The Somatostatin 2A Receptor Is Enriched in Migrating Neurons during Rat and Human Brain Development and Stimulates Migration and Axonal Outgrowth
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{"title"=>"The somatostatin 2A receptor is enriched in migrating neurons during rat and human brain development and stimulates migration and axonal outgrowth", "type"=>"journal", "authors"=>[{"first_name"=>"Virginia", "last_name"=>"Le Verche", "scopus_author_id"=>"24280182300"}, {"first_name"=>"Angela M.", "last_name"=>"Kaindl", "scopus_author_id"=>"6701719236"}, {"first_name"=>"Catherine", "last_name"=>"Verney", "scopus_author_id"=>"7003701111"}, {"first_name"=>"Zsolt", "last_name"=>"Csaba", "scopus_author_id"=>"55980221700"}, {"first_name"=>"Stéphane", "last_name"=>"Peineau", "scopus_author_id"=>"6506158176"}, {"first_name"=>"Paul", "last_name"=>"Olivier", "scopus_author_id"=>"16043146700"}, {"first_name"=>"Homa", "last_name"=>"Adle-Biassette", "scopus_author_id"=>"55903937800"}, {"first_name"=>"Christophe", "last_name"=>"Leterrier", "scopus_author_id"=>"12792195500"}, {"first_name"=>"Tania", "last_name"=>"Vitalis", "scopus_author_id"=>"6701352870"}, {"first_name"=>"Julie", "last_name"=>"Renaud", "scopus_author_id"=>"23028965200"}, {"first_name"=>"Bénédicte", "last_name"=>"Dargent", "scopus_author_id"=>"6701705268"}, {"first_name"=>"Pierre", "last_name"=>"Gressens", "scopus_author_id"=>"15042308300"}, {"first_name"=>"Pascal", "last_name"=>"Dournaud", "scopus_author_id"=>"6603926666"}], "year"=>2009, "source"=>"PLoS ONE", "identifiers"=>{"isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "issn"=>"19326203", "pui"=>"354587768", "pmid"=>"19434240", "doi"=>"10.1371/journal.pone.0005509", "sgr"=>"65649089512", "scopus"=>"2-s2.0-65649089512"}, "id"=>"c1303a5e-3003-3854-922a-3d2819d0de65", "abstract"=>"The neuropeptide somatostatin has been suggested to play an important role during neuronal development in addition to its established modulatory impact on neuroendocrine, motor and cognitive functions in adults. Although six somatostatin G protein-coupled receptors have been discovered, little is known about their distribution and function in the developing mammalian brain. In this study, we have first characterized the developmental expression of the somatostatin receptor sst2A, the subtype found most prominently in the adult rat and human nervous system. In the rat, the sst2A receptor expression appears as early as E12 and is restricted to post-mitotic neuronal populations leaving the ventricular zone. From E12 on, migrating neuronal populations immunopositive for the receptor were observed in numerous developing regions including the cerebral cortex, hippocampus and ganglionic eminences. Intense but transient immunoreactive signals were detected in the deep part of the external granular layer of the cerebellum, the rostral migratory stream and in tyrosine hydroxylase- and serotonin- positive neurons and axons. Activation of the sst2A receptor in vitro in rat cerebellar microexplants and primary hippocampal neurons revealed stimulatory effects on neuronal migration and axonal growth, respectively. In the human cortex, receptor immunoreactivity was located in the preplate at early development stages (8 gestational weeks) and was enriched to the outer part of the germinal zone at later stages. In the cerebellum, the deep part of the external granular layer was strongly immunoreactive at 19 gestational weeks, similar to the finding in rodents. In addition, migrating granule cells in the internal granular layer were also receptor-positive. Together, theses results strongly suggest that the somatostatin sst2A receptor participates in the development and maturation of specific neuronal populations during rat and human brain ontogenesis.", "link"=>"http://www.mendeley.com/research/somatostatin-2a-receptor-enriched-migrating-neurons-during-rat-human-brain-development-stimulates-mi", "reader_count"=>25, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>4, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>3, "Student > Bachelor"=>1, "Professor"=>1, "Other"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>4, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>3, "Student > Bachelor"=>1, "Professor"=>1, "Other"=>1}, "reader_count_by_subject_area"=>{"Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>18, "Medicine and Dentistry"=>2, "Neuroscience"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Psychology"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>1}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>18}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Argentina"=>1, "Brazil"=>2, "France"=>1, "Germany"=>1}, "group_count"=>0}

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/901487"], "description"=>"<p>A) Representative image of an external granular layer (EGL) microexplant after 3 days <i>in vitro</i> in culture. The core of the explant and surrounding scattered migrating granules cells are labeled with DAPI (blue). Neuronal processes are labeled by neuronal class III β-tubulin immunoreactivity (green). B) In individual granule cells, sst2A receptor immunoreactivity is visible in both neuronal perikarya and processes (red). C) Illustration of sst2A receptor immunolabeling (red) in a β-tubulin-immunoreactive (green) axon. Note the sst2A-immunoreactive puncta in a growth cone structure (arrow). D, E) In comparison to control (D) the number of migrating granule cells is significantly increased in 100 nm octreotide-treated EGL (E) microexplants. The octreotide-induced granule cell migration increase is dose-dependent as revealed by quantitative analysis (F). *p<0.05; **p<0.01; ***p<0.001. Values represent mean±SEM. Scale bars: A, D, E, 500 µm; B, C, 10 µm.</p>", "links"=>[], "tags"=>["sst2a", "receptor", "activation", "granule"], "article_id"=>571929, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g014", "stats"=>{"downloads"=>1, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_sst2A_receptor_activation_on_in_vitro_granule_cell_migration_/571929", "title"=>"Effect of sst2A receptor activation on <i>in vitro</i> granule cell migration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:15:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/900827"], "description"=>"<p>A–A″) Intensely labeled sst2A receptor-immunoreactive neurons (red in A′–A″) form chain-like clusters in the middle part of the cortical plate (CP). Note that long sst2A receptor-immunoreactive radial processes reach the pial surface (PS). B–B″) Receptor-immunolabeled cells and processes (red in B, B″) are closely apposed by vimentin-positive processes (green in B′B″), suggesting migration of sst2A-labeled cells on radial glia. C–C″) Sst2A receptor-immunoreactive processes (red in C, C″) are contacted by fibers that are immunoreactive for SRIF (green in D, D″) (arrowheads), the endogen ligand of the receptor. Scale bars: 20 µm.</p>", "links"=>[], "tags"=>["cellular", "sst2a", "receptor", "immunofluorescence", "cerebral", "cortex", "gw"], "article_id"=>571269, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g011", "stats"=>{"downloads"=>2, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regional_and_cellular_distribution_of_the_sst2A_receptor_immunofluorescence_in_the_human_cerebral_cortex_at_GW_19_/571269", "title"=>"Regional and cellular distribution of the sst2A receptor immunofluorescence in the human cerebral cortex at GW 19.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:12:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/899754"], "description"=>"<p>A) At E16, intense sst2A receptor immunoreactivity is observed in the substantia nigra (SN; boxed area) and along the medial forebrain bundle (mfb; arrowhead). B–B″) At E16, the sst2A receptor (red in B, B″) and tyrosine hydroxylase (TH) (green in B′, B″) immunoreactivities extensively overlap both in the SN and in emerging processes of the mfb. C–C″) At E18, sst2A receptor immunoreactivity is dramatically decreased in both the SN and the mfb. D–D″) High magnification microscopic images illustrate numerous sst2A receptor-immunoreactive fibers (red in D,D′) in the mfb at E16. Some of them are TH-positive (green in D′,D″) (arrowheads). E–E″) Some sst2A receptor-immunolabeled axons (red in E, E″) of the mfb express 5-HT (green in E′, E″) (arrowheads). F,G) Pre-embedding immunogold immunohistochemistry of the sst2A receptor in the mfb at E16 illustrates very high density of immunoparticles in axons (F) and growth cone-like structures (G). Note that although the majority of immunoparticles are intracellular, some are found associated to the plasma membrane. H) At E14, intense sst2A receptor immunolabeling is observed on sagittal sections in the developing hypothalamus (boxed area). I) Illustration of receptor immunoreactivity on coronal section at the level of hypothalamic area at E16. Note the receptor immunoreactivity in the caudal ganglionic eminence (CGE) (arrow). J,K) J represents magnification of boxed area in I. At high magnification, sst2A receptor immunoreactivity is found at the periphery of numerous hypothalamic neurons. III, third ventricle; HA, hypothalamic area. Scale bars: A, 500 µm; B–B″, C–C″, 50 µm; D–D″, E–E″, J, 20 µm; F, G, 1 µm; H, 250 µm; I, 200 µm; K, 10 µm.</p>", "links"=>[], "tags"=>["cellular", "subcellular", "localization", "sst2a", "receptor", "immunoreactivity", "sagittal", "coronal", "sections", "mesencephalon", "diencephalon", "e14"], "article_id"=>570185, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g006", "stats"=>{"downloads"=>2, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regional_cellular_and_subcellular_localization_of_sst2A_receptor_immunoreactivity_on_sagittal_A_8211_H_and_coronal_I_8211_K_sections_of_the_rat_mesencephalon_and_diencephalon_between_E14_and_E18_/570185", "title"=>"Regional, cellular and subcellular localization of sst2A receptor immunoreactivity on sagittal (A–H) and coronal (I–K) sections of the rat mesencephalon and diencephalon between E14 and E18.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:06:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/901285"], "description"=>"<p>A–A″) In sagittal sections at P0, an intense band of sst2A receptor immunoreactivity is observed from the anterior subventricular zone (SVZa), through the rostral migratory stream (RMS) and ending in the olfactory bulb (OB). From the SVZa, shown in detail in the high magnification insets, chains of immunoreactive neurons perpendicular to the SVZa long axis extend into the white matter of the overlying cerebral cortex. B–B″ represents high magnification of the area labeled with asterisk in A. The sst2A receptor immunoreactive cells are principally localized along the ventral and dorsal surface of RMS. C) High magnification of sst2A receptor immunoreactivity at the entrance of RMS into the olfactory bulb at P5 illustrates immunoreactive cells at the surface of the stream as well as embedded in central position. D) In the dorsal part of the RMS, sst2A receptor-immunoreactive cells (red) contain NeuN labeling in their nuclei (green; arrowhead). E) Sst2A receptor- (red) and NeuN- (blue) double-labeled cells (arrowhead) of the RMS do not contain BrdU immunoreactivity (green), demonstrating that receptor expression is restricted to post-mitotic neurons. Scale bars: A–A″, 500 µm; B–B″, C, 100 µm; D, 20 µm; E, 10 µm.</p>", "links"=>[], "tags"=>["sst2a", "receptor", "perinatal", "rostral", "migratory"], "article_id"=>571728, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g013", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immunofluorescence_of_sst2A_receptor_in_the_rat_perinatal_rostral_migratory_stream_/571728", "title"=>"Immunofluorescence of sst2A receptor in the rat perinatal rostral migratory stream.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:14:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/899058"], "description"=>"<p>A) At E14, sst2A receptor immunoreactivity is detected in the developing cerebellum (boxed area). Note the strong expression of the receptor in the developing hypothalamus (arrowhead) and rhombencephalon (asterisk). B) The sst2A receptor immunoreactivity is intense at the outer border of the cerebellar neuroepithelium (asterisk) and the adjacent upper component of the rhombic lip (rl). C) At E16, strong cellular sst2A receptor labeling is evident in the dorsal part of the cerebellum, where the progenitors of the external granular layer (EGL) migrate. D,E) Pre-embedding immunogold immunohistochemistry of the sst2A receptor in the developing external germinal layer at E16 illustrates that immunoparticles are predominantly localized at the internal surface of the plasma membrane (arrowheads). F,G) High magnification confocal microscopic analysis of the developing EGL reveals redistribution of surface receptors to intracellular compartments upon agonist stimulation. In control conditions, sst2A receptor immunoreactivity outlines the periphery of neurons (F). Forty minutes after agonist administration, accumulation of immunoreactive puncta in the cytoplasm become evident (G). H) At P5, intense sst2A receptor immunofluorescence is observed in the EGL. I–I″ represent magnification of boxed area in H. The sst2A receptor-immunoreactive neurons (red) are predominantly located in the deep part of EGL (I). The Ki-67-immuonreactive proliferative neurons (green) are distributed predominantly in the superficial EGL (I′). Accordingly only few sst2A receptor-immunoreactive neurons are Ki-67-positive (I″; arrowheads). J–J″) In the EGL, most sst2A receptor-immunolabeled neurons (red in J, J″) are positive for the neuronal-specific nuclear protein NeuN (green in J′, J″) (arrowheads) and demonstrate the post-mitotic nature of sst2A-positive EGL neurons. K, K″) At P5, the large unipolar calretinin-immunoreactive brush cells (green in K′, K″) are sst2A receptor immunoreactive (red in K, K″). Note the colocalization of sst2A receptor and calretinin in a long brush cell process (arrowhead). cb, cerebellar neuroepithelium; CB, cerebellum. Scale bars: A, 250 µm; B, H, K–K″, 50 µm; C, 20 µm, D, 200 nm; E, 400 nm. F, G, I–I″, J–J″, 10 µm.</p>", "links"=>[], "tags"=>["cellular", "subcellular", "sst2a", "receptor", "immunoreactivity", "sagittal", "sections", "cerebellum", "pre-", "postnatal"], "article_id"=>569490, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g003", "stats"=>{"downloads"=>1, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regional_cellular_and_subcellular_distribution_of_sst2A_receptor_immunoreactivity_in_sagittal_sections_of_the_rat_cerebellum_during_pre_and_postnatal_development_/569490", "title"=>"Regional, cellular and subcellular distribution of sst2A receptor immunoreactivity in sagittal sections of the rat cerebellum during pre- and postnatal development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:02:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/900205"], "description"=>"<p>A–A″′) At E14, the sst2A receptor immunoreactivity is detected in the preplate (PP). Receptor immunoreactivity is observed in cell bodies and basal processes perpendicular to the pial surface (A″′). B–B″′) At E16, intense receptor immunoreactivity is confined to neuronal cells located in the subplate/intermediate zone (SP/IZ; defined by arrowheads). Immunolabeling is located in cell bodies and small processes of closely packed and presumably migrating neurons (B″′). C–C″′) At E18, the sst2A receptor immunoreactivity is confined to cells in the intermediate zone but absent from the adjacent subplate (defined by arrowheads). D–D″′) At E21, sst2A receptor immunoreactivity is concentrated in the subventricular zone (SVZ) and the adjacent deep part of IZ. Immunoreactivity is apparent in cell bodies and radially oriented processes (D, D″′). E) At P5, the sst2A receptor immunoreactivity is diffusely distributed over the neuropil. The labeling intensity decreases towards the deep layers. At high magnification, receptor immunoreactivity appears diffusely distributed within the neuropil (E″′). A″′, B″′, C″′, D″′ and E″′ represent magnifications of boxed areas on A″, B″, C″, D″ and E″, respectively. CP/MZ, cortical plate/marginal zone; CP, cortical plate; MZ, marginal zone; VZ, ventricular zone; I–VI, cortical layers I to VI; WM, white matter. Scale bars: A–A″, B–B″, 50 µm; C–C″, D–D″, E–E″, 100 µm; A″′–E″′,10 µm.</p>", "links"=>[], "tags"=>["sst2a", "receptor", "coronal", "sections", "neocortical", "e14"], "article_id"=>570646, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g008", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immunofluorescence_of_the_sst2A_receptor_in_coronal_sections_through_the_rat_neocortical_wall_between_E14_and_P5_/570646", "title"=>"Immunofluorescence of the sst2A receptor in coronal sections through the rat neocortical wall between E14 and P5.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:08:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/898797"], "description"=>"<p>A) Triple-labeling with sst2A receptor (red), 5-HT (green) and DAPI (blue) in the ventral part of the brainstem illustrates that most serotoninergic neurons are sst2A receptor immunoreactive. B,B′ represent magnification of the boxed area in A. Note the extensive colocalization of sst2A receptor and 5-HT in both cell bodies and processes. C) The sst2A receptor is also expressed in serotoninergic migrating cells in the more dorsal part of the mesencephalon presumably corresponding to the dorsal raphe nucleus. D,D′ represents magnification of the boxed area in C and illustrates double-labeling in both the soma and processes of migrating neurons. Scale bars: A, C, 50 µm; B, D, 20 µm.</p>", "links"=>[], "tags"=>["sst2a", "receptor", "serotoninergic", "neurons", "brainstem"], "article_id"=>569239, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g002", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_the_sst2A_receptor_in_serotoninergic_neurons_of_the_rat_brainstem_at_E16_/569239", "title"=>"Expression of the sst2A receptor in serotoninergic neurons of the rat brainstem at E16.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:01:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/899963"], "description"=>"<p>A,B) Intense sst2A receptor immunoreactivity is detected at E16 in the post-mitotic areas of the lateral ganglionic eminence (LGE) and the caudal ganglionic eminence (CGE) (B). Note the presence of sst2A receptor immunoreactivity in the cortex (cx) and hippocampus (hi). C represents magnification of boxed area in B and illustrates that the sst2A receptor immunoreactivity is found in cell bodies and short processes in the CGE. D,E) Pre-embedding immunogold immunohistochemistry of the sst2A receptor in the CGE illustrates that high density of immunoparticles are localized intracellularly. However, sst2A receptor-immunoreactive particles are also found in association with the plasma membrane (arrowheads in D). Note that in a neuronal process the majority of the immunoparticles are membrane-associated (arrowheads in E). F represents magnification of the boxed area in A. Numerous cells are immunoreactive for sst2A in the LGE. G represents high magnification of the area labeled with an arrow on A and illustrates that fibers are also sst2A receptor-immunolabeled. H,I) High magnification confocal microscopic analysis in the CGE demonstrates redistribution of receptors upon agonist stimulation. In control conditions, sst2A receptor immunoreactivity outlines the periphery of cells (H). Forty minutes after agonist administration, receptor immunoreactivity is confined to small puncta in the cytoplasm (I). J,K) At E18, intense sst2A receptor immunoreactivity is observed in the dorso-medial part of the caudate-putamen in rostral (J) and caudal (K) sections close to the ventricular surface. Scattered sst2A receptor immunoreactivity is also evident in the medial part of the developing caudate-putamen (asterisk). L represents magnification of boxed area on J. The sst2A receptor immunoreactivity is observed in large number of cells and their short processes in the dorsal caudate-putamen. Note the lack of sst2A receptor immunoreactivity in the subventricular zone (SVZ). M,N are high magnifications from the area labeled with asterisk on J. The sst2A receptor is expressed in neuronal perikarya and processes in the medial part of the caudate-putamen. Scale bars: A, B, 200 µm; C, F, G, L, 20 µm; D, 500 nm; E, 250 nm; H, I, M, N, 10 µm; J, K, 500 µm.</p>", "links"=>[], "tags"=>["cellular", "subcellular", "sst2a", "receptor", "immunoreactivity", "coronal", "sections", "telencephalon", "e16"], "article_id"=>570392, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g007", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regional_cellular_and_subcellular_distribution_of_sst2A_receptor_immunoreactivity_on_coronal_sections_of_the_rat_telencephalon_at_E16_and_E18_/570392", "title"=>"Regional, cellular and subcellular distribution of sst2A receptor immunoreactivity on coronal sections of the rat telencephalon at E16 and E18.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:07:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/898563"], "description"=>"<p>A) Densely packed sst2A receptor-immunoreactive cells are observed in the marginal zone contiguous to the ventricular zone of the rhombomeres (r1 to r6, arrowheads) and in the lateral reticular formation (LRtF). B–B″) Sst2A receptor-immunoreactive cells (red) are localized in the marginal zone (B) whereas proliferating cells identified by the proliferation marker Ki-67 (green) are concentrated in the ventricular zone (B′). The lack of overlap between the two signals (B″) indicates that sst2A receptor-expressing cells are predominantly post-mitotic. C) The majority of sst2A receptor-immunoreactive cells have small round perikarya and some exhibit immunolabeled processes that are oriented perpendicularly to the ventricular surface. D) A few sst2A receptor-immunoreactive cells are bipolar, displaying the morphological features of migrating neurons. E) In the LRtF, cell bodies are strongly sst2A receptor-immunoreactive. F–F″) An sst2A receptor-immunoreactive cell (red in F, F″) of the LRtF is found to be Ki-67-positive (green in F′, F″) (arrowheads). The low percentage of colocalization (F″) indicates that the majority of receptor-expressing cells are post-mitotic. G–G″) The post-mitotic feature of most sst2A receptor-immunoreactive cells (red in G, G″) of the rhombencephalon is further indicated by the colocalization (G″) with the post-mitotic neuronal marker β-tubulin (green in G′, G″) (arrowheads), as illustrated in the facial nucleus. Scale bars: A, 250 µm; B–B″, G–G″, 50 µm; C, E, 20 µm; F, 10 µm.</p>", "links"=>[], "tags"=>["cellular", "localization", "sst2a", "receptor", "immunoreactivity", "sagittal", "sections", "rhombencephalon", "embryonic", "13"], "article_id"=>568985, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g001", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regional_and_cellular_localization_of_the_sst2A_receptor_immunoreactivity_in_sagittal_sections_of_the_rat_rhombencephalon_at_embryonic_day_13_E13_/568985", "title"=>"Regional and cellular localization of the sst2A receptor immunoreactivity in sagittal sections of the rat rhombencephalon at embryonic day 13 (E13).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 05:59:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/899443"], "description"=>"<p>A) At GW 19, intense receptor immunoreactivity (red in A, A″) is observed in the deep part of the external granular layer (EGL). Note the large number of DAPI-positive cell nuclei (blue in A′, A″) in the superficial EGL. B–B″′ represent high magnification of boxed area in A. The sst2A receptor immunoreactivity (red in B, B″′) is mainly distributed in the deep part of the EGL whereas SRIF-immunoreactive cells (green in B′, B″′) are mainly located in the deep part of the molecular layer (ML). C–C″′) At GW 20, the high density sst2A receptor immunoreactivity (red in C, C″′) in the deep EGL is still present. In addition, intense receptor immunolabeling is detected in the internal granular layer (IGL; asterisk) and overlap with NeuN-immunoreactive cells (green in C′–C″′). D represents magnification of boxed area in C. The sst2A receptor is expressed in cells bodies located in the deep part of the EGL. E–E″′) In the IGL, the vast majority of NeuN- (green in E′, E″′) and DAPI- (blue in E″, E″′) positive cell nuclei are outlined by sst2A receptor immunoreactivity (red in E, E″′) (arrowheads), suggesting that the receptor is expressed by migrating granule cells. Scale bars: A–A″, C–C″′, 100 µm; B–B″′, D, E–E″′, 20 µm.</p>", "links"=>[], "tags"=>["cellular", "sst2a", "receptor", "immunoreactivity", "coronal", "sections", "prenatal"], "article_id"=>569887, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g005", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regional_and_cellular_distribution_of_sst2A_receptor_immunoreactivity_on_coronal_sections_of_the_prenatal_human_cerebellum_/569887", "title"=>"Regional and cellular distribution of sst2A receptor immunoreactivity on coronal sections of the prenatal human cerebellum.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:04:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/900404"], "description"=>"<p>A–C) Pre-embedding immunogold immunohistochemistry of the sst2A receptor in the developing cortex at E16 demonstrates localization of immunoparticles at the internal surface of the plasma membrane (arrowheads). D,E) High magnification confocal microscopic analysis reveals agonist-induced redistribution of surface receptors to intracellular compartments. In control conditions, sst2A receptor immunoreactivity outlines the periphery of cells (D). Forty minutes after agonist administration, accumulation of immunoreactive puncta in the cytoplasm become evident (E). Scale bars, A, C, 500 nm; B, 1 µm; D, E, 10 µm.</p>", "links"=>[], "tags"=>["localization", "sst2a", "receptor", "immunoreactivity", "neocortical", "cells"], "article_id"=>570848, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g009", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Subcellular_localization_of_sst2A_receptor_immunoreactivity_in_neocortical_cells_at_E16_/570848", "title"=>"Subcellular localization of sst2A receptor immunoreactivity in neocortical cells at E16.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:09:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/901627"], "description"=>"<p>A–A″) Representative image of sst2A receptor localization in a primary hippocampal cell after 24 h <i>in vitro</i> in culture. Receptor immunoreactivity (green in A, A″) is present in the cell body and processes. Cell morphology is revealed by actin-binding protein phalloidin (red in A′, A″). Note that sst2A receptor immunoreactivity is also present in growth cones (insets in A–A″). B–D) Representative images of neurons from control (ctrl; B), 10 nM octreotide-treated (10 nM oct.; C) and 50 nM octreotide-treated (50 nM oct.; D) cultures. Arrows depict the axonal process which appears longer when cells are treated with 50 nM octreotide. E) Quantitative analysis reveals that the axon length (right panel) is significantly increased in the 50 nM oct. group when compared to the control group. The mean cell body surface (left panel) and the mean dendritic length (middle panel) are not modified by sst2A receptor agonist treatments. Values (mean±SEM) are expressed in relation to an arbitrary unit (100%) of the control values. *p<0.05; ns, not significant. Scale bars: A–A″, B–D, 20 µm.</p>", "links"=>[], "tags"=>["sst2a", "receptor", "agonist", "axonal", "dendritic"], "article_id"=>572072, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g015", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_sst2A_receptor_agonist_on_axonal_and_dendritic_patterning_/572072", "title"=>"Effect of sst2A receptor agonist on axonal and dendritic patterning.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:16:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/901758"], "description"=>"<p>List of Primary Antibodies.</p>", "links"=>[], "tags"=>["cell biology/cell signaling", "cell biology/neuronal and glial cell biology", "neuroscience/neurodevelopment", "neuroscience/neuronal and glial cell biology", "neuroscience/neuronal signaling mechanisms", "neurological disorders/developmental and pediatric neurology", "neurological disorders/epilepsy"], "article_id"=>572201, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.t001", "stats"=>{"downloads"=>2, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_List_of_Primary_Antibodies_/572201", "title"=>"List of Primary Antibodies.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 06:17:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/899206"], "description"=>"<p>(A) At E18, strong sst2A receptor immunoreactivity is found not only in the rhombic lip (rl) and external granular layer (EGL) but also in the rostro-ventral part of the cerebellum between the cerebellar ventricular area (IV) and the ventral hindbrain (boxed area). B–B″) The large, elongated sst2A receptor-immunoreactive cells (red in B, B″) lie parallel with the ventricular surface. These neurons also express tyrosine hydroxylase (TH; green in B′, B″), a marker of catecholaminergic neurons. C) At E21, intense sst2A receptor immunoreactivity (red in C, C″) is observed in the developing locus coeruleus (LC) and overlap with TH immunolabeling (green in D′,D″). D represents high magnification of boxed area in C. Note that intense sst2A receptor immunoreactivity (red) outlines the periphery of TH-positive (green) neurons (arrowheads). E) At P3, the locus coeruleus exhibits also strong sst2A receptor immunoreactivity (red). The blue labeling represents DAPI staining. CB, cerebellum; IV, fourth ventricle. Scale bars: A, 200 µm; B–B″, C–C″, E, 100 µm; D–D″, 20 µm.</p>", "links"=>[], "tags"=>["cellular", "sst2a", "receptor", "immunoreactivity", "locus"], "article_id"=>569648, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regional_and_cellular_distribution_of_sst2A_receptor_immunoreactivity_in_the_rat_developing_locus_coeruleus_/569648", "title"=>"Regional and cellular distribution of sst2A receptor immunoreactivity in the rat developing locus coeruleus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:03:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/901062"], "description"=>"<p>A–A″) At E16, sst2A receptor immunoreactivity (red in A, A″) is localized in the intermediate zone (IZ) of the hippocampus. Note the lack of immunoreactivity in the ventricular zone (VZ). B–B″) At E21, the most intense immunolabeling is found in the intermediate zone of CA1. In addition, less intense immunolabeling is apparent in the pyramidal cell layer as well as in the strata oriens and radiatum of CA1, in the CA3 and in the developing dentate gyrus (DG). C) In the hilus of the DG, sst2A receptor immunoreactivity appears diffusely distributed. D represents magnification of the area labeled with asterisk in B and illustrates the diffuse sst2A receptor immunolabeling observed in the CA1 pyramidal cell layer. E represents magnification of boxed area in B. The sst2A receptor immunolabeling is intense in cells of the IZ whereas the subventricular zone (SVZ) is devoid of labeling. F) At P3, intense immunofluorescence is detected in the pyramidal layer, strata oriens and radiatum of CA1-3, as well as in the hilus of DG. The molecular layer of dentate gyrus is weakly immunoreactive. G represents magnification of boxed area in F and illustrates the intense sst2A receptor immunolabeling localized in CA1 pyramidal cell bodies and proximal dendrites. H represents magnification of area labeled with asterisk in F and illustrates the diffuse sst2A receptor immunolabeling observed in the hilus of the DG. Scale bars: A–A″, B–B″, F, 100 µm; C, D, E, G, H, 20 µm.</p>", "links"=>[], "tags"=>["sst2a", "receptor", "immunoreactivity", "hippocampus", "pre-", "postnatal"], "article_id"=>571506, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g012", "stats"=>{"downloads"=>2, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_the_sst2A_receptor_immunoreactivity_in_the_rat_hippocampus_during_pre_and_postnatal_development_/571506", "title"=>"Distribution of the sst2A receptor immunoreactivity in the rat hippocampus during pre- and postnatal development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:13:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/900617"], "description"=>"<p>A,B) Embryonic sagittal sections at GW 8 at the level of the medial cerebral cortex (A) reveals numerous receptor immunoreactive cell bodies (purple color) in the preplate (PP) (inset box) and in the subventricular zone (SVZ). By contrast the ventricular zone (VZ) is devoid of receptor immunoreactivity. The red color is due to the counterstaining of sections with neutral red. In the lateral part of the medial cerebral cortex (B), sst2A receptor immunoreactivity is detected in the marginal zone (MZ), cortical plate (CP), subplate/intermediate zone (SP/IZ) and SVZ (inset box). C–E) At GW 12 in coronal sections, albeit less intense, the pattern of receptor immunoreactivity is comparable to that observed at GW 8 with higher signals in the MZ (C,D) and SVZ (C,E). D and E are magnifications of boxed areas in C at the level of the MZ and the SVZ, respectively. Note in D that some bipolar neurons expressing the sst2A receptor are visible in the CP and in E that patches of labeling are observed in the SVZ contiguous to the VZ. F, G) In coronal sections at GW 23, the labeling is present in neurons of CP (F) as well as in presumably post-mitotic migrating neurons in the IZ (G). H–J) In coronal sections at birth, the labeling is diffusely distributed in layers II–III and V. In this latter layer some neurons positive for the sst2A receptor are also observed (I,J). Scale bars: A, B, D, E, G, 25 µm; C, F, H, 100 µm; Inset in A,B and I,J, 10 µm.</p>", "links"=>[], "tags"=>["cellular", "sst2a", "receptor", "immunoreactivity"], "article_id"=>571061, "categories"=>["Cell Biology", "Neuroscience"], "users"=>["Virginia Le Verche", "Angela M. Kaindl", "Catherine Verney", "Zsolt Csaba", "Stéphane Peineau", "Paul Olivier", "Homa Adle-Biassette", "Christophe Leterrier", "Tania Vitalis", "Julie Renaud", "Bénédicte Dargent", "Pierre Gressens", "Pascal Dournaud"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0005509.g010", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Regional_and_cellular_distribution_of_sst2A_receptor_immunoreactivity_in_the_human_developing_cortex_/571061", "title"=>"Regional and cellular distribution of sst2A receptor immunoreactivity in the human developing cortex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:10:50"}

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  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
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  • {"unique-ip"=>"11", "full-text"=>"17", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
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  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"10", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"12", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"8", "full-text"=>"11", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"16", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"11", "full-text"=>"15", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}

Relative Metric

{"start_date"=>"2009-01-01T00:00:00Z", "end_date"=>"2009-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[315, 570, 717, 826, 931, 1027, 1137, 1224, 1308, 1379, 1458, 1542, 1613, 1694, 1768, 1841, 1909, 1957, 2019, 2082, 2127, 2182, 2232, 2290, 2352, 2419, 2476, 2525, 2572, 2627, 2670, 2722, 2800, 2846, 2901, 2963, 3017, 3078, 3136, 3210, 3253, 3303, 3366, 3431, 3486, 3538, 3600, 3663, 3723, 3776, 3815, 3880, 3966, 4036, 4103, 4145, 4193, 4232, 4304, 4369, 4426]}]}
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