Necessity of Hippocampal Neurogenesis for the Therapeutic Action of Antidepressants in Adult Nonhuman Primates
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{"title"=>"Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult Nonhuman primates", "type"=>"journal", "authors"=>[{"first_name"=>"Tarique D.", "last_name"=>"Perera", "scopus_author_id"=>"7004137068"}, {"first_name"=>"Andrew J.", "last_name"=>"Dwork", "scopus_author_id"=>"7004603066"}, {"first_name"=>"Kathryn A.", "last_name"=>"Keegan", "scopus_author_id"=>"8859093900"}, {"first_name"=>"Lakshmi", "last_name"=>"Thirumangalakudi", "scopus_author_id"=>"13005533600"}, {"first_name"=>"Cecilia M.", "last_name"=>"Lipira", "scopus_author_id"=>"16302170900"}, {"first_name"=>"Niamh", "last_name"=>"Joyce", "scopus_author_id"=>"38461230100"}, {"first_name"=>"Christopher", "last_name"=>"Lange", "scopus_author_id"=>"7202366676"}, {"first_name"=>"J. Dee", "last_name"=>"Higley", "scopus_author_id"=>"7006276835"}, {"first_name"=>"Gorazd", "last_name"=>"Rosoklija", "scopus_author_id"=>"6602542662"}, {"first_name"=>"Rene", "last_name"=>"Hen", "scopus_author_id"=>"7005852886"}, {"first_name"=>"Harold A.", "last_name"=>"Sackeim", "scopus_author_id"=>"7102880523"}, {"first_name"=>"Jeremy D.", "last_name"=>"Coplan", "scopus_author_id"=>"7005374796"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-79954494320", "sgr"=>"79954494320", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0017600", "pmid"=>"21525974", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pui"=>"361627618"}, "id"=>"842296f4-ee38-351b-bd43-1e9d507a623c", "abstract"=>"BACKGROUND: Rodent studies show that neurogenesis is necessary for mediating the salutary effects of antidepressants. Nonhuman primate (NHP) studies may bridge important rodent findings to the clinical realm since NHP-depression shares significant homology with human depression and kinetics of primate neurogenesis differ from those in rodents. After demonstrating that antidepressants can stimulate neurogenesis in NHPs, our present study examines whether neurogenesis is required for antidepressant efficacy in NHPs. MATERIALS/METHODOLOGY: Adult female bonnets were randomized to three social pens (N = 6 each). Pen-1 subjects were exposed to control-conditions for 15 weeks with half receiving the antidepressant fluoxetine and the rest receiving saline-placebo. Pen-2 subjects were exposed to 15 weeks of separation-stress with half receiving fluoxetine and half receiving placebo. Pen-3 subjects 2 weeks of irradiation (N = 4) or sham-irradiation (N = 2) and then exposed to 15 weeks of stress and fluoxetine. Dependent measures were weekly behavioral observations and postmortem neurogenesis levels.\\n\\nRESULTS: Exposing NHPs to repeated separation stress resulted in depression-like behaviors (anhedonia and subordinance) accompanied by reduced hippocampal neurogenesis. Treatment with fluoxetine stimulated neurogenesis and prevented the emergence of depression-like behaviors. Ablation of neurogenesis with irradiation abolished the therapeutic effects of fluoxetine. Non-stressed controls had normative behaviors although the fluoxetine-treated controls had higher neurogenesis rates. Across all groups, depression-like behaviors were associated with decreased rates of neurogenesis but this inverse correlation was only significant for new neurons in the anterior dentate gyrus that were at the threshold of completing maturation.\\n\\nCONCLUSION: We provide evidence that induction of neurogenesis is integral to the therapeutic effects of fluoxetine in NHPs. Given the similarity between monkeys and humans, hippocampal neurogenesis likely plays a similar role in the treatment of clinical depression. Future studies will examine several outstanding questions such as whether neuro-suppression is sufficient for producing depression and whether therapeutic neuroplastic effects of fluoxetine are specific to antidepressants.", "link"=>"http://www.mendeley.com/research/necessity-hippocampal-neurogenesis-therapeutic-action-antidepressants-adult-nonhuman-primates", "reader_count"=>154, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>10, "Researcher"=>35, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>44, "Student > Postgraduate"=>8, "Student > Master"=>15, "Other"=>9, "Student > Bachelor"=>18, "Professor"=>8}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>10, "Researcher"=>35, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>44, "Student > Postgraduate"=>8, "Student > Master"=>15, "Other"=>9, "Student > Bachelor"=>18, "Professor"=>8}, "reader_count_by_subject_area"=>{"Unspecified"=>10, "Agricultural and Biological Sciences"=>61, "Philosophy"=>1, "Earth and Planetary Sciences"=>1, "Economics, Econometrics and Finance"=>1, "Nursing and Health Professions"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Medicine and Dentistry"=>31, "Neuroscience"=>26, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Physics and Astronomy"=>1, "Psychology"=>17, "Linguistics"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>31}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Psychology"=>{"Psychology"=>17}, "Unspecified"=>{"Unspecified"=>10}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Neuroscience"=>{"Neuroscience"=>26}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>61}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Linguistics"=>{"Linguistics"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"Greece"=>1, "Canada"=>2, "United States"=>4, "Japan"=>2, "United Kingdom"=>2, "France"=>1, "Germany"=>2, "Spain"=>1}, "group_count"=>6}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/392546", "https://ndownloader.figshare.com/files/392555", "https://ndownloader.figshare.com/files/392578"], "description"=>"<div><h3>Background</h3><p>Rodent studies show that neurogenesis is necessary for mediating the salutary effects of antidepressants. Nonhuman primate (NHP) studies may bridge important rodent findings to the clinical realm since NHP-depression shares significant homology with human depression and kinetics of primate neurogenesis differ from those in rodents. After demonstrating that antidepressants can stimulate neurogenesis in NHPs, our present study examines whether neurogenesis is required for antidepressant efficacy in NHPs.</p> <h3>Materials/Methodology</h3><p>Adult female bonnets were randomized to three social pens (N = 6 each). Pen-1 subjects were exposed to control-conditions for 15 weeks with half receiving the antidepressant fluoxetine and the rest receiving saline-placebo. Pen-2 subjects were exposed to 15 weeks of separation-stress with half receiving fluoxetine and half receiving placebo. Pen-3 subjects 2 weeks of irradiation (N = 4) or sham-irradiation (N = 2) and then exposed to 15 weeks of stress and fluoxetine. Dependent measures were weekly behavioral observations and postmortem neurogenesis levels.</p> <h3>Results</h3><p>Exposing NHPs to repeated separation stress resulted in depression-like behaviors (anhedonia and subordinance) accompanied by reduced hippocampal neurogenesis. Treatment with fluoxetine stimulated neurogenesis and prevented the emergence of depression-like behaviors. Ablation of neurogenesis with irradiation abolished the therapeutic effects of fluoxetine. Non-stressed controls had normative behaviors although the fluoxetine-treated controls had higher neurogenesis rates. Across all groups, depression-like behaviors were associated with decreased rates of neurogenesis but this inverse correlation was only significant for new neurons in the anterior dentate gyrus that were at the threshold of completing maturation.</p> <h3>Conclusion</h3><p>We provide evidence that induction of neurogenesis is integral to the therapeutic effects of fluoxetine in NHPs. Given the similarity between monkeys and humans, hippocampal neurogenesis likely plays a similar role in the treatment of clinical depression. Future studies will examine several outstanding questions such as whether neuro-suppression is sufficient for producing depression and whether therapeutic neuroplastic effects of fluoxetine are specific to antidepressants.</p> </div>", "links"=>[], "tags"=>["hippocampal", "neurogenesis", "therapeutic", "antidepressants", "nonhuman", "primates"], "article_id"=>137517, "categories"=>["Neuroscience", "Mental Health", "Biophysics"], "users"=>["Tarique D. Perera", "Andrew J. Dwork", "Kathryn A. Keegan", "Lakshmi Thirumangalakudi", "Cecilia M. Lipira", "Niamh Joyce", "Christopher Lange", "J. Dee Higley", "Gorazd Rosoklija", "Rene Hen", "Harold A. Sackeim", "Jeremy D. Coplan"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0017600.s001", "https://dx.doi.org/10.1371/journal.pone.0017600.s002", "https://dx.doi.org/10.1371/journal.pone.0017600.s003"], "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Necessity_of_Hippocampal_Neurogenesis_for_the_Therapeutic_Action_of_Antidepressants_in_Adult_Nonhuman_Primates/137517", "title"=>"Necessity of Hippocampal Neurogenesis for the Therapeutic Action of Antidepressants in Adult Nonhuman Primates", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-04-15 02:05:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/782185"], "description"=>"<p>a. Anhedonia scores. Anhedonia scores showed an effect of group (F<sub>4,65</sub> = 5.6, p = 0.0001), time (F<sub>5,65</sub> = 17.1, p<0.0001), group and time interaction (F<sub>20,65</sub> = 3.4, p = 0.0001). Bonferroni post-hoc tests showed that Stress-Placebo and Radiation-Stress-Drug groups had greater anhedonia compared to Control-Drug, Control-Placebo, and Stress-Drug groups by 13–15 weeks (p<0.01). Error bars represent standard error of mean. b. Hierarchy scores in stressed subjects. Hierarchy (defined as the difference between dominance and subordinance scores) showed an interaction between group and time (F<sub>10, 35</sub> = 2.1, p = 0.04). Bonferroni post-hoc tests showed that the Stress-Drug group had higher hierarchy scores compared to Stress-Placebo (p<0.01) and Radiation-Stress-Drug (p<0.05) by week 13–15. The controls showed no changes in hierarchy over the 15 weeks (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017600#pone.0017600.s001\" target=\"_blank\">Fig.S1</a>). c. Affiliation scores in homecage. Affiliation (physical contact and huddling) showed an effect of group (F<sub>4, 65</sub> = 4.1, p = 0.023) and time (F<sub>5, 65</sub> = 2.6, p = 0.033) and a group by time interaction (F<sub>20, 65</sub> = 2.4, p = 0.005). Bonferroni post-hoc tests showed that the stressed subjects (Stress-Placebo, Stress-Drug, and Radiation-Stress-Drug) had greater affiliation compared to non-stressed subjects (Control-Drug and Control-Placebo) (p<0.05) during most of weeks 1–15.</p>", "links"=>[], "tags"=>["Mental health", "biophysics", "neuroscience"], "article_id"=>452547, "categories"=>["Neuroscience", "Mental Health", "Biophysics"], "users"=>["Tarique D. Perera", "Andrew J. Dwork", "Kathryn A. Keegan", "Lakshmi Thirumangalakudi", "Cecilia M. Lipira", "Niamh Joyce", "Christopher Lange", "J. Dee Higley", "Gorazd Rosoklija", "Rene Hen", "Harold A. Sackeim", "Jeremy D. Coplan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017600.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Behavioral_Results_/452547", "title"=>"Behavioral Results.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:42:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/782413"], "description"=>"<p>a. Neurogenesis rates based on maturational stage and regional distribution Neurogenesis rates at the three maturational stages were divided based on location in the anterior (left panel) or posterior (right panel) dentate gyrus. Multivariate analysis conducted on these six subdivisions showed an overall effect of experimental group (F<sub>4,5</sub> = 90.01, p<0.0001). Univariate analysis of experimental group effects for each of the six sub-divisions of neurogenesis rates revealed significant effects only for Stage 3 neurons in the anterior dentate gyrus (F<sub>4,5</sub> = 22.25, p<0.0001). Bonferroni post-hoc tests showed that only Stage 3 anterior dentate gyrus neurons were reduced in both depressive groups (Stress-Placebo and Stress-Drug-Radiation) compared to non-depressed groups (p<0.05). Data were Log<sub>10</sub> transformed for statistical analysis to correct for uneven variance. b. Correlation between anhedonia scores and neurogenesis rates. Multiple regression analysis was conducted between anhedonia scores obtained at 5 different observation periods and the 6 subdivisions of neurogenesis rates. Anhedonia rates at the final observation period (weeks 13–15) inversely correlated <i>only</i> with Stage 3 anterior dentate gyrus neurons (r<sup>2</sup> = 0.52, p<0.001). Since the regression curve appeared non-linear, a second degree polynomial fit was found to be the best (r<sup>2</sup> = 0.67, p<0.0001). Anhedonia rates at weeks 10–12 inversely correlated with Stage 4 anterior dentate gyrus neurons (r<sup>2</sup> = 0.28, p = 0.02). Likewise, a second-degree polynomial fit was found to be the best (r<sup>2</sup> = 0.34, p<0.01).</p>", "links"=>[], "tags"=>["Mental health", "biophysics", "neuroscience"], "article_id"=>452777, "categories"=>["Neuroscience", "Mental Health", "Biophysics"], "users"=>["Tarique D. Perera", "Andrew J. Dwork", "Kathryn A. Keegan", "Lakshmi Thirumangalakudi", "Cecilia M. Lipira", "Niamh Joyce", "Christopher Lange", "J. Dee Higley", "Gorazd Rosoklija", "Rene Hen", "Harold A. Sackeim", "Jeremy D. Coplan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017600.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Neurogenesis_rates_/452777", "title"=>"Neurogenesis rates.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:46:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/782602"], "description"=>"<p>Two-way ANOVA with Bonferroni post-hoc comparisons showed a significant decrease in granule cell layer volumes of Stress-Placebo and Radiation-Stress-Drug groups when compared with control-placebo (p<0.01).</p>", "links"=>[], "tags"=>["granule"], "article_id"=>452967, "categories"=>["Neuroscience", "Mental Health", "Biophysics"], "users"=>["Tarique D. Perera", "Andrew J. Dwork", "Kathryn A. Keegan", "Lakshmi Thirumangalakudi", "Cecilia M. Lipira", "Niamh Joyce", "Christopher Lange", "J. Dee Higley", "Gorazd Rosoklija", "Rene Hen", "Harold A. Sackeim", "Jeremy D. Coplan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017600.g005", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Volume_of_granule_cell_layer_/452967", "title"=>"Volume of granule cell layer.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:49:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/782521"], "description"=>"<p>Log<sub>10</sub> transformed rates of BrdU-labeled cells in the SGZ did not show an effect of experimental group (F<sub>4,13</sub> = 1.7, p = 0.46). b. Right panel: Precursor cell proliferation rates. Hippocampal cell proliferation rates at the time of sacrifice were identified by the expression of Ki67. Log<sub>10</sub> transformed rates of Ki67 expressing cells showed an overall effect of group (F<sub>4,13</sub> = 6.8, p<0.001) stemming from decreased counts in Stress-Placebo compared to all other groups per Bonferroni post-hoc tests (p<0.01). b Left panel: Maturational fate of BrdU-labeled cells on week 7. The percentage of BrdU-labeled cells that co-labeled with NeuN was designated as new neurons and BrdU-labeled cells that co-labeled with Iba-1 were designated as microglia. Two-way ANOVA showed an overall interaction between group and maturational stage (P<0.0001), as well as an effect of group (p = 0.036), and maturational fate (p<0.0001). Bonferroni post-hoc tests showed greater levels of BrdU-NeuN co-labeling (p<0.01) and lower levels of BrdU-Iba-1 co-labeling (P<0.001) in the 4 non-irradiated subjects (Control-Drug, Control-Placebo, Stress-Drug, and Stress-Placebo) compared to irradiated subjects (Radiation-Stress-Drug group).</p>", "links"=>[], "tags"=>["precursor", "brdu-labeling", "represented", "proliferating", "hippocampal", "precursors", "took", "brdu", "week-7", "survived"], "article_id"=>452867, "categories"=>["Neuroscience", "Mental Health", "Biophysics"], "users"=>["Tarique D. Perera", "Andrew J. Dwork", "Kathryn A. Keegan", "Lakshmi Thirumangalakudi", "Cecilia M. Lipira", "Niamh Joyce", "Christopher Lange", "J. Dee Higley", "Gorazd Rosoklija", "Rene Hen", "Harold A. Sackeim", "Jeremy D. Coplan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017600.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_a_Left_panel_Precursor_cell_survival_rates_BrdU_labeling_represented_proliferating_hippocampal_precursors_that_took_up_BrdU_on_week_7_and_survived_until_sacrifice_on_week_15_/452867", "title"=>"a. Left panel: Precursor cell survival rates. BrdU-labeling represented proliferating hippocampal precursors that took up BrdU on week-7 and survived until sacrifice on week-15.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:47:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/782284"], "description"=>"<p>a. Doublecortin-expressing cells in the SGZ at different stages of maturation. Stage 1. Immature neurons that lack dendrites, or have short dendrites that lack branches. Stage 2. Differentiating neurons with dendrites that have secondary branches and extend no further than the inner molecular layer. Stage 3. Neurons with dendrites that have tertiary branches and extend into the outer molecular layer. b. Confocal image of BrdU-NeuN co-labeled cells. Stage 4 BrdU-labeled cells (green) that also express the mature neuronal marker NeuN (red) with the overlayed images of NeuN and BrdU labeling (yellow).</p>", "links"=>[], "tags"=>["doublecortin-expressing", "neurons", "stages", "maturation", "brdu-neun", "co-labeled"], "article_id"=>452643, "categories"=>["Neuroscience", "Mental Health", "Biophysics"], "users"=>["Tarique D. Perera", "Andrew J. Dwork", "Kathryn A. Keegan", "Lakshmi Thirumangalakudi", "Cecilia M. Lipira", "Niamh Joyce", "Christopher Lange", "J. Dee Higley", "Gorazd Rosoklija", "Rene Hen", "Harold A. Sackeim", "Jeremy D. Coplan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017600.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Images_of_Doublecortin_expressing_new_neurons_at_different_stages_of_maturation_and_BrdU_NeuN_co_labeled_cells_/452643", "title"=>"Images of Doublecortin-expressing new neurons at different stages of maturation and BrdU-NeuN co-labeled cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-04-15 00:44:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/782741"], "description"=>"<p>Study Design: Schematic illustrating study design and schedule.</p>", "links"=>[], "tags"=>["schematic", "illustrating"], "article_id"=>453098, "categories"=>["Neuroscience", "Mental Health", "Biophysics"], "users"=>["Tarique D. Perera", "Andrew J. Dwork", "Kathryn A. Keegan", "Lakshmi Thirumangalakudi", "Cecilia M. Lipira", "Niamh Joyce", "Christopher Lange", "J. Dee Higley", "Gorazd Rosoklija", "Rene Hen", "Harold A. Sackeim", "Jeremy D. Coplan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017600.t001", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Study_Design_Schematic_illustrating_study_design_and_schedule_/453098", "title"=>"Study Design: Schematic illustrating study design and schedule.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-04-15 00:51:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/782693"], "description"=>"<p>Behavioral Categories: Set of 40 behaviors observed during home cage ratings were collapsed into eight subscales for behavioral analysis.</p>", "links"=>[], "tags"=>["40", "behaviors", "observed", "ratings", "collapsed", "subscales"], "article_id"=>453048, "categories"=>["Neuroscience", "Mental Health", "Biophysics"], "users"=>["Tarique D. Perera", "Andrew J. Dwork", "Kathryn A. Keegan", "Lakshmi Thirumangalakudi", "Cecilia M. Lipira", "Niamh Joyce", "Christopher Lange", "J. Dee Higley", "Gorazd Rosoklija", "Rene Hen", "Harold A. Sackeim", "Jeremy D. Coplan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017600.t002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Behavioral_Categories_Set_of_40_behaviors_observed_during_home_cage_ratings_were_collapsed_into_eight_subscales_for_behavioral_analysis_/453048", "title"=>"Behavioral Categories: Set of 40 behaviors observed during home cage ratings were collapsed into eight subscales for behavioral analysis.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-04-15 00:50:48"}

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