{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T06:03:07Z","timestamp":1789192987711,"version":"build-2803163510"},"reference-count":35,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2016,10,1]],"date-time":"2016-10-01T00:00:00Z","timestamp":1475280000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"}],"funder":[{"name":"NIMH R01","award":["086828"],"award-info":[{"award-number":["086828"]}]},{"name":"SIU School of Medicine startup funds"},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81271488"],"award-info":[{"award-number":["81271488"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Pearl River Scholar Program by Guangdong Province"},{"name":"Science and Technology Program of Guangzhou","award":["2014Y2-00096"],"award-info":[{"award-number":["2014Y2-00096"]}]},{"name":"Foundation for High-level Talents in Higher Education of Guangdong","award":["310109-012"],"award-info":[{"award-number":["310109-012"]}]},{"name":"Research Project for Colleges and Universities in Guangzhou, China","award":["12A002S"],"award-info":[{"award-number":["12A002S"]}]},{"name":"Research Fund for the Doctoral Program of Guangzhou Medical University","award":["2012C07"],"award-info":[{"award-number":["2012C07"]}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Behavioural Brain Research"],"published-print":{"date-parts":[[2016,10]]},"DOI":"10.1016\/j.bbr.2016.07.002","type":"journal-article","created":{"date-parts":[[2016,7,4]],"date-time":"2016-07-04T12:20:25Z","timestamp":1467634825000},"page":"135-143","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":29,"special_numbering":"C","title":["The essential role of hippocampal alpha6 subunit-containing GABAA receptors in maternal separation stress-induced adolescent depressive behaviors"],"prefix":"10.1016","volume":"313","author":[{"given":"Linjie","family":"Yang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ting","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ke","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhisheng","family":"Wei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xuran","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mingfa","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gregory M.","family":"Rose","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0222-553X","authenticated-orcid":false,"given":"Xiang","family":"Cai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.bbr.2016.07.002_bib0005","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1002\/mrdd.10074","article-title":"Early life influences on life-long patterns of behavior and health","volume":"9","author":"McEwen","year":"2003","journal-title":"Ment. Retard. Dev. Disabil Res. Rev."},{"key":"10.1016\/j.bbr.2016.07.002_bib0010","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1016\/j.neubiorev.2005.03.011","article-title":"Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research","volume":"29","author":"Pryce","year":"2005","journal-title":"Neurosci. Biobehav. Rev."},{"key":"10.1016\/j.bbr.2016.07.002_bib0015","doi-asserted-by":"crossref","first-page":"79","DOI":"10.4196\/kjpp.2009.13.2.79","article-title":"Maternal social separation of adolescent rats induces hyperactivity and anxiolytic behavior","volume":"13","author":"Kwak","year":"2009","journal-title":"Korean J. Physiol. Pharmacol."},{"key":"10.1016\/j.bbr.2016.07.002_bib0020","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1016\/S0006-3223(01)01157-X","article-title":"The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies","volume":"49","author":"Heim","year":"2001","journal-title":"Biol. Psychiatry"},{"key":"10.1016\/j.bbr.2016.07.002_bib0025","doi-asserted-by":"crossref","first-page":"5329","DOI":"10.1523\/JNEUROSCI.23-12-05329.2003","article-title":"Separation-induced receptor changes in the hippocampus and amygdala of Octodon degus: influence of maternal vocalizations","volume":"23","author":"Ziabreva","year":"2003","journal-title":"J. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0030","doi-asserted-by":"crossref","first-page":"1401","DOI":"10.1017\/S095457941200079X","article-title":"Maternal separation with early weaning: a rodent model providing novel insights into neglect associated developmental deficits","volume":"24","author":"Carlyle","year":"2012","journal-title":"Dev. Psychopathol."},{"key":"10.1016\/j.bbr.2016.07.002_bib0035","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1016\/0306-4530(93)90042-J","article-title":"Maternal separation in neonatal rats elicits activation of the hypothalamic-pituitary-adrenocortical axis: a putative role for corticotropin-releasing factor","volume":"18","author":"Pihoker","year":"1993","journal-title":"Psychoneuroendocrinology"},{"key":"10.1016\/j.bbr.2016.07.002_bib0040","doi-asserted-by":"crossref","first-page":"12213","DOI":"10.1073\/pnas.2131679100","article-title":"Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioral stress responses","volume":"100","author":"Hsu","year":"2003","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.bbr.2016.07.002_bib0045","doi-asserted-by":"crossref","first-page":"1680","DOI":"10.1016\/j.neurobiolaging.2014.01.024","article-title":"Maternal separation impairs long term-potentiation in CA1-CA3 synapses and hippocampal-dependent memory in old rats","volume":"35","author":"Sousa","year":"2014","journal-title":"Neurobiol. Aging"},{"key":"10.1016\/j.bbr.2016.07.002_bib0050","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1038\/nature04404","article-title":"GABA regulates synaptic integration of newly generated neurons in the adult brain","volume":"439","author":"Ge","year":"2006","journal-title":"Nature"},{"key":"10.1016\/j.bbr.2016.07.002_bib0055","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1111\/j.1460-9568.2011.07782.x","article-title":"Spatiotemporal specificity of GABAA receptor-mediated regulation of adult hippocampal neurogenesis","volume":"34","author":"Duveau","year":"2011","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0060","doi-asserted-by":"crossref","first-page":"14318","DOI":"10.1523\/JNEUROSCI.0709-12.2012","article-title":"BDNF promotes differentiation and maturation of adult-born neurons through GABAergic transmission","volume":"32","author":"Waterhouse","year":"2012","journal-title":"J. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0065","doi-asserted-by":"crossref","first-page":"166","DOI":"10.3389\/fncel.2014.00166","article-title":"Regulation of adult neurogenesis by GABAergic transmission: signaling beyond GABAA-receptors","volume":"8","author":"Pallotto","year":"2014","journal-title":"Front. Cell. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0070","first-page":"291","article-title":"International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function","volume":"50","author":"Barnard","year":"1998","journal-title":"Pharmacol. Rev."},{"key":"10.1016\/j.bbr.2016.07.002_bib0075","doi-asserted-by":"crossref","first-page":"9891","DOI":"10.1073\/pnas.96.17.9891","article-title":"theta, a novel gamma-aminobutyric acid type A receptor subunit","volume":"96","author":"Bonnert","year":"1999","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.bbr.2016.07.002_bib0080","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1038\/nrn2370","article-title":"GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition","volume":"9","author":"Jacob","year":"2008","journal-title":"Nat. Rev. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0085","doi-asserted-by":"crossref","first-page":"1108","DOI":"10.1124\/jpet.103.064360","article-title":"Structural determinants of the pharmacological properties of the GABAA receptor alpha6 subunit","volume":"309","author":"Drafts","year":"2004","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"10.1016\/j.bbr.2016.07.002_bib0090","doi-asserted-by":"crossref","first-page":"846","DOI":"10.1152\/jn.01199.2005","article-title":"Specific subtypes of GABAA receptors mediate phasic and tonic forms of inhibition in hippocampal pyramidal neurons","volume":"96","author":"Prenosil","year":"2006","journal-title":"J. Neurophysiol."},{"key":"10.1016\/j.bbr.2016.07.002_bib0095","doi-asserted-by":"crossref","first-page":"1421","DOI":"10.1523\/JNEUROSCI.4751-07.2008","article-title":"Which GABA(A) receptor subunits are necessary for tonic inhibition in the hippocampus?","volume":"14","author":"Glykys","year":"2008","journal-title":"J. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0100","doi-asserted-by":"crossref","first-page":"989","DOI":"10.1113\/jphysiol.2007.146746","article-title":"The expression of GABAA beta subunit isoforms in synaptic and extrasynaptic receptor populations of mouse dentate gyrus granule cells","volume":"586","author":"Herd","year":"2008","journal-title":"J. Physiol."},{"key":"10.1016\/j.bbr.2016.07.002_bib0105","doi-asserted-by":"crossref","first-page":"1693","DOI":"10.1523\/JNEUROSCI.18-05-01693.1998","article-title":"Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells","volume":"18","author":"Nusser","year":"1998","journal-title":"J. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0110","doi-asserted-by":"crossref","first-page":"3357","DOI":"10.1523\/JNEUROSCI.4799-05.2006","article-title":"Contributions of the GABAA receptor alpha6 subunit to phasic and tonic inhibition revealed by a naturally occurring polymorphism in the alpha6 gene","volume":"26","author":"Santhakumar","year":"2006","journal-title":"J. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0115","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1126\/science.1083328","article-title":"Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants","volume":"301","author":"Santarelli","year":"2003","journal-title":"Science (New York, NY)"},{"key":"10.1016\/j.bbr.2016.07.002_bib0120","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1038\/nn.3355","article-title":"Local potentiation of excitatory synapses by serotonin and its alteration in rodent models of depression","volume":"16","author":"Cai","year":"2013","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0125","doi-asserted-by":"crossref","first-page":"1350","DOI":"10.1523\/JNEUROSCI.17-04-01350.1997","article-title":"Ligand-gated ion channel subunit partnerships: GABAA receptor alpha6 subunit gene inactivation inhibits delta subunit expression","volume":"17","author":"Jones","year":"1997","journal-title":"J. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0130","doi-asserted-by":"crossref","first-page":"1783","DOI":"10.1038\/nn.3559","article-title":"Opposite actions of alcohol on tonic GABA(A) receptor currents mediated by nNOS and PKC activity","volume":"16","author":"Kaplan","year":"2013","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0135","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1016\/j.neuron.2004.09.026","article-title":"Unique roles of SK and Kv4.2 potassium channels in dendritic integration","volume":"44","author":"Cai","year":"2004","journal-title":"Neuron"},{"key":"10.1016\/j.bbr.2016.07.002_bib0140","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1152\/jn.00813.2005","article-title":"Multiple mechanisms of endocannabinoid response initiation in hippocampus","volume":"95","author":"Edwards","year":"2006","journal-title":"J. Neurophysiol."},{"key":"10.1016\/j.bbr.2016.07.002_bib0145","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1038\/nn.2517","article-title":"Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses","volume":"13","author":"Kim","year":"2010","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.bbr.2016.07.002_bib0150","doi-asserted-by":"crossref","first-page":"5345","DOI":"10.4049\/jimmunol.171.10.5345","article-title":"Mast cell degranulation requires N-ethylmaleimide-sensitive factor-mediated SNARE disassembly","volume":"171","author":"Puri","year":"2003","journal-title":"J. Immunol."},{"key":"10.1016\/j.bbr.2016.07.002_bib0155","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1111\/j.1471-4159.2007.05136.x","article-title":"Enhanced behavioral sensitivity to the competitive GABA agonist, gaboxadol, in transgenic mice over-expressing hippocampal extrasynaptic alpha6beta GABA(A) receptors","volume":"105","author":"Saarelainen","year":"2008","journal-title":"J. Neurochem."},{"key":"10.1016\/j.bbr.2016.07.002_bib0160","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1038\/mp.2010.120","article-title":"The GABAergic deficit hypothesis of major depressive disorder","volume":"16","author":"Luscher","year":"2011","journal-title":"Mol. Psychiatry"},{"key":"10.1016\/j.bbr.2016.07.002_bib0165","doi-asserted-by":"crossref","first-page":"1718","DOI":"10.1152\/jn.00243.2004","article-title":"Expression of distinct alpha subunits of GABAA receptor regulates inhibitory synaptic strength","volume":"92","author":"Ortinski","year":"2004","journal-title":"J. Neurophysiol."},{"key":"10.1016\/j.bbr.2016.07.002_bib0170","first-page":"223","article-title":"Prenatal maternal stress associated with ADHD and autistic traits in early childhood","volume":"1","author":"Ronald","year":"2010","journal-title":"Front. Psychol."},{"key":"10.1016\/j.bbr.2016.07.002_bib0175","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.jneumeth.2015.01.031","article-title":"Proteomic analysis of maternal separation-induced striatal changes in a rat model of ADHD: The spontaneously hypertensive rat","volume":"252","author":"Womersley","year":"2015","journal-title":"J. Neurosci. Methods"}],"container-title":["Behavioural Brain Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0166432816304302?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0166432816304302?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2019,11,2]],"date-time":"2019-11-02T02:11:15Z","timestamp":1572660675000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0166432816304302"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,10]]},"references-count":35,"alternative-id":["S0166432816304302"],"URL":"https:\/\/doi.org\/10.1016\/j.bbr.2016.07.002","relation":{},"ISSN":["0166-4328"],"issn-type":[{"value":"0166-4328","type":"print"}],"subject":[],"published":{"date-parts":[[2016,10]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"The essential role of hippocampal alpha6 subunit-containing GABAA receptors in maternal separation stress-induced adolescent depressive behaviors","name":"articletitle","label":"Article Title"},{"value":"Behavioural Brain Research","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.bbr.2016.07.002","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Published by Elsevier B.V.","name":"copyright","label":"Copyright"}]}}