{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,4]],"date-time":"2026-09-04T18:50:58Z","timestamp":1788547858785,"version":"build-2803163510"},"reference-count":93,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,6,23]],"date-time":"2023-06-23T00:00:00Z","timestamp":1687478400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurosci."],"abstract":"<jats:p>In recent years, the hypothalamus has emerged as a new neurogenic area, capable of generating new neurons after development. Neurogenesis-dependent neuroplasticity seems to be critical to continuously adapt to internal and environmental changes. Stress is a potent environmental factor that can produce potent and enduring effects on brain structure and function. Acute and chronic stress is known to cause alterations in neurogenesis and microglia in classical adult neurogenic regions such as the hippocampus. The hypothalamus is one of the major brain regions implicated in homeostatic stress and emotional stress systems, but little is known about the effect of stress on the hypothalamus. Here, we studied the impact of acute and intense stress (water immersion and restrain stress, WIRS), which may be considered as an inducer of an animal model of posttraumatic stress disorder, on neurogenesis and neuroinflammation in the hypothalamus of adult male mice, focusing on three nuclei: PVN, VMN and ARC, and also in the periventricular area. Our data revealed that a unique stressor was sufficient to provoke a significant impact on hypothalamic neurogenesis by inducing a reduction in the proliferation and number of immature neurons identified as DCX+ cells. These differences were accompanied by marked microglial activation in the VMN and ARC, together with a concomitant increase in IL-6 levels, indicating that WIRS induced an inflammatory response. To investigate the possible molecular mechanisms responsible for neuroplastic and inflammatory changes, we tried to identify proteomic changes. The data revealed that WIRS induced changes in the hypothalamic proteome, modifying the abundance of three and four proteins after 1\u2009h or 24\u2009h of stress application, respectively. These changes were also accompanied by slight changes in the weight and food intake of the animals. These results are the first to show that even a short-term environmental stimulus such as acute and intense stress can have neuroplastic, inflammatory, functional and metabolic consequences on the adult hypothalamus.<\/jats:p>","DOI":"10.3389\/fnins.2023.1190418","type":"journal-article","created":{"date-parts":[[2023,6,24]],"date-time":"2023-06-24T19:58:57Z","timestamp":1687636737000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":8,"title":["New insights into hypothalamic neurogenesis disruption after acute and intense stress: implications for microglia and inflammation"],"prefix":"10.3389","volume":"17","author":[{"given":"Mar\u00eda Inmaculada","family":"Infantes-L\u00f3pez","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea","family":"Nieto-Quero","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patricia","family":"Chaves-Pe\u00f1a","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emma","family":"Zambrana-Infantes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manuel","family":"Cifuentes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Javier","family":"M\u00e1rquez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carmen","family":"Pedraza","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Margarita","family":"P\u00e9rez-Mart\u00edn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,6,23]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1007\/978-1-4020-8831-5_9","article-title":"Altered lipid metabolism in brain injury and disorders","volume-title":"Lipids in health and disease","author":"Adibhatla","year":"2008"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"23892","DOI":"10.1074\/jbc.M700678200","article-title":"The CB1 cannabinoid receptor mediates excitotoxicity-induced neural progenitor proliferation and neurogenesis","volume":"282","author":"Aguado","year":"2007","journal-title":"J. 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Synaptic Neurosci."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1002\/cne.22698","article-title":"Cyto- and chemoarchitecture of the hypothalamic paraventricular nucleus in the C57BL\/6J male mouse: a study of immunostaining and multiple fluorescent tract tracing","volume":"520","author":"Biag","year":"2012","journal-title":"J. Comp. Neurol."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1080\/10253890.2021.1879787","article-title":"Early life stress decreases cell proliferation and the number of putative adult neural stem cells in the adult hypothalamus","volume":"24","author":"Bielefeld","year":"2021","journal-title":"Stress"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"1365210","DOI":"10.1155\/2019\/1365210","article-title":"Interleukin-6 expression by hypothalamic microglia in multiple inflammatory contexts: a systematic review","volume":"2019","author":"Bobbo","year":"2019","journal-title":"Biomed. Res. Int."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"1166","DOI":"10.1097\/NEN.0000000000000138","article-title":"The calcium-binding protein EFhd2 modulates synapse formation in vitro and is linked to human dementia","volume":"73","author":"Borger","year":"2014","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"840","DOI":"10.1523\/JNEUROSCI.3215-12.2013","article-title":"Neonatal Leptin exposure specifies innervation of Presympathetic hypothalamic neurons and improves the metabolic status of Leptin-deficient mice","volume":"33","author":"Bouyer","year":"2013","journal-title":"J. Neurosci."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"1087","DOI":"10.1093\/cercor\/bhx009","article-title":"Regulation of dendritic spine morphology in hippocampal neurons by Copine-6","volume":"28","author":"Burk","year":"2018","journal-title":"Cereb. Cortex"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"484","DOI":"10.1038\/nn.4495","article-title":"A molecular census of arcuate hypothalamus and median eminence cell types","volume":"20","author":"Campbell","year":"2017","journal-title":"Nat. Neurosci."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1037\/t01554-000","article-title":"The role of the hippocampus in the pathophysiology of major depression","volume":"29","author":"Campbell","year":"2004","journal-title":"J. Psychiatry Neurosci."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"579953","DOI":"10.3389\/fnins.2020.579953","article-title":"Excitotoxicity: still hammering the ischemic brain in 2020","volume":"14","author":"Choi","year":"2020","journal-title":"Front. 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Sci."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"R60","DOI":"10.1186\/gb-2003-4-5-p3","article-title":"DAVID: database for annotation, visualization, and integrated discovery","volume":"4","author":"Dennis","year":"2003","journal-title":"Genome Biol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"1453","DOI":"10.1523\/JNEUROSCI.0993-19.2019","article-title":"Microglia actively remodel adult hippocampal neurogenesis through the phagocytosis Secretome","volume":"40","author":"Diaz-Aparicio","year":"2020","journal-title":"J. Neurosci."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"10819","DOI":"10.1073\/pnas.152334899","article-title":"Brain monoglyceride lipase participating in endocannabinoid inactivation","volume":"99","author":"Dinh","year":"2002","journal-title":"Proc. Natl. Acad. Sci."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"797","DOI":"10.1016\/j.cmet.2016.04.013","article-title":"Adult NG2-glia are required for median Eminence-mediated Leptin sensing and body weight control","volume":"23","author":"Djogo","year":"2016","journal-title":"Cell Metab."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1186\/s12974-018-1371-6","article-title":"Profiling the proteomic inflammatory state of human astrocytes using DIA mass spectrometry","volume":"15","author":"Dozio","year":"2018","journal-title":"J. Neuroinflammation"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1097\/MOL.0000000000000801","article-title":"Lipids and brain inflammation in APOE4-associated dementia","volume":"33","author":"Duro","year":"2022","journal-title":"Curr. Opin. Lipidol."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"5048","DOI":"10.1210\/endo.138.11.5647","article-title":"Corticotropin releasing factor receptor type II (CRF2) messenger ribonucleic acid levels in the hypothalamic ventromedial nucleus of the infant rat are reduced by maternal deprivation","volume":"138","author":"Eghbal-Ahmadi","year":"1997","journal-title":"Endocrinology"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"13632","DOI":"10.1073\/pnas.2234031100","article-title":"Inflammation is detrimental for neurogenesis in adult brain","volume":"100","author":"Ekdahl","year":"2003","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1016\/j.semcdb.2019.01.001","article-title":"Microglia: Neuroimmune-sensors of stress","volume":"94","author":"Frank","year":"2019","journal-title":"Semin. Cell Dev. 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Neurosci."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"603","DOI":"10.1002\/cphy.c150015","article-title":"Regulation of the hypothalamic-pituitary-adrenocortical stress response","volume":"6","author":"Herman","year":"2016","journal-title":"Comp. Physiol."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"6459","DOI":"10.1523\/JNEUROSCI.20-17-06459.2000","article-title":"Impaired synaptic plasticity and cAMP response element-binding protein activation in Ca2+\/calmodulin-dependent protein kinase type IV\/gr-deficient mice","volume":"20","author":"Ho","year":"2000","journal-title":"J. Neurosci."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1186\/s12974-017-0876-8","article-title":"Kososan, a Kampo medicine, prevents a social avoidance behavior and attenuates neuroinflammation in socially defeated mice","volume":"14","author":"Ito","year":"2017","journal-title":"J. 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Neurosci."},{"key":"ref34","first-page":"381","volume-title":"The role of the microglia in acute CNS injury","author":"Kawabori","year":"2015"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"1689","DOI":"10.1126\/science.1092864","article-title":"Microglia: the enemy within?","volume":"302","author":"Kempermann","year":"2003","journal-title":"Science"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"624","DOI":"10.1016\/j.neuroscience.2014.07.047","article-title":"Heat stress attenuates new cell generation in the hypothalamus: a role for miR-138","volume":"277","author":"Kisliouk","year":"2014","journal-title":"Neuroscience"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"3389","DOI":"10.1002\/cne.23355","article-title":"Tanycyte-like cells form a blood-cerebrospinal fluid barrier in the circumventricular organs of the mouse brain","volume":"521","author":"Langlet","year":"2013","journal-title":"J. Comp. Neurol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1172\/JCI61562","article-title":"Alteration of hypothalamic cellular dynamics in obesity","volume":"122","author":"Lee","year":"2012","journal-title":"J. Clin. Invest."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"700","DOI":"10.1038\/nn.3079","article-title":"Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche","volume":"15","author":"Lee","year":"2012","journal-title":"Nat. Neurosci."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"1696","DOI":"10.3389\/fimmu.2019.01696","article-title":"The role of inflammation in depression and fatigue","volume":"10","author":"Lee","year":"2019","journal-title":"Front. Immunol."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"13282","DOI":"10.1038\/ncomms13282","article-title":"The pseudokinase CaMKv is required for the activity-dependent maintenance of dendritic spines","volume":"7","author":"Liang","year":"2016","journal-title":"Nat. Commun."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1016\/j.yhbeh.2012.03.005","article-title":"Social isolation impairs adult neurogenesis in the limbic system and alters behaviors in female prairie voles","volume":"62","author":"Lieberwirth","year":"2012","journal-title":"Horm. Behav."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1016\/j.bbi.2015.12.019","article-title":"Forced swimming sabotages the morphological and synaptic maturation of newborn granule neurons and triggers a unique pro-inflammatory milieu in the hippocampus","volume":"53","author":"Llorens-Mart\u00edn","year":"2016","journal-title":"Brain Behav. Immun."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"1501","DOI":"10.1017\/S1461145714000285","article-title":"Iptakalim confers an antidepressant effect in a chronic mild stress model of depression through regulating neuro-inflammation and neurogenesis","volume":"17","author":"Lu","year":"2014","journal-title":"Int. J. Neuropsychopharmacol."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"940","DOI":"10.1016\/j.neuropharm.2010.01.012","article-title":"Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients","volume":"58","author":"Lucassen","year":"2010","journal-title":"Neuropharmacology"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"440","DOI":"10.3389\/fncel.2014.00440\/abstract","article-title":"Neurodevelopmental origin and adult neurogenesis of the neuroendocrine hypothalamus","volume":"8","author":"Maggi","year":"2015","journal-title":"Front. Cell. Neurosci."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"8","DOI":"10.3389\/fnmol.2015.00086\/abstract","article-title":"Sugar consumption produces effects similar to early life stress exposure on hippocampal markers of neurogenesis and stress response","author":"Maniam","year":"2016","journal-title":"Front. Mol. Neurosci."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"683","DOI":"10.1001\/jamaneurol.2020.1127","article-title":"Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China","volume":"77","author":"Mao","year":"2020","journal-title":"JAMA Neurol."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"78","DOI":"10.5688\/aj710478","article-title":"Physiology of the autonomic nervous system","volume":"71","author":"McCorry","year":"2007","journal-title":"Am. J. Pharm. Educ."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1172\/JCI43134","article-title":"Remodeling of the arcuate nucleus energy-balance circuit is inhibited in obese mice","volume":"122","author":"McNay","year":"2012","journal-title":"J. Clin. Invest."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"e13984","DOI":"10.1371\/journal.pone.0013984","article-title":"Enrichment map: a network-based method for gene-set enrichment visualization and interpretation","volume":"5","author":"Merico","year":"2010","journal-title":"PLoS One"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1016\/j.neuron.2011.05.001","article-title":"Adult neurogenesis in the mammalian brain: significant answers and significant questions","volume":"70","author":"Ming","year":"2011","journal-title":"Neuron"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1007\/s11055-017-0420-4","article-title":"Stress-induced changes in Corticoliberin and vasopressin expression in the hypothalamus of female rats in a model of post-traumatic stress disorder","volume":"47","author":"Mironova","year":"2017","journal-title":"Neurosci. Behav. Physiol."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"e19859","DOI":"10.1371\/journal.pone.0019859","article-title":"Plasma Corticosterone activates SGK1 and induces morphological changes in Oligodendrocytes in Corpus callosum","volume":"6","author":"Miyata","year":"2011","journal-title":"PLoS One"},{"key":"ref55","doi-asserted-by":"publisher","first-page":"1760","DOI":"10.1126\/science.1088417","article-title":"Inflammatory blockade restores adult hippocampal neurogenesis","volume":"302","author":"Monje","year":"2003","journal-title":"Science"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"100356","DOI":"10.1016\/j.ynstr.2021.100356","article-title":"Do changes in microglial status underlie neurogenesis impairments and depressive-like behaviours induced by psychological stress? A systematic review in animal models","volume":"15","author":"Nieto-Quero","year":"2021","journal-title":"Neurobiol. Stress"},{"key":"ref57","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1016\/j.bbi.2015.08.022","article-title":"TNF-\u03b1 from hippocampal microglia induces working memory deficits by acute stress in mice","volume":"55","author":"Ohgidani","year":"2016","journal-title":"Brain Behav. Immun."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1007\/s12576-016-0467-y","article-title":"Effect of water-immersion restraint stress on tryptophan catabolism through the kynurenine pathway in rat tissues","volume":"67","author":"Ohta","year":"2017","journal-title":"J. Physiol. Sci."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"3458","DOI":"10.1016\/j.neuron.2022.10.020","article-title":"Microglia states and nomenclature: a field at its crossroads","volume":"110","author":"Paolicelli","year":"2022","journal-title":"Neuron"},{"key":"ref60","volume-title":"The mouse brain in stereotaxic coordinates. Compact","author":"Paxinos","year":"2004"},{"key":"ref61","doi-asserted-by":"publisher","first-page":"1533","DOI":"10.1111\/j.1460-9568.2010.07220.x","article-title":"IGF-I stimulates neurogenesis in the hypothalamus of adult rats","volume":"31","author":"P\u00e9rez-Mart\u00edn","year":"2010","journal-title":"Eur. J. Neurosci."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"723","DOI":"10.1523\/JNEUROSCI.2479-09.2010","article-title":"De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance","volume":"30","author":"Pierce","year":"2010","journal-title":"J. Neurosci."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1146\/annurev-clinpsy-050212-185606","article-title":"Depression, stress, and Anhedonia: toward a synthesis and integrated model","volume":"10","author":"Pizzagalli","year":"2014","journal-title":"Annu. Rev. Clin. Psychol."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"1464","DOI":"10.1002\/glia.23318","article-title":"Plaque-dependent morphological and electrophysiological heterogeneity of microglia in an Alzheimer\u2019s disease mouse model","volume":"66","author":"Plescher","year":"2018","journal-title":"Glia"},{"key":"ref65","doi-asserted-by":"publisher","first-page":"5750","DOI":"10.1523\/JNEUROSCI.2772-17.2018","article-title":"Persistent but labile synaptic plasticity at excitatory synapses","volume":"38","author":"Pradier","year":"2018","journal-title":"J. Neurosci."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"395","DOI":"10.2147\/JEP.S386745","article-title":"The oil formulation derived from Moringa Oleifera seeds ameliorates behavioral abnormalities in water-immersion restraint stress mouse model","volume":"14","author":"Purwoningsih","year":"2022","journal-title":"J. Exp. Pharmacol."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"132","DOI":"10.4103\/0019-5545.33264","article-title":"The limbic system","volume":"49","author":"RajMohan","year":"2007","journal-title":"Indian J. Psychiatry"},{"key":"ref68","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/ncomms11613","article-title":"The calcium sensor Copine-6 regulates spine structural plasticity and learning and memory","volume":"7","author":"Reinhard","year":"2016","journal-title":"Nat. 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Neurosci. Res."},{"key":"ref79","doi-asserted-by":"publisher","first-page":"D607","DOI":"10.1093\/nar\/gky1131","article-title":"STRING v11: protein\u2013protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets","volume":"47","author":"Szklarczyk","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref80","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1002\/9781118921692.ch3","article-title":"The synaptic physiology of the central nervous system response to stress","author":"Tasker","year":"2015","journal-title":"Neuroendocrinol. Stress"},{"key":"ref81","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1038\/nrn2647","article-title":"Neural regulation of endocrine and autonomic stress responses","volume":"10","author":"Ulrich-Lai","year":"2009","journal-title":"Nat. Rev. Neurosci."},{"key":"ref82","doi-asserted-by":"publisher","first-page":"442","DOI":"10.1021\/acschemneuro.6b00009","article-title":"Lifestyle shapes the dialogue between environment, microglia, and adult neurogenesis","volume":"7","author":"Valero","year":"2016","journal-title":"ACS Chem. Neurosci."},{"key":"ref83","doi-asserted-by":"publisher","first-page":"1262","DOI":"10.2174\/13894501113149990208","article-title":"Acute and chronic stress-induced disturbances of microglial plasticity, phenotype and function","volume":"14","author":"Walker","year":"2013","journal-title":"Curr. Drug Targets"},{"key":"ref84","doi-asserted-by":"publisher","first-page":"951","DOI":"10.1172\/JCI24301","article-title":"PI3K integrates the action of insulin and leptin on hypothalamic neurons","volume":"115","author":"Xu","year":"2005","journal-title":"J. Clin. Invest."},{"key":"ref85","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.psyneuen.2017.09.006","article-title":"Ghrelin and hypothalamic NPY\/AgRP expression in mice are affected by chronic early-life stress exposure in a sex-specific manner","volume":"86","author":"Yam","year":"2017","journal-title":"Psychoneuroendocrinology"},{"key":"ref86","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fnins.2019.01072","article-title":"Effects of 3 weeks of water immersion and restraint stress on sleep in mice","volume":"13","author":"Yasugaki","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref87","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1210\/en.2005-1051","article-title":"Ventromedial Arcuate nucleus communicates peripheral metabolic information to the Suprachiasmatic nucleus","volume":"147","author":"Yi","year":"2006","journal-title":"Endocrinology"},{"key":"ref88","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.pneurobio.2018.04.001","article-title":"Regulation and function of neurogenesis in the adult mammalian hypothalamus","volume":"170","author":"Yoo","year":"2018","journal-title":"Prog. Neurobiol."},{"key":"ref89","doi-asserted-by":"publisher","first-page":"1987","DOI":"10.1002\/glia.23817","article-title":"Tanycyte ablation in the arcuate nucleus and median eminence increases obesity susceptibility by increasing body fat content in male mice","volume":"68","author":"Yoo","year":"2020","journal-title":"Glia"},{"key":"ref90","doi-asserted-by":"publisher","first-page":"669","DOI":"10.2217\/pgs-2019-0015","article-title":"The ANKS1B gene and its associated phenotypes: focus on CNS drug response","volume":"20","author":"Younis","year":"2019","journal-title":"Pharmacogenomics"},{"key":"ref91","doi-asserted-by":"publisher","first-page":"3624","DOI":"10.1523\/JNEUROSCI.2742-12.2013","article-title":"Acute and long-term suppression of feeding behavior by POMC neurons in the brainstem and hypothalamus, respectively","volume":"33","author":"Zhan","year":"2013","journal-title":"J Neurosci"},{"key":"ref92","doi-asserted-by":"publisher","first-page":"9088","DOI":"10.3390\/ijms23169088","article-title":"Physiological and pathological functions of neuronal hemoglobin: a key underappreciated protein in Parkinson\u2019s disease","volume":"23","author":"Zheng","year":"2022","journal-title":"Int. J. Mol. Sci."},{"key":"ref93","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1002\/glia.23558","article-title":"Lipid transporter Spns2 promotes microglia pro-inflammatory activation in response to amyloid-beta peptide","volume":"67","author":"Zhong","year":"2019","journal-title":"Glia"}],"updated-by":[{"DOI":"10.3389\/fnins.2023.1335034","type":"corrigendum","label":"Corrigendum","source":"publisher","updated":{"date-parts":[[2023,11,23]],"date-time":"2023-11-23T00:00:00Z","timestamp":1700697600000}}],"container-title":["Frontiers in Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2023.1190418\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,23]],"date-time":"2023-11-23T14:26:22Z","timestamp":1700749582000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2023.1190418\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,23]]},"references-count":93,"alternative-id":["10.3389\/fnins.2023.1190418"],"URL":"https:\/\/doi.org\/10.3389\/fnins.2023.1190418","relation":{"corrigendum":[{"id-type":"doi","id":"10.3389\/fnins.2023.1335034","asserted-by":"object"}]},"ISSN":["1662-453X"],"issn-type":[{"value":"1662-453X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,23]]},"article-number":"1190418"}}