Sex-Dependent Psychoneuroendocrine Effects of THC and MDMA in an Animal Model of Adolescent Drug Consumption
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{"title"=>"Sex-dependent psychoneuroendocrine effects of THC and MDMA in an animal model of adolescent drug consumption", "type"=>"journal", "authors"=>[{"first_name"=>"Alvaro", "last_name"=>"Llorente-Berzal", "scopus_author_id"=>"24776022200"}, {"first_name"=>"Emma", "last_name"=>"Puighermanal", "scopus_author_id"=>"18038378100"}, {"first_name"=>"Aurelijus", "last_name"=>"Burokas", "scopus_author_id"=>"35368197000"}, {"first_name"=>"Andrés", "last_name"=>"Ozaita", "scopus_author_id"=>"6603838294"}, {"first_name"=>"Rafael", "last_name"=>"Maldonado", "scopus_author_id"=>"26643254500"}, {"first_name"=>"Eva M.", "last_name"=>"Marco", "scopus_author_id"=>"35586285600"}, {"first_name"=>"Maria Paz", "last_name"=>"Viveros", "scopus_author_id"=>"6506540335"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"24223797", "doi"=>"10.1371/journal.pone.0078386", "pui"=>"372132785", "issn"=>"19326203", "sgr"=>"84892611833", "scopus"=>"2-s2.0-84892611833"}, "id"=>"42900671-6a48-3808-acb2-d0a03bb0e29f", "abstract"=>"Ecstasy is a drug that is usually consumed by young people at the weekends and frequently, in combination with cannabis. In the present study we have investigated the long-term effects of administering increasing doses of delta-9-tetrahydrocannabinol [THC; 2.5, 5, 10 mg/kg; i.p.] from postnatal day (pnd) 28 to 45, alone and/or in conjunction with 3,4-methylenedioxymethamphetamine [MDMA; two daily doses of 10 mg/kg every 5 days; s.c.] from pnd 30 to 45, in both male and female Wistar rats. When tested one day after the end of the pharmacological treatment (pnd 46), MDMA administration induced a reduction in directed exploration in the holeboard test and an increase in open-arm exploration in an elevated plus maze. In the long-term, cognitive functions in the novel object test were seen to be disrupted by THC administration to female but not male rats. In the prepulse inhibition test, MDMA-treated animals showed a decrease in prepulse inhibition at the most intense prepulse studied (80 dB), whereas in combination with THC it induced a similar decrease at 75 dB. THC decreased hippocampal Arc expression in both sexes, while in the frontal cortex this reduction was only evident in females. MDMA induced a reduction in ERK1/2 immunoreactivity in the frontal cortex of male but not female animals, and THC decreased prepro-orexin mRNA levels in the hypothalamus of males, although this effect was prevented when the animals also received MDMA. The results presented indicate that adolescent exposure to THC and/or MDMA induces long-term, sex-dependent psychophysiological alterations and they reveal functional interactions between the two drugs.", "link"=>"http://www.mendeley.com/research/sexdependent-psychoneuroendocrine-effects-thc-mdma-animal-model-adolescent-drug-consumption", "reader_count"=>40, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>5, "Librarian"=>1, "Student > Doctoral Student"=>3, "Researcher"=>4, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>2, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>5, "Librarian"=>1, "Student > Doctoral Student"=>3, "Researcher"=>4, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>2, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Medicine and Dentistry"=>6, "Agricultural and Biological Sciences"=>14, "Neuroscience"=>8, "Psychology"=>4, "Chemistry"=>1, "Social Sciences"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Neuroscience"=>{"Neuroscience"=>8}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"United States"=>3, "Spain"=>2}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1267200"], "description"=>"<p>Animals were exposed to increasing doses of THC (2.5, 5 and 10 mg/kg or vehicle) from pnd 28 to 45 and to MDMA (10 mg/kg or saline) twice daily every 5 days from pnd 30 to 45 (see text for details). The animals' body temperature was measured just before the first MDMA (or Sal) injection to establish the baseline, and then one, two and four hours later, the latter immediately before the second MDMA (or Sal) injection, as well as one hour after that second injection (arrows indicate MDMA/Sal injections). The figures show the change in rectal temperature with respect to the baseline temperature (mean ± S.E.M.) expressed in degrees centigrade (°C). The number of animals per experimental group: males, Vh-Sal (16), Vh-MDMA (14), THC-Sal (16), THC-MDMA (14); and females, Vh-Sal (16), Vh-MDMA (14), THC-Sal (16), THC-MDMA (12). According to a repeated measures ANOVA (P<0.05), (g) represents a significant MDMA effect within the same sex group.</p>", "links"=>[], "tags"=>["days", "mdma"], "article_id"=>841197, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.g003", "stats"=>{"downloads"=>1, "page_views"=>32, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_body_temperature_on_the_first_pnd_30_and_last_pnd_45_days_of_MDMA_administration_/841197", "title"=>"Changes in body temperature on the first (pnd 30) and last (pnd 45) days of MDMA administration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267215"], "description"=>"<p>Behavioral tests were carried out on animals that had been exposed in the adolescent period to increasing doses of THC (2.5, 5 and 10 mg/kg or vehicle) from pnd 28 to 45 and to MDMA (10 mg/kg or saline) twice daily every 5 days from pnd 30 to 45 (see text for details). Three-way ANOVA analyses were performed, except for on the closed arm entries, with factors being sex (males <i>vs.</i> females), neonatal manipulation (control <i>vs.</i> MD) and drug treatment (Sal <i>vs.</i> Coc). The main statistical values are shown: F, with degrees of freedom, or H (in the case of Kruskal-Wallis) for closed arm entries, and p-values. Non-significant results are not included (−). Behavioral tests: HB, holeboard test; EPM, elevated plus maze; OF, open field; NOT, novel object test; PPI, prepulse inhibition test.</p>", "links"=>[], "tags"=>[], "article_id"=>841211, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.t001", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Main_results_from_the_statistical_analysis_of_behavioral_data_/841211", "title"=>"Main results from the statistical analysis of behavioral data.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267199"], "description"=>"<p>The animals were exposed to increasing doses of THC (2.5, 5 and 10 mg/kg or vehicle) from pnd 28 to 45, and to MDMA (10 mg/kg or saline) twice daily every 5 days from pnd 30 to 45 (see text for details). Body weight was registered daily during the administration period, from pnd 28 to 45, and every five days from pnd 50 to 70 (arrows indicate MDMA/Sal injections). The gain in body weight (in grams, g; mean ± S.E.M.) is expressed as the difference in body weight in males (upper panels) and females (lower panels) on each experimental day, and pnd 30 was established as the reference day. Number of animals per experimental group: males, Vh-Sal (16), Vh-MDMA (14), THC-Sal (16), THC-MDMA (14); and females, Vh-Sal (16), Vh-MDMA (14), THC-Sal (16), THC-MDMA (12). According to a repeated measures ANOVA (P<0.05): (e) significant overall effect of THC within the same sex group; (g) significant MDMA effect within the same sex group.</p>", "links"=>[], "tags"=>[], "article_id"=>841196, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.g002", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolution_of_body_weight_gain_during_the_drug_administration_period_left_panels_and_following_drug_withdrawal_right_panels_/841196", "title"=>"Evolution of body weight gain during the drug administration period (left panels) and following drug withdrawal (right panels).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267204"], "description"=>"<p>Animals were exposed to increasing doses of THC (2.5, 5 and 10 mg/kg or vehicle) from pnd 28 to 45 and to MDMA (10 mg/kg or saline) twice daily every 5 days from pnd 30 to 45 (see text for details). The histograms represent the percentage of PPI (mean ± S.E.M.) with three different pre-pulse intensities (73, 75 and 80 dB). Number of animals per experimental group: males, Vh-Sal (16), Vh-MDMA (12), THC-Sal (16), THC-MDMA (14); and females, Vh-Sal (16), Vh-MDMA (14), THC-Sal (16), THC-MDMA (10). According to ANOVA (P<0.05): (a) significant overall effect of sex; (c) significant overall effect of MDMA treatment; (f) significant MDMA effect among THC-treated animals.</p>", "links"=>[], "tags"=>["prepulse", "inhibition", "performed", "pnd"], "article_id"=>841201, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.g006", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_prepulse_inhibition_test_PPI_was_performed_at_adulthood_on_pnd_84_/841201", "title"=>"The prepulse inhibition test (PPI) was performed at adulthood, on pnd 84.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267203"], "description"=>"<p>Animals were exposed to increasing doses of THC (2.5, 5 and 10 mg/kg or vehicle) from pnd 28 to 45 and to MDMA (10 mg/kg or saline) twice daily every 5 days from pnd 30 to 45 (see text for details). The histograms (mean ± S.E.M.) show the discrimination index (left panel) measured as the difference between the time spent exploring the novel object (N) and the time spent exploring the familiar one (F1 or F2) in function of the total time spent exploring the two objects during the test session [N−F/(N+F)]. The time animals spent exploring both objects during the test session is also shown (right panel). Number of animals per experimental group: males, Vh-Sal (15), Vh-MDMA (12), THC-Sal (15), THC-MDMA (11); and females, Vh-Sal (15), Vh-MDMA (13), THC-Sal (16), THC-MDMA (10). According to ANOVA (P<0.05): (a) significant overall effect of sex; (c) significant overall effect of MDMA treatment; (e) significant overall effect of THC within the same sex group.</p>", "links"=>[], "tags"=>["performed", "pnd"], "article_id"=>841200, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.g005", "stats"=>{"downloads"=>3, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_novel_object_test_NOT_was_performed_on_pnd_75_/841200", "title"=>"The novel object test (NOT) was performed on pnd 75.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267217"], "description"=>"<p>Quantitative real-time PCR analysis of hypothalamic preproorexin expression in adult animals sacrificed around pnd 90. Animals were exposed to increasing doses of THC (2.5, 5 and 10 mg/kg or vehicle) from pnd 28 to 45, and to MDMA (10 mg/kg or saline) twice a day every 5 days from pnd 30 to 45 (see text for details). Levels of prepro-orexin mRNA (mean ± S.E.M.) are expressed in arbitrary units in reference to the control animals (Vh-Sal) of their corresponding sex group. In parenthesis, the number of animals per experimental group. ANOVA (P<0.05):</p>h<p>significant effect of THC in saline-treated male animals.</p>", "links"=>[], "tags"=>["prepro-orexin"], "article_id"=>841213, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.t005", "stats"=>{"downloads"=>7, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hypothalamic_expression_of_prepro_orexin_transcripts_/841213", "title"=>"Hypothalamic expression of prepro-orexin transcripts.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267201"], "description"=>"<p>Animals were exposed to increasing doses of THC (2.5, 5 and 10 mg/kg or vehicle) from pnd 28 to 45, and twice daily to MDMA (10 mg/kg or saline) every 5 days from pnd 30 to 45 (see text for details). Histograms (mean ± S.E.M.) show the percentage time spent in the open arms (right panel) and the frequency of the closed arm entries (left panel). Number of animals per experimental group: males, Vh-Sal (14), Vh-MDMA (9), THC-Sal (14), THC-MDMA (9); and females, Vh-Sal (14), Vh-MDMA (10), THC-Sal (14), THC-MDMA (5). According to the Kruskal-Wallis test and ANOVA (P<0.05): (a) significant overall effect of sex; (c) significant overall effect of MDMA treatment.</p>", "links"=>[], "tags"=>["elevated", "maze", "performed", "pnd", "holeboard"], "article_id"=>841198, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.g004", "stats"=>{"downloads"=>4, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_elevated_plus_maze_test_was_performed_one_day_after_the_last_drug_administration_on_pnd_46_immediately_after_the_holeboard_test_/841198", "title"=>"The elevated plus maze test was performed one day after the last drug administration, on pnd 46, immediately after the holeboard test.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267198"], "description"=>"<p>Animals were exposed to increasing doses of THC (2.5, 5 and 10 mg/kg or vehicle, i.p.) from pnd 28 to 45, and to MDMA (10 mg/kg or saline, s.c.) twice daily every 5 days from pnd 30 to 45 with an inter-dose interval of 4 h (n = 16 animals per experimental group, see text for details). One day after the last drug administration, on pnd 46, the holeboard test (HB) was performed, immediately followed by the elevated plus maze test (EPM). The novel object test (NOT) was performed on pnd 75, and open-field (OF) data obtained from the first day of habituation to the arena on pnd 71 was also used. The animals were submitted to the prepulse inhibition test (PPI) on pnd 84. Thereafter, around pnd 90 (pnd 89–92), the animals were sacrificed and their brain was collected for future analyses. In addition, blood samples were extracted from the tail vein on pnd 50 for endocrine measurements, and from the trunk at sacrifice.</p>", "links"=>[], "tags"=>[], "article_id"=>841195, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.g001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Timeline_of_the_experimental_design_/841195", "title"=>"Timeline of the experimental design.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267216"], "description"=>"<p>Plasma corticosterone and leptin levels (mean ± SEM, ng/ml), in young adolescent (pnd 50) or adult animals (sacrificed around pnd 90). Animals were exposed to increasing doses of THC (2.5, 5 and 10 mg/kg) or vehicle from pnd 28 to 45, and to MDMA (10 mg/kg) or saline twice daily every 5 days from pnd 30 to 45 (see text for details). In parenthesis, the number of animals per experimental group. ANOVA (P<0.05),</p>a<p>significant overall effect of sex;</p>e<p>significant overall effect of THC within the same sex group;</p>g<p>significant MDMA effect within the same sex group.</p>", "links"=>[], "tags"=>[], "article_id"=>841212, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.t004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Endocrine_measurements_/841212", "title"=>"Endocrine measurements.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267212"], "description"=>"<p>Locomotor and behavioral parameters registered on pnd 71 of male and female animals administered with vehicle (Vh) or increasing doses of THC (2.5, 5 and 10 mg/kg) from pnd 28 to 45, and with saline (Sal) or MDMA (10 mg/kg twice daily) every 5 day from pnd 30 to pnd 45. The data are expressed as the mean ± SEM. In parenthesis, the number of animals per experimental group. ANOVA (P<0.05),</p>a<p>significant overall effect of sex;</p>b<p>significant overall effect of THC;</p>d<p>significant effect of MDMA in vehicle-treated animals.</p>", "links"=>[], "tags"=>[], "article_id"=>841209, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.t003", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_General_activity_in_an_square_arena_/841209", "title"=>"General activity in an square arena.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267210"], "description"=>"<p>Animals were exposed to increasing doses of THC (2.5, 5 and 10 mg/kg) or vehicle from pnd 28 to 45, and to MDMA (10 mg/kg) or saline twice daily every 5 days from pnd 30 to 45 (see text for details). The histograms (mean ± S.E.M.) show the relative change in optical density with respect to the male or female control group. Number of animals per experimental group (n = 4–5). According to ANOVA (P<0.05): (e) significant overall effect of THC within the same sex group; (f) significant MDMA effect among THC-treated animals; (g) significant MDMA effect within the same sex group.</p>", "links"=>[], "tags"=>["activity-regulated", "cytoskeletal-associated", "phosphorylated", "extracellular", "signal-regulated", "kinase", "frontal", "cortex", "hippocampus", "animals", "sacrificed", "pnd"], "article_id"=>841207, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.g007", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Accumulation_of_activity_regulated_cytoskeletal_associated_protein_Arc_upper_panels_and_phosphorylated_extracellular_signal_regulated_kinase_phosphor_ERK1_2_lower_panels_in_the_frontal_cortex_left_panels_and_hippocampus_right_panels_of_adult_animals_sacr/841207", "title"=>"Accumulation of activity-regulated cytoskeletal-associated protein (Arc, upper panels) and phosphorylated extracellular signal-regulated kinase (phosphor-ERK1/2, lower panels) in the frontal cortex (left panels) and hippocampus (right panels) of adult animals sacrificed around pnd 90.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-04 03:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1267211"], "description"=>"<p>Locomotor and explorative activity was registered in the holeboard test on pnd 46 for male and female animals administered with vehicle (Vh) or increasing doses of THC (2.5, 5 and 10 mg/kg) from pnd 28 to 45, and with saline (Sal) or MDMA (10 mg/kg twice daily) every 5 day from pnd 30 (until pnd 45). The data are expressed as the mean ± S.E.M. In parenthesis, the number of animals per experimental group. ANOVA (P<0.05),</p>b<p>significant overall effect of THC;</p>c<p>significant overall effect of MDMA treatment.</p>", "links"=>[], "tags"=>["holeboard"], "article_id"=>841208, "categories"=>["Biological Sciences"], "users"=>["Álvaro Llorente-Berzal", "Emma Puighermanal", "Aurelijus Burokas", "Andrés Ozaita", "Rafael Maldonado", "Eva M. Marco", "María-Paz Viveros"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0078386.t002", "stats"=>{"downloads"=>2, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Locomotor_activity_and_exploration_in_the_holeboard_test_/841208", "title"=>"Locomotor activity and exploration in the holeboard test.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-11-04 03:32:55"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Physiology", "average_usage"=>[256, 449, 572, 676, 775, 866, 955, 1041, 1127, 1213, 1290, 1370, 1437]}, {"subject_area"=>"/Medicine and health sciences", "average_usage"=>[264, 460, 584, 692, 794, 887, 978, 1067, 1154, 1241, 1328, 1408, 1474]}, {"subject_area"=>"/Medicine and health sciences/Physiology", "average_usage"=>[258, 449, 572, 679, 775, 866, 956, 1041, 1124, 1211, 1291, 1371, 1437]}, {"subject_area"=>"/People and places/Population groupings", "average_usage"=>[265, 456, 578, 682, 782, 881, 965, 1053, 1133, 1223, 1310, 1391, 1457]}]}
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