{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,20]],"date-time":"2026-04-20T13:59:09Z","timestamp":1776693549195,"version":"3.51.2"},"reference-count":83,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,2,16]],"date-time":"2023-02-16T00:00:00Z","timestamp":1676505600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100013759","name":"Commonwealth Health Research Board","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100013759","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004979","name":"Center for Innovative Technology","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100004979","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000025","name":"National Institute of Mental Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell Dev. Biol."],"abstract":"<jats:p>The corticotropin-releasing hormone (CRH)-expressing neurons in the hypothalamus are critical regulators of the neuroendocrine stress response pathway, known as the hypothalamic-pituitary-adrenal (HPA) axis. As developmental vulnerabilities of CRH neurons contribute to stress-associated neurological and behavioral dysfunctions, it is critical to identify the mechanisms underlying normal and abnormal CRH neuron development. Using zebrafish, we identified<jats:italic>Down syndrome cell adhesion molecule like-1<\/jats:italic>(<jats:italic>dscaml1<\/jats:italic>) as an integral mediator of CRH neuron development and necessary for establishing normal stress axis function. In<jats:italic>dscaml1<\/jats:italic>mutant animals, hypothalamic CRH neurons had higher<jats:italic>crhb<\/jats:italic>(the CRH homolog in zebrafish) expression, increased cell number, and reduced cell death compared to wild-type controls. Physiologically,<jats:italic>dscaml1<\/jats:italic>mutant animals had higher baseline stress hormone (cortisol) levels and attenuated responses to acute stressors. Together, these findings identify<jats:italic>dscaml1<\/jats:italic>as an essential factor for stress axis development and suggest that HPA axis dysregulation may contribute to the etiology of human<jats:italic>DSCAML1<\/jats:italic>-linked neuropsychiatric disorders.<\/jats:p>","DOI":"10.3389\/fcell.2023.1113675","type":"journal-article","created":{"date-parts":[[2023,2,16]],"date-time":"2023-02-16T10:23:58Z","timestamp":1676543038000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["Deficiency in the cell-adhesion molecule dscaml1 impairs hypothalamic CRH neuron development and perturbs normal neuroendocrine stress axis function"],"prefix":"10.3389","volume":"11","author":[{"given":"Manxiu","family":"Ma","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alyssa A.","family":"Brunal","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kareem C.","family":"Clark","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carleigh","family":"Studtmann","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Katelyn","family":"Stebbins","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shin-ichi","family":"Higashijima","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Y. Albert","family":"Pan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2023,2,16]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1016\/j.ygcen.2009.04.007","article-title":"Ontogeny of the corticotropin-releasing factor system in zebrafish","volume":"164","author":"Alderman","year":"2009","journal-title":"Gen. Comp. Endocrinol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/j.ygcen.2008.09.011","article-title":"The zebrafish stress axis: molecular fallout from the teleost-specific genome duplication event","volume":"161","author":"Alsop","year":"2009","journal-title":"Gen. Comp. Endocrinol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"R711","DOI":"10.1152\/ajpregu.00671.2007","article-title":"Development of the corticosteroid stress axis and receptor expression in zebrafish","volume":"294","author":"Alsop","year":"2008","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1007\/s00441-018-2859-1","article-title":"Development of neuroendocrine neurons in the mammalian hypothalamus","volume":"375","author":"Alvarez-Bolado","year":"2019","journal-title":"Cell Tissue Res."},{"key":"B5","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1038\/npp.2015.215","article-title":"Genetic approaches to hypothalamic-pituitary-adrenal Axis regulation","volume":"41","author":"Arnett","year":"2016","journal-title":"Neuropsychopharmacology"},{"key":"B6","doi-asserted-by":"publisher","first-page":"dmm041913","DOI":"10.1242\/dmm.041913","article-title":"Deficiency in the endocytic adaptor proteins PHETA1\/2 impairs renal and craniofacial development","volume":"13","author":"Ates","year":"2020","journal-title":"Dis. models Mech."},{"key":"B7","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1186\/s12868-016-0298-z","article-title":"Identification of environmental stressors and validation of light preference as a measure of anxiety in larval zebrafish","volume":"17","author":"Bai","year":"2016","journal-title":"BMC Neurosci."},{"key":"B8","doi-asserted-by":"publisher","first-page":"173","DOI":"10.3354\/dao002173","article-title":"Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow trout","volume":"2","author":"Barton","year":"1987","journal-title":"Dis. aquatic Org."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1.26.1","DOI":"10.1002\/0471142301.ns0126s74","article-title":"Anterograde or retrograde transsynaptic circuit tracing in vertebrates with vesicular stomatitis virus vectors","volume":"74","author":"Beier","year":"2016","journal-title":"Curr. Protoc. Neurosci."},{"key":"B10","doi-asserted-by":"publisher","first-page":"587978","DOI":"10.3389\/fnmol.2020.587978","article-title":"Effects of constitutive and acute connexin 36 deficiency on brain-wide susceptibility to PTZ-induced neuronal hyperactivity","volume":"13","author":"Brunal","year":"2020","journal-title":"Front. Mol. Neurosci."},{"key":"B11","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/j.bbr.2014.05.005","article-title":"Modeling PTSD in the zebrafish: are we there yet?","volume":"276","author":"Caramillo","year":"2015","journal-title":"Behav. Brain Res."},{"key":"B12","doi-asserted-by":"publisher","first-page":"12796","DOI":"10.1038\/s41598-019-49388-3","article-title":"Active behaviour during early development shapes glucocorticoid reactivity","volume":"9","author":"Castillo-Ramirez","year":"2019","journal-title":"Sci. Rep."},{"key":"B13","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1002\/cne.21496","article-title":"Distribution of corticotropin-releasing hormone in the developing zebrafish brain","volume":"505","author":"Chandrasekar","year":"2007","journal-title":"J. Comp. Neurol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1515\/RNS.2011.007","article-title":"Stressing zebrafish for behavioral genetics","volume":"22","author":"Clark","year":"2011","journal-title":"Rev. Neurosci."},{"key":"B15","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1006\/dbio.2001.0432","article-title":"Apoptosis in the developing zebrafish embryo","volume":"240","author":"Cole","year":"2001","journal-title":"Dev. Biol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1111\/j.1365-2826.1992.tb00200.x","article-title":"Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal Axis","volume":"4","author":"Dallman","year":"1992","journal-title":"J. Neuroendocrinol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/j.1749-6632.2009.04433.x","article-title":"Structural and functional evolution of vertebrate neuroendocrine stress systems","volume":"1163","author":"Denver","year":"2009","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"B82","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1093\/nar\/30.1.207","article-title":"Gene Expression Omnibus: NCBI gene expression and hybridization array data repository","volume":"30","author":"Edgar","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"B18","doi-asserted-by":"publisher","first-page":"16961","DOI":"10.1073\/pnas.1902596116","article-title":"Epithelial delamination is protective during pharmaceutical-induced enteropathy","volume":"116","author":"Espenschied","year":"2019","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B19","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1111\/j.1365-2826.2009.01825.x","article-title":"Control of cell number in the sexually dimorphic brain and spinal cord","volume":"21","author":"Forger","year":"2009","journal-title":"J. Neuroendocrinol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"326","DOI":"10.1016\/j.ydbio.2011.10.028","article-title":"Cell autonomy of DSCAM function in retinal development","volume":"361","author":"Fuerst","year":"2012","journal-title":"Dev. Biol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"484","DOI":"10.1016\/j.neuron.2009.09.027","article-title":"DSCAM and DSCAML1 function in self-avoidance in multiple cell types in the developing mouse retina","volume":"64","author":"Fuerst","year":"2009","journal-title":"Neuron"},{"key":"B22","doi-asserted-by":"publisher","first-page":"86","DOI":"10.3389\/fnmol.2012.00086","article-title":"DSCAMs: restoring balance to developmental forces","volume":"5","author":"Garrett","year":"2012","journal-title":"Front. Mol. Neurosci."},{"key":"B23","doi-asserted-by":"publisher","first-page":"e16144","DOI":"10.7554\/eLife.16144","article-title":"Replacing the PDZ-interacting C-termini of DSCAM and DSCAML1 with epitope tags causes different phenotypic severity in different cell populations","volume":"5","author":"Garrett","year":"2016","journal-title":"eLife"},{"key":"B24","doi-asserted-by":"publisher","first-page":"68","DOI":"10.3389\/fnbeh.2012.00068","article-title":"A zebrafish model of glucocorticoid resistance shows serotonergic modulation of the stress response","volume":"6","author":"Griffiths","year":"2012","journal-title":"Front. Behav. Neurosci."},{"key":"B25","doi-asserted-by":"publisher","first-page":"3394","DOI":"10.1210\/EN.2015-1021","article-title":"Manipulation of interrenal cell function in developing zebrafish using genetically targeted ablation and an optogenetic tool","volume":"156","author":"Gutierrez-Triana","year":"2015","journal-title":"Endocrinology"},{"key":"B26","doi-asserted-by":"publisher","first-page":"206","DOI":"10.1186\/s40478-020-01082-6","article-title":"Down syndrome cell adhesion molecule like-1 (DSCAML1) links the GABA system and seizure susceptibility","volume":"8","author":"Hayase","year":"2020","journal-title":"Acta Neuropathol. Commun."},{"key":"B27","doi-asserted-by":"publisher","first-page":"135","DOI":"10.3389\/fnana.2017.00135","article-title":"Hypothalamic projections to the optic tectum in larval zebrafish","volume":"11","author":"Heap","year":"2017","journal-title":"Front. Neuroanat."},{"key":"B28","doi-asserted-by":"publisher","first-page":"2","DOI":"10.3389\/fnana.2015.00002","article-title":"Coexpression analysis of nine neuropeptides in the neurosecretory preoptic area of larval zebrafish","volume":"9","author":"Herget","year":"2015","journal-title":"Front. Neuroanat."},{"key":"B29","doi-asserted-by":"publisher","first-page":"1542","DOI":"10.1002\/cne.23480","article-title":"Molecular neuroanatomy and chemoarchitecture of the neurosecretory preoptic-hypothalamic area in zebrafish larvae","volume":"522","author":"Herget","year":"2014","journal-title":"J. Comp. Neurol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"137","DOI":"10.3389\/fendo.2016.00137","article-title":"Paraventricular hypothalamic mechanisms of chronic stress adaptation","volume":"7","author":"Herman","year":"2016","journal-title":"Front. Endocrinol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1016\/j.yebeh.2017.10.025","article-title":"Seizure-induced activation of the HPA axis increases seizure frequency and comorbid depression-like behaviors","volume":"78","author":"Hooper","year":"2018","journal-title":"Epilepsy Behav. E&B"},{"key":"B32","doi-asserted-by":"publisher","first-page":"e48","DOI":"10.1093\/nar\/gkv035","article-title":"Increased functional protein expression using nucleotide sequence features enriched in highly expressed genes in zebrafish","volume":"43","author":"Horstick","year":"2015","journal-title":"Nucleic acids Res."},{"key":"B33","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1038\/nature13908","article-title":"The contribution of de novo coding mutations to autism spectrum disorder","volume":"515","author":"Iossifov","year":"2014","journal-title":"Nature"},{"key":"B34","doi-asserted-by":"publisher","first-page":"275","DOI":"10.3109\/10253890.2014.913017","article-title":"Neonatal maternal separation up-regulates protein signalling for cell survival in rat hypothalamus","volume":"17","author":"Irles","year":"2014","journal-title":"Stress"},{"key":"B35","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1016\/j.bbr.2005.11.019","article-title":"Effect of different doses of corticosterone on depression-like behavior and HPA axis responses to a novel stressor","volume":"168","author":"Johnson","year":"2006","journal-title":"Behav. Brain Res."},{"key":"B36","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1016\/j.neuron.2015.09.048","article-title":"Genes that affect brain structure and function identified by rare variant analyses of mendelian neurologic disease","volume":"88","author":"Karaca","year":"2015","journal-title":"Neuron"},{"key":"B37","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1038\/mp.2008.91","article-title":"Continuous expression of corticotropin-releasing factor in the central nucleus of the amygdala emulates the dysregulation of the stress and reproductive axes","volume":"14","author":"Keen-Rhinehart","year":"2009","journal-title":"Mol. Psychiatry"},{"key":"B38","doi-asserted-by":"publisher","first-page":"6545","DOI":"10.1038\/srep06545","article-title":"Efficient generation of knock-in transgenic zebrafish carrying reporter\/driver genes by CRISPR\/Cas9-mediated genome engineering","volume":"4","author":"Kimura","year":"2014","journal-title":"Sci. Rep."},{"key":"B39","doi-asserted-by":"publisher","first-page":"2571","DOI":"10.1523\/JNEUROSCI.4470-09.2010","article-title":"Transient early-life forebrain corticotropin-releasing hormone elevation causes long-lasting anxiogenic and despair-like changes in mice","volume":"30","author":"Kolber","year":"2010","journal-title":"J. Neurosci."},{"key":"B40","doi-asserted-by":"publisher","first-page":"3757","DOI":"10.1242\/dev.126.17.3757","article-title":"Nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate","volume":"126","author":"Lister","year":"1999","journal-title":"Development"},{"key":"B41","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1146\/annurev-physiol-012110-142320","article-title":"Zebrafish in endocrine systems: recent advances and implications for human disease","volume":"73","author":"Lohr","year":"2011","journal-title":"Annu. Rev. Physiol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1007","DOI":"10.1242\/dev.033878","article-title":"Zebrafish diencephalic A11-related dopaminergic neurons share a conserved transcriptional network with neuroendocrine cell lineages","volume":"136","author":"Lohr","year":"2009","journal-title":"Development"},{"key":"B43","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"85","DOI":"10.3389\/fncir.2019.00085","article-title":"Structural neural connectivity analysis in zebrafish with restricted anterograde transneuronal viral labeling and quantitative brain mapping","volume":"13","author":"Ma","year":"","journal-title":"Front. Neural circuits"},{"key":"B45","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1523\/JNEUROSCI.1783-19.2019","article-title":"Zebrafish dscaml1 deficiency impairs retinal patterning and oculomotor function","volume":"40","author":"Ma","year":"","journal-title":"J. Neurosci."},{"key":"B46","doi-asserted-by":"publisher","first-page":"895","DOI":"10.1046\/j.1095-8649.2003.00074.x","article-title":"Morphological development of the gonads in zebrafish","volume":"62","author":"Maack","year":"2003","journal-title":"J. Fish Biol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"4046","DOI":"10.1038\/ncomms5046","article-title":"Distinct roles for BAI1 and TIM-4 in the engulfment of dying neurons by microglia","volume":"5","author":"Mazaheri","year":"2014","journal-title":"Nat. Commun."},{"key":"B48","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1523\/JNEUROSCI.0733-19.2019","article-title":"Revisiting the stress concept: Implications for affective disorders","volume":"40","author":"McEwen","year":"2020","journal-title":"J. Neurosci."},{"key":"B49","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1016\/B978-0-12-391857-4.00009-4","article-title":"Methods for cell and particle tracking","volume":"504","author":"Meijering","year":"2012","journal-title":"Methods Enzymol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"D394","DOI":"10.1093\/nar\/gkaa1106","article-title":"PANTHER version 16: a revised family classification, tree-based classification tool, enhancer regions and extensive API","volume":"49","author":"Mi","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"B51","doi-asserted-by":"publisher","first-page":"889155","DOI":"10.3389\/fnins.2022.889155","article-title":"To stick or not to stick: The multiple roles of cell adhesion molecules in neural circuit assembly","volume":"16","author":"Moreland","year":"2022","journal-title":"Front. Neurosci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"145","DOI":"10.3389\/fncir.2013.00145","article-title":"Glucocorticoid receptor activity regulates light adaptation in the zebrafish retina","volume":"7","author":"Muto","year":"2013","journal-title":"Front. Neural Circuits"},{"key":"B53","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1007\/s00441-018-2900-4","article-title":"Anatomy, development, and plasticity of the neurosecretory hypothalamus in zebrafish","volume":"375","author":"Nagpal","year":"2019","journal-title":"Cell Tissue Res."},{"key":"B54","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/oso\/9780199638086.003.0001","article-title":"Introduction: zebrafish as a system to study development and organogenesis","volume-title":"Zebrafish: A practical approach","author":"N\u00fcsslein-Volhard","year":"2002"},{"key":"B55","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/j.eplepsyres.2013.10.013","article-title":"Seizure-induced disinhibition of the HPA axis increases seizure susceptibility","volume":"108","author":"O'Toole","year":"2014","journal-title":"Epilepsy Res."},{"key":"B56","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1111\/gtc.12831","article-title":"Potential involvement of DSCAML1 mutations in neurodevelopmental disorders","volume":"26","author":"Ogata","year":"2021","journal-title":"Genes Cells"},{"key":"B57","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1242\/dev.076588","article-title":"Robo2 determines subtype-specific axonal projections of trigeminal sensory neurons","volume":"139","author":"Pan","year":"2012","journal-title":"Development"},{"key":"B58","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-3-030-40002-6_1","article-title":"Development of the neuroendocrine hypothalamus","volume-title":"Developmental neuroendocrinology","author":"Placzek","year":"2020"},{"key":"B59","doi-asserted-by":"publisher","first-page":"492","DOI":"10.1016\/j.devcel.2011.07.012","article-title":"p63 mediates an apoptotic response to pharmacological and disease-related ER stress in the developing epidermis","volume":"21","author":"Pyati","year":"2011","journal-title":"Dev. Cell"},{"key":"B60","doi-asserted-by":"publisher","first-page":"1039","DOI":"10.1038\/nmeth.3581","article-title":"Whole-brain activity mapping onto a zebrafish brain atlas","volume":"12","author":"Randlett","year":"2015","journal-title":"Nat. Methods"},{"key":"B61","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1016\/j.yfrne.2013.10.001","article-title":"Corticotropin releasing factor in neuroplasticity","volume":"35","author":"Regev","year":"2014","journal-title":"Front. Neuroendocrinol."},{"key":"B62","doi-asserted-by":"publisher","first-page":"100247","DOI":"10.1016\/j.bbih.2021.100247","article-title":"DNA methylation and exposure to violence among African American young adult males","volume":"14","author":"Saadatmand","year":"2021","journal-title":"Brain, Behav. Immun. - Health"},{"key":"B63","doi-asserted-by":"publisher","first-page":"e99669","DOI":"10.15252\/embj.201899669","article-title":"Nuclear import of the DSCAM-cytoplasmic domain drives signaling capable of inhibiting synapse formation","volume":"38","author":"Sachse","year":"2019","journal-title":"EMBO J."},{"key":"B64","doi-asserted-by":"publisher","first-page":"536","DOI":"10.1016\/j.cell.2020.04.008","article-title":"Synaptic specificity, recognition molecules, and assembly of neural circuits","volume":"181","author":"Sanes","year":"2020","journal-title":"Cell"},{"key":"B65","doi-asserted-by":"publisher","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: an open-source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"B83","doi-asserted-by":"publisher","DOI":"10.1101\/2022.02.11.479024","article-title":"A single-cell resolution gene expression atlas of the larval zebrafish brain","author":"Shainer","year":"2022","journal-title":"bioRxiv"},{"key":"B66","doi-asserted-by":"publisher","first-page":"507","DOI":"10.1146\/annurev.neuro.25.112701.142745","article-title":"Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain","volume":"25","author":"Simerly","year":"2002","journal-title":"Annu. Rev. Neurosci."},{"key":"B67","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/j.physbeh.2016.11.014","article-title":"A users guide to HPA axis research","volume":"178","author":"Spencer","year":"2017","journal-title":"Physiol. Behav."},{"key":"B68","doi-asserted-by":"publisher","first-page":"3378","DOI":"10.1210\/endo.130.6.1597149","article-title":"Development of Cushing's syndrome in corticotropin-releasing factor transgenic mice","volume":"130","author":"Stenzel-Poore","year":"1992","journal-title":"Endocrinology"},{"key":"B69","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1111\/j.1749-6632.2011.05904.x","article-title":"PACAP: a master regulator of neuroendocrine stress circuits and the cellular stress response","volume":"1220","author":"Stroth","year":"2011","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"B70","doi-asserted-by":"publisher","first-page":"3350","DOI":"10.1523\/JNEUROSCI.3390-15.2016","article-title":"The severity of acute stress is represented by increased synchronous activity and recruitment of hypothalamic CRH neurons","volume":"36","author":"Vom Berg-Maurer","year":"2016","journal-title":"J. Neurosci."},{"key":"B71","doi-asserted-by":"publisher","first-page":"3777","DOI":"10.1038\/s41380-022-01567-x","article-title":"Brain-wide perception of the emotional valence of light is regulated by distinct hypothalamic neurons","volume":"27","author":"Wagle","year":"2022","journal-title":"Mol. Psychiatry"},{"key":"B72","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/j.yfrne.2005.09.001","article-title":"Glucocorticoid regulation of peptide genes in neuroendocrine CRH neurons: A complexity beyond negative feedback","volume":"26","author":"Watts","year":"2005","journal-title":"Front. Neuroendocrinol."},{"key":"B73","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1152\/physrev.1997.77.3.591","article-title":"The stress response in fish","volume":"77","author":"Wendelaar Bonga","year":"1997","journal-title":"Physiol. Rev."},{"key":"B74","doi-asserted-by":"publisher","first-page":"1291","DOI":"10.1534\/genetics.114.169284","article-title":"Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains","volume":"198","author":"Wilson","year":"2014","journal-title":"Genetics"},{"key":"B75","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1146\/annurev-cellbio-100818-125204","article-title":"Developmental cell death in the cerebral cortex","volume":"35","author":"Wong","year":"2019","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"B76","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1038\/nature06469","article-title":"Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina","volume":"451","author":"Yamagata","year":"2008","journal-title":"Nature"},{"key":"B77","doi-asserted-by":"publisher","first-page":"3579","DOI":"10.1523\/JNEUROSCI.6319-09.2010","article-title":"Synaptic localization and function of Sidekick recognition molecules require MAGI scaffolding proteins","volume":"30","author":"Yamagata","year":"2010","journal-title":"J. Neurosci."},{"key":"B78","doi-asserted-by":"publisher","first-page":"478","DOI":"10.1016\/j.devcel.2015.01.019","article-title":"Programmed cell death in neurodevelopment","volume":"32","author":"Yamaguchi","year":"2015","journal-title":"Dev. Cell"},{"key":"B79","doi-asserted-by":"publisher","first-page":"e79406","DOI":"10.1371\/journal.pone.0079406","article-title":"An optimized whole-body cortisol quantification method for assessing stress levels in larval zebrafish","volume":"8","author":"Yeh","year":"2013","journal-title":"PLoS One"},{"key":"B80","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1016\/j.neuroscience.2012.03.046","article-title":"Hypothalamic vasopressin system regulation by maternal separation: its impact on anxiety in rats","volume":"215","author":"Zhang","year":"2012","journal-title":"Neuroscience"},{"key":"B81","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1038\/mp.2012.64","article-title":"An affective disorder in zebrafish with mutation of the glucocorticoid receptor","volume":"18","author":"Ziv","year":"2013","journal-title":"Mol. Psychiatry"}],"container-title":["Frontiers in Cell and Developmental Biology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2023.1113675\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,7]],"date-time":"2023-12-07T00:22:16Z","timestamp":1701908536000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2023.1113675\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,16]]},"references-count":83,"alternative-id":["10.3389\/fcell.2023.1113675"],"URL":"https:\/\/doi.org\/10.3389\/fcell.2023.1113675","relation":{},"ISSN":["2296-634X"],"issn-type":[{"value":"2296-634X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,16]]},"article-number":"1113675"}}