid metabolism plays an important role in regulating the homeostatic response and can protect against neuronal impairments induced by prolonged waking.</p></div>", "links"=>[], "tags"=>["droplet", "regulates", "homeostasis", "prevents", "impairments"], "article_id"=>141897, "categories"=>["Medicine", "Neuroscience", "Physiology"], "users"=>["Matthew S. Thimgan", "Yasuko Suzuki", "Laurent Seugnet", "Laura Gottschalk", "Paul J. Shaw"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000466.s001", "https://dx.doi.org/10.1371/journal.pbio.1000466.s002", "https://dx.doi.org/10.1371/journal.pbio.1000466.s003", "https://dx.doi.org/10.1371/journal.pbio.1000466.s004", "https://dx.doi.org/10.1371/journal.pbio.1000466.s005", "https://dx.doi.org/10.1371/journal.pbio.1000466.s006"], "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Perilipin_Homologue_Lipid_Storage_Droplet_2_Regulates_Sleep_Homeostasis_and_Prevents_Learning_Impairments_Following_Sleep_Loss/141897", "title"=>"The <em>Perilipin</em> Homologue, <em>Lipid Storage Droplet 2</em>, Regulates Sleep Homeostasis and Prevents Learning Impairments Following Sleep Loss", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-08-31 00:31:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/831883"], "description"=>"<p>(A) <i>cyc<sup>01</sup></i> flies show a large homeostatic response after 7 h of sleep deprivation (SD, black) but do not display a homeostatic response following waking induced by 7 h of starvation (stv, gray). The sleep deprivation and starvation experiments were conducted in parallel on female siblings whose baseline sleep was monitored for 3 d; experiments were conducted in constant darkness (DD). Cumulative sleep lost or gained during SD or starvation. A negative slope indicates sleep lost, and a positive slope indicates sleep gained; when the slope is zero, recovery is complete. Stippled bar indicates treatment and white bar indicates recovery (<i>n</i> = 72 for each group, data are presented as mean ± SEM). (B) <i>Amylase</i> mRNA for sleep deprived and starved <i>cyc<sup>01</sup></i> flies expressed as a percentage change from age-matched untreated controls as measured by QPCR (<i>n</i> = 3 replicates of 20 heads/group; *<i>p</i><.05 Student's <i>t</i> test). (C) APS performance is significantly disrupted by SD but is unchanged following starvation in <i>cyc<sup>01</sup></i> flies. The performance index is the number of photonegative choices during the last 4 trials of a 16-trial test; a higher score indicates learning. One way ANOVA <i>F</i>[<sub>2,30</sub>]  = 5.26; <i>n</i> = 10/group; *<i>p</i><.05 modified Bonferroni Test. (D) <i>per<sup>01</sup></i> flies show a large sleep rebound following 7 h of sleep deprivation but do not display a homeostatic response following 7 h of starvation (<i>n</i> = 72 for each group). (E) <i>Amylase</i> mRNA for sleep deprived and starved <i>per<sup>01</sup></i>flies expressed as a percentage change from age-matched untreated controls as measured by QPCR (<i>n</i> = 3 replicates of 20 heads/group; *<i>p</i><.05 Student's <i>t</i> test). (F) APS performance is significantly disrupted by SD but is unchanged following starvation in <i>per<sup>01</sup></i> flies. One way ANOVA <i>F</i>[<sub>2,26</sub>]  = 2.6; *<i>p</i><.05 modified Bonferroni Test.</p>", "links"=>[], "tags"=>["produces", "waking", "activate"], "article_id"=>502250, "categories"=>["Medicine", "Neuroscience", "Physiology"], "users"=>["Matthew S. Thimgan", "Yasuko Suzuki", "Laurent Seugnet", "Laura Gottschalk", "Paul J. Shaw"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000466.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Starvation_produces_a_waking_state_that_does_not_activate_sleep_homeostasis_/502250", "title"=>"Starvation produces a waking state that does not activate sleep homeostasis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-31 00:37:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/832252"], "description"=>"<p>(A) A representative section of <i>Lsd2<sup>rev</sup></i> head stained with Oil Red O. Head fat bodies are denoted by arrowheads. (B) A representative section of <i>Lsd2<sup>51</sup></i> head stained with Oil Red O. (C) <i>Lsd2<sup>51</sup></i> mutants (<i>n</i> = 22) do not exhibit a homeostatic response following 12 h of sleep deprivation while their genetic background control, <i>Lsd2<sup>rev</sup></i> (<i>n</i> = 41), do exhibit a sleep rebound following sleep loss. *<i>p</i> = 0.012; Student's <i>t</i> test. (D) <i>Amylase</i> mRNA levels of <i>Lsd2<sup>51</sup></i> mutants are significantly lower than genetic background controls, <i>Lsd<sup>rev</sup></i>, following 12 h of sleep deprivation. Data are presented as percentage from untreated siblings (2 replicates of <i>n</i> = 20 heads/group). *<i>p</i><.05, Student's <i>t</i> test. (E) Learning is not impaired in <i>Lsd2<sup>51</sup></i> mutants (<i>n</i> = 7) following 12 h of sleep deprivation compared to untreated controls (<i>n</i> = 8); <i>p</i> = 0.37 Student's <i>t</i> test. (F) Learning is impaired in <i>Lsd2<sup>rev</sup></i> flies (<i>n</i> = 15) following 12 h of sleep deprivation compared to untreated controls (<i>n</i> = 15).* <i>p</i> = 0.036 Student's <i>t</i> test.</p>", "links"=>[], "tags"=>["mutant", "flies", "mimic", "phenotypes", "seen", "starved"], "article_id"=>502617, "categories"=>["Medicine", "Neuroscience", "Physiology"], "users"=>["Matthew S. Thimgan", "Yasuko Suzuki", "Laurent Seugnet", "Laura Gottschalk", "Paul J. Shaw"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000466.g005", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lsd2_mutant_flies_mimic_the_phenotypes_seen_in_starved_cyc_01_flies_/502617", "title"=>"<i>Lsd2</i> mutant flies mimic the phenotypes seen in starved <i>cyc<sup>01</sup></i> flies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-31 00:43:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/832037"], "description"=>"<p>(A) Representative Oil Red O staining, which stains lipids red, reveals high levels of fat stores in the abdomen of female <i>cyc<sup>01</sup></i> flies. Boxed areas (Ai and Aii) are presented at higher magnification. * denotes developing eggs, and arrowheads are placed in the lumen of the gut and point to gut epithelial cells. Arrows point to the location of the fat bodies which abut the cuticle (9 flies were examined). (B) Representative section of <i>ry<sup>506</sup></i> abdomen, the background control for <i>cyc<sup>01</sup></i>. <i>ry<sup>506</sup></i> have little accumulation of lipid droplets in the abdomen in similar areas to (A) as revealed by Oil Red O staining. Boxed areas (Bi and Bii) are presented at higher magnification (9 flies were examined). (C) Representative section of Oil Red O stained <i>cyc<sup>01</sup>/Df</i> abdomen reveals high levels of fat stores. (Ci and Cii) are presented at higher magnification (9 flies were examined). (D) Organismal triglyceride (TG) levels are elevated in <i>cyc<sup>01</sup></i>, <i>cyc<sup>01</sup></i>/<i>Df</i>, and <i>cyc<sup>01/</sup>ry<sup>506</sup></i>flies compared to <i>ry<sup>506</sup></i> controls; one-way ANOVA for Genotype <i>F</i>[<sub>4,38</sub>]  = 3.2; *<i>p</i><.05 modified Bonferroni Test; <i>n</i>≥7 groups/condition, a group was comprised of 10 flies. (E) An elevated homeostatic response is observed in <i>cyc<sup>01</sup></i> mutants that were starved for 7 h (<i>n</i> = 45) on 1% agar containing 25 µM etomoxir. No further increase in homeostasis is found in <i>cyc<sup>01</sup></i> sleep deprived for 7 h on food containing 25 µM etomoxir (<i>n</i> = 72); compare with <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000466#pbio-1000466-g001\" target=\"_blank\">Figure 1A</a>. Siblings starved in the absence of etomoxir are shown for comparison (<i>n</i> = 92); all experiments were conducted in parallel.</p>", "links"=>[], "tags"=>["flies"], "article_id"=>502410, "categories"=>["Medicine", "Neuroscience", "Physiology"], "users"=>["Matthew S. Thimgan", "Yasuko Suzuki", "Laurent Seugnet", "Laura Gottschalk", "Paul J. Shaw"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000466.g003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_cyc_01_flies_have_increased_adiposity_/502410", "title"=>"<i>cyc<sup>01</sup></i> flies have increased adiposity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-31 00:40:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/832148"], "description"=>"<p>(A) <i>bmm</i> mRNA expression is elevated in the heads of <i>cyc<sup>01</sup></i> flies after sleep deprivation but not after starvation. (B) A representative section of <i>bmm<sup>rev</sup></i> head stained with Oil Red O, head fat bodies are denoted by arrowheads; fat droplets are discrete and well defined. (C) A representative section of <i>bmm<sup>1</sup></i> head stained with Oil Red O; head fat bodies are filled with stored lipids without space in between the droplets. (D) <i>bmm<sup>1</sup></i> mutants exhibit a large sleep rebound following 12 h of sleep deprivation compared with genetic background controls, <i>bmm<sup>rev</sup></i>; <i>n</i> = 23 and <i>n</i> = 21, respectively; * <i>p</i> = 0.0033, Student's <i>t</i> test. This finding was replicated in 6 independent experiments (<i>bmm<sup>rev</sup> n</i> = 198; <i>bmm<sup>1</sup></i>  = 189). (E) <i>bmm<sup>1</sup></i> mutants have increased <i>Amylase</i> mRNA levels after sleep deprivation compared with <i>bmm<sup>rev</sup></i>. Representative results are normalized to untreated siblings (2 replicates of <i>n</i> = 20 heads/group). (F) Rescue of sleep homeostasis in <i>bmm<sup>1</sup></i> mutants. A homeostatic response is observed in both parental lines, <i>Actin-GAL4/+; bmm<sup>1</sup></i>/<i>bmm<sup>1</sup></i> (<i>n</i> = 88) and <i>UAS-bmm<sup>wt</sup></i>/+;<i>bmm<sup>1</sup></i>/<i>bmm<sup>1</sup></i> (<i>n</i> = 105) following 12 h of sleep deprivation. However, the rescue line <i>Actin-GAL4/UAS-bmm<sup>wt</sup></i>; <i>bmm<sup>1</sup></i>/<i>bmm<sup>1</sup></i> (<i>n</i> = 55) did not respond to sleep loss with an observable homeostatic response. One way ANOVA <i>F</i>[<sub>2,245</sub>]  = 7.00; *<i>p</i><.001 modified Bonferroni Test.</p>", "links"=>[], "tags"=>["rebound"], "article_id"=>502520, "categories"=>["Medicine", "Neuroscience", "Physiology"], "users"=>["Matthew S. Thimgan", "Yasuko Suzuki", "Laurent Seugnet", "Laura Gottschalk", "Paul J. Shaw"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000466.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletion_of_bmm_results_in_an_increased_rebound_after_sleep_deprivation_/502520", "title"=>"Deletion of <i>bmm</i> results in an increased rebound after sleep deprivation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-31 00:42:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/831972"], "description"=>"<p>(A) Starvation induces waking in Wild-type <i>Canton-S</i> flies (squares, <i>n</i> = 16) and flies mutant for the canonical clock gene <i>Clock</i> (<i>Clk<sup>jrk</sup></i>, diamonds, <i>n</i> = 16). <i>CS</i> flies were kept on a 12∶12 LD schedule and starved for 12 h during the dark period (stippled). <i>Clk<sup>jrk</sup></i> mutants were maintained under DD and starved for 12 h. At the end of the starvation period, flies were then placed back on to normal food into LD or DD, respectively, for recovery (black). Cumulative sleep lost or gained during was calculated. Data are presented as mean ± SEM. (B) Recovery sleep measured in <i>w<sup>1118</sup></i> flies following 12 h of sleep deprivation (<i>n</i> = 18) or 12 h of starvation (<i>n</i> = 9) during the dark period. % sleep recovered is calculated for each individual as a ratio of the minutes of sleep gained above baseline during recovery divided by the total min of sleep lost during sleep deprivation. Sleep homeostasis was larger in sleep deprived flies versus their starved siblings (* <i>p</i> = 0.018 by Student's <i>t</i> test). (C) Starved <i>w<sup>1118</sup></i> flies (gray bar, <i>n</i> = 8) exhibit similar learning scores after extended waking versus untreated circadian matched controls (white bar, <i>n</i> = 10) while their sleep deprived siblings (black bar, <i>n</i> = 8) display impaired learning; One way ANOVA <i>F</i>[<sub>2,23</sub>]  = 2.1; *<i>p</i><.05 modified Bonferroni Test.</p>", "links"=>[], "tags"=>["induced", "starvation", "activate", "homeostasis", "wild-type", "flies", "mutants"], "article_id"=>502335, "categories"=>["Medicine", "Neuroscience", "Physiology"], "users"=>["Matthew S. Thimgan", "Yasuko Suzuki", "Laurent Seugnet", "Laura Gottschalk", "Paul J. Shaw"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000466.g002", "stats"=>{"downloads"=>4, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Waking_induced_by_starvation_does_not_activate_sleep_homeostasis_in_wild_type_flies_or_mutants_for_Clock_/502335", "title"=>"Waking induced by starvation does not activate sleep homeostasis in wild-type flies or mutants for <i>Clock</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-31 00:38:55"}

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  • {"unique-ip"=>"22", "full-text"=>"20", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"16", "full-text"=>"19", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"22", "full-text"=>"19", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"1"}
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  • {"unique-ip"=>"22", "full-text"=>"22", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
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  • {"unique-ip"=>"13", "full-text"=>"13", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"10", "full-text"=>"11", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2017", "month"=>"1"}
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  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
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  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
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  • {"unique-ip"=>"15", "full-text"=>"15", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
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  • {"unique-ip"=>"11", "full-text"=>"11", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"18", "full-text"=>"23", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"25", "full-text"=>"22", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"12", "full-text"=>"11", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
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  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
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Relative Metric

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