{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T12:40:23Z","timestamp":1789130423477,"version":"build-2803163510"},"reference-count":110,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2018,10,26]],"date-time":"2018-10-26T00:00:00Z","timestamp":1540512000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100010198","name":"Ministerio de Econom\u00eda, Industria y Competitividad, Gobierno de Espa\u00f1a","doi-asserted-by":"publisher","award":["PSI2014-51847-R"],"award-info":[{"award-number":["PSI2014-51847-R"]}],"id":[{"id":"10.13039\/501100010198","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100010198","name":"Ministerio de Econom\u00eda, Industria y Competitividad, Gobierno de Espa\u00f1a","doi-asserted-by":"publisher","award":["PSI 2017-83023-R"],"award-info":[{"award-number":["PSI 2017-83023-R"]}],"id":[{"id":"10.13039\/501100010198","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Instituto de Salud Carlos III (ES)","award":["RETICS RD16\/0017\/0007"],"award-info":[{"award-number":["RETICS RD16\/0017\/0007"]}]},{"DOI":"10.13039\/501100004587","name":"Instituto de Salud Carlos III","doi-asserted-by":"publisher","award":["RETICS RD2012\/0028\/0021"],"award-info":[{"award-number":["RETICS RD2012\/0028\/0021"]}],"id":[{"id":"10.13039\/501100004587","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002911","name":"Universidad Complutense de Madrid","doi-asserted-by":"publisher","award":["GRUPOS UCM-BSCH 951579"],"award-info":[{"award-number":["GRUPOS UCM-BSCH 951579"]}],"id":[{"id":"10.13039\/501100002911","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0206421","type":"journal-article","created":{"date-parts":[[2018,10,26]],"date-time":"2018-10-26T17:35:25Z","timestamp":1540575325000},"page":"e0206421","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":37,"title":["Social stress during adolescence activates long-term microglia inflammation insult in reward processing nuclei"],"prefix":"10.1371","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1121-8879","authenticated-orcid":true,"given":"Marta","family":"Rodr\u00edguez-Arias","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandra","family":"Montagud-Romero","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana Mar\u00eda","family":"Guardia Carri\u00f3n","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carmen","family":"Ferrer-P\u00e9rez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana","family":"P\u00e9rez-Villalba","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eva","family":"Marco","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meritxell","family":"L\u00f3pez Gallardo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4119-4636","authenticated-orcid":true,"given":"Mar\u00eda-Paz","family":"Viveros","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jos\u00e9","family":"Mi\u00f1arro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2018,10,26]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/j.ejphar.2005.09.032","article-title":"Individual differences in drug dependence in rats: the role of genetic factors and life events","volume":"526","author":"BA Ellenbroek","year":"2005","journal-title":"Eur J Pharmacol"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1196\/annals.1376.019","article-title":"Genetic and environmental influences on the development of alcoholism: resilience vs. risk","volume":"1094","author":"MA Enoch","year":"2006","journal-title":"Ann N Y Acad Sci"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1016\/j.neuropharm.2011.07.007","article-title":"Stress modulation of drug self-administration: implications for addiction comorbidity with post-traumatic stress disorder","volume":"62","author":"ML Logrip","year":"2011","journal-title":"Neuropharmacology"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1007\/s00213-011-2263-y","article-title":"Translational and reverse translational research on the role of stress in drug craving and relapse","volume":"218","author":"R Sinha","year":"2011","journal-title":"Psychopharmacology"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/B978-0-444-52002-9.00009-7","article-title":"Animal models of psychiatric disorders","volume":"106","author":"GF Koob","year":"2012","journal-title":"Handb Clin Neurol"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.brainres.2009.11.008","article-title":"The role of CRF and CRF-related peptides in the dark side of addiction","volume":"1314","author":"GF Koob","year":"2010","journal-title":"Brain Res"},{"key":"ref7","first-page":"133","article-title":"Drug use and abuse: Signs\/symptoms, physical and psychological effects and intervention approaches","author":"M Rodr\u00edguez-Arias","year":"2013"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1038\/npp.2015.142","article-title":"Stress-Induced Reinstatement of Drug Seeking: 20 Years of Progress","volume":"41","author":"JR Mantsch","year":"2016","journal-title":"Neuropsychopharmacology"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.1176\/appi.ajp.160.6.1041","article-title":"Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability","volume":"160","author":"RA Chambers","year":"2003","journal-title":"Am J Psychiatry"},{"key":"ref10","first-page":"115","article-title":"Modeling adolescent development and alcohol use in animals","volume":"24","author":"L Spear","year":"2000","journal-title":"Alcohol Res Health"},{"issue":"7105","key":"ref11","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1038\/442865a","article-title":"Neurodevelopment: how does the teenage brain work?","volume":"442","author":"K Powell","year":"2006","journal-title":"Nature"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.pbb.2009.04.018","article-title":"Impulsivity, frontal lobes and risk for addiction","volume":"93","author":"FT Crews","year":"2009","journal-title":"Pharmacol Biochem Behav"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.pbb.2009.01.021","article-title":"The maturation of incentive processing and cognitive control","volume":"93","author":"C Geier","year":"2009","journal-title":"Pharmacol Biochem Behav"},{"key":"ref14","first-page":"227","article-title":"Addiction-From Pathophysiology to Treatment","author":"M Rodr\u00edguez-Arias","year":"2012"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/j.beproc.2011.03.004","article-title":"Differential long-term effects of social stress during adolescence on anxiety in Wistar and wild-type rats","volume":"87","author":"J Vidal","year":"2011","journal-title":"Behav Processes"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1037\/spq0000120","article-title":"School bullying and drug use later in life: A meta-analytic investigation","volume":"31","author":"MM Ttofi","year":"2016","journal-title":"Sch Psychol"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1016\/0031-9384(93)90278-N","article-title":"Long-term impairment of autonomic circadian rhythms after brief intermittent social stress","volume":"53","author":"W Tornatzky","year":"1993","journal-title":"Physiol Behav"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1046\/j.1365-2826.1999.00350.x","article-title":"Long-lasting deficient dexamethasone suppression of hypothalamic-pituitary-adrenocortical activation following peripheral CRF challenge in socially defeated rats","volume":"11","author":"B Buwalda","year":"1999","journal-title":"J Neuroendocrinol"},{"key":"ref19","article-title":"Animal Conflict- Chapman and Hall","author":"FA Huntingford","year":"1987"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1037\/a0015752","article-title":"Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults","volume":"123","author":"MJ Watt","year":"2009","journal-title":"Behav Neurosci"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1016\/j.neubiorev.2017.01.018","article-title":"Impact of adolescent social experiences on behavior and neural circuits implicated in mental illnesses","volume":"76","author":"AR Burke","year":"2017","journal-title":"Neurosci Biobehav Rev"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1111\/adb.12301","article-title":"Effects of repeated social defeat on adolescent mice on cocaine-induced CPP and self-administration in adulthood: integrity of the blood-brain barrier","volume":"22","author":"M Rodr\u00edguez-Arias","year":"2017","journal-title":"Addict Biol"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"2063","DOI":"10.1007\/s00213-017-4612-y","article-title":"Repeated social defeat and the rewarding effects of cocaine in adult and adolescent mice: dopamine transcription factors, proBDNF signaling pathways, and the TrkB receptor in the mesolimbic system","volume":"234","author":"S Montagud-Romero","year":"2017","journal-title":"Psychopharmacology"},{"key":"ref24","first-page":"15","article-title":"he effects of social defeat and other stressors on the expression of circadian rhythms","volume":"5","author":"P Meerlo","year":"2002","journal-title":"T"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1016\/S0091-3057(00)00382-8","article-title":"Effects of social defeat and of diazepam on behavior in a resident-intruder test in male DBA\/2 mice","volume":"67","author":"LA Lumley","year":"2000","journal-title":"Pharmacol Biochem Behav"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1007\/s002130050230","article-title":"Acquisition of cocaine self-administration after social stress: role of accumbens dopamine","volume":"130","author":"JW Tidey","year":"1997","journal-title":"Psychopharmacology"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1038\/sj.npp.1300587","article-title":"Brief social defeat stress: long lasting effects on cocaine taking during a binge and zif268 mRNA expression in the amygdala and prefrontal cortex","volume":"30","author":"HE 3rd Covington","year":"2005","journal-title":"Neuropsychopharmacology"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1007\/s00213-005-0190-5","article-title":"Intense cocaine self-administration after episodic social defeat stress, but not after aggressive behavior: dissociation from corticosterone activation","volume":"183","author":"HE Covington 3rd","year":"2005","journal-title":"Psychopharmacology"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"3067","DOI":"10.1007\/s00213-015-3947-5","article-title":"Escalation of cocaine self-administration in adulthood after social defeat of adolescent rats: role of social experience and adaptive coping behavior","volume":"232","author":"AR Burke","year":"2015","journal-title":"Psychopharmacology"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1007\/s00213-011-2266-8","article-title":"Prevention of social stress-escalated cocaine self-administration by CRF-R1 antagonist in the rat VTA","volume":"218","author":"CO Boyson","year":"2011","journal-title":"Psychopharmacology"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"6659","DOI":"10.1523\/JNEUROSCI.3942-13.2014","article-title":"Social stress and CRF-dopamine interactions in the VTA: role in long-term escalation of cocaine self-administration","volume":"34","author":"CO Boyson","year":"2014","journal-title":"J Neurosci"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"4093","DOI":"10.1523\/JNEUROSCI.2232-15.2016","article-title":"Episodic Social Stress-Escalated Cocaine Self-Administration: Role of Phasic and Tonic Corticotropin Releasing Factor in the Anterior and Posterior Ventral Tegmental Area","volume":"36","author":"EN Holly","year":"2016","journal-title":"J Neurosci"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"1241","DOI":"10.1038\/sj.npp.1300872","article-title":"Social defeat stress-induced behavioral responses are mediated by the endogenous kappa opioid system","volume":"31","author":"JP McLaughlin","year":"2006","journal-title":"Neuropsychopharmacology"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"19168","DOI":"10.1073\/pnas.0910705106","article-title":"Activation of the kappa opioid receptor in the dorsal raphe nucleus mediates the aversive effects of stress and reinstates drug seeking","volume":"106","author":"BB Land","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1097\/FBP.0000000000000074","article-title":"Stress-induced increases in depression-like and cocaine place-conditioned behaviors are reversed by disruption of memories during reconsolidation","volume":"25","author":"KA Hymel","year":"2014","journal-title":"Behav Pharmacol"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.pbb.2015.05.008","article-title":"Acute social defeat stress increases the conditioned rewarding effects of cocaine in adult but not in adolescent mice","volume":"135","author":"S Montagud-Romero","year":"2015","journal-title":"Pharmacol Biochem Behav"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.pnpbp.2016.07.008","article-title":"Role of dopamine neurotransmission in the long-term effects of repeated social defeat on the conditioned rewarding effects of cocaine","volume":"71","author":"S Montagud-Romero","year":"2016","journal-title":"Prog Neuropsychopharmacol Biol Psychiatry"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.ejphar.2017.01.039","article-title":"Dopamine D2 receptors mediate the increase in reinstatement of the conditioned rewarding effects of cocaine induced by acute social defeat","volume":"799","author":"MD Reguil\u00f3n","year":"2017","journal-title":"Eur J Pharmacol"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1038\/npp.2016.102","article-title":"Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal","volume":"42","author":"MD Weber","year":"2017","journal-title":"Neuropsychopharmacology"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1001\/jamapsychiatry.2015.22","article-title":"Are Anti-inflammatory Therapies Viable Treatments for Psychiatric Disorders?: Where the Rubber Meets the Road","volume":"72","author":"AH Miller","year":"2015","journal-title":"JAMA Psychiatry"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1038\/nrn2297","article-title":"From inflammation to sickness and depression: When the immune system subjugates the brain","volume":"9","author":"R Dantzer","year":"2008","journal-title":"Nature Reviews Neuroscience"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"179","DOI":"10.2147\/JIR.S141033","article-title":"The role of neuroinflammation and neurovascular dysfunction in major depressive disorder","volume":"11","author":"SW Jeon","year":"2018","journal-title":"Journal of Inflammation Research"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1152\/physrev.00039.2016","article-title":"Neuroimmune Interactions: From the Brain to the Immune System and Vice Versa","volume":"98","author":"R Dantzer","year":"2018","journal-title":"Physiol Rev"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.bbr.2017.04.020","article-title":"The influence of stress on neuroinflammation and alterations in brain structure and function in major depressive disorder","volume":"329","author":"Y-K Kim","year":"2017","journal-title":"Behav Brain Res"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1016\/j.neuroscience.2015.01.001","article-title":"Peripheral and central effects of repeated social defeat stress: monocyte trafficking, microglial activation, and anxiety","volume":"289","author":"BF Reader","year":"2015","journal-title":"Neuroscience"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"16136","DOI":"10.1073\/pnas.1415191111","article-title":"Individual differences in the peripheral immune system promote resilience versus susceptibility to social stress","volume":"111","author":"GE Hodes","year":"2014","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1016\/j.biopsych.2013.11.029","article-title":"Re-establishment of anxiety in stress-sensitized mice is caused by monocyte trafficking from the spleen to the brain","volume":"75","author":"ES Wohleb","year":"2014","journal-title":"Biol Psychiatry"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1016\/j.pharmthera.2008.07.006","article-title":"Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake","volume":"120","author":"KA Miczek","year":"2008","journal-title":"Pharmacol Ther"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.pnpbp.2016.04.016","article-title":"`Up-regulation of histone acetylation induced by social defeat mediates the conditioned rewarding effects of cocaine","volume":"70","author":"S Montagud-Romero","year":"2016","journal-title":"Prog Neuropsychopharmacol Biol Psychiatry"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1016\/j.matbio.2009.02.002","article-title":"Matrix metalloproteinase-9 deficiency leads to prolonged foreign body response in the brain associated with increased IL-1beta levels and leakage of the blood-brain barrier","volume":"28","author":"W Tian","year":"2009","journal-title":"Matrix Biol"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"1939","DOI":"10.1038\/jcbfm.2010.45","article-title":"Hemoglobin-induced oxidative stress contributes to matrix metalloproteinase activation and blood-brain barrier dysfunction in vivo","volume":"30","author":"M Katsu","year":"2010","journal-title":"J Cereb Blood Flow Metab"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"9301","DOI":"10.1523\/JNEUROSCI.1418-07.2007","article-title":"Chronic interleukin-1beta expression in mouse brain leads to leukocyte infiltration and neutrophil-independent blood brain barrier permeability without overt neurodegeneration","volume":"27","author":"SS Shaftel","year":"2007","journal-title":"J Neurosci"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"1393","DOI":"10.1097\/00004647-200112000-00003","article-title":"Matrix metalloproteinase inhibition prevents oxidative stress-associated blood-brain barrier disruption after transient focal cerebral ischemia","volume":"21","author":"Y Gasche","year":"2001","journal-title":"J Cereb Blood Flow Metab"},{"issue":"6116","key":"ref54","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1126\/science.1227901","article-title":"Microglia: scapegoat, saboteur, or something else?","volume":"339","author":"A Aguzzi","year":"2013","journal-title":"Science"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.bbi.2013.12.010","article-title":"Dynamic structural remodelling of microglia in health and disease: a review of the models, the signals and the mechanisms","volume":"37","author":"FR Walker","year":"2014","journal-title":"Brain Behav Immun"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.schres.2015.01.015","article-title":"Decreased glial reactivity could be involved in the antipsychotic-like effect of cannabidiol","volume":"164","author":"FV Gomes","year":"2015","journal-title":"Schizophrenia Res"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1017\/S1740925X12000063","article-title":"Functions of microglia in the central nervous system\u2014beyond the immune response","volume":"7","author":"H Wake","year":"2011","journal-title":"Neuron Glia Biol"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"235","DOI":"10.3389\/fncel.2017.00235","article-title":"Microglia Morphological Categorization in a Rat Model of Neuroinflammation by Hierarchical Cluster and Principal Components Analysis","volume":"11","author":"MDM Fern\u00e1ndez-Arjona","year":"2017","journal-title":"Front Cell Neurosci"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1152\/physrev.00011.2010","article-title":"Physiology of microglia","volume":"91","author":"H Kettenmann","year":"2011","journal-title":"Physiol Rev"},{"key":"ref60","article-title":"Microglial dysregulation in psychiatric disease","author":"LR Frick","year":"2013","journal-title":"Clin Dev Immunol"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"1442","DOI":"10.1093\/cercor\/bhr229","article-title":"Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex","volume":"22","author":"M Hinwood","year":"2012","journal-title":"Cereb Cortex"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"1058","DOI":"10.1016\/j.bbi.2010.02.001","article-title":"Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions","volume":"24","author":"RJ Tynan","year":"2010","journal-title":"Brain Behav Immun"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"1388","DOI":"10.1016\/j.neuroscience.2007.02.043","article-title":"Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18","volume":"146","author":"S Sugama","year":"2007","journal-title":"Neuroscience"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"1262","DOI":"10.2174\/13894501113149990208","article-title":"Acute and chronic stress-induced disturbances of microglial plasticity, phenotype and function","volume":"14","author":"FR Walker","year":"2013","journal-title":"Curr Drug Targets"},{"key":"ref65","doi-asserted-by":"crossref","first-page":"211","DOI":"10.3389\/fncel.2014.00211","article-title":"Astrocytic modulation of blood brain barrier: perspectives on Parkinson&apos;s disease","volume":"8","author":"R Cabezas","year":"2014","journal-title":"Front Cell Neurosci"},{"key":"ref66","doi-asserted-by":"crossref","first-page":"1490","DOI":"10.1038\/sj.npp.1301275","article-title":"Chronic social stress inhibits cell proliferation in the adult medial prefrontal cortex: hemispheric asymmetry and reversal by fluoxetine treatment","volume":"32","author":"B Cz\u00e9h","year":"2007","journal-title":"Neuropsychopharmacology"},{"key":"ref67","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1007\/s00401-013-1223-5","article-title":"Neuropathology of stress","volume":"127","author":"PJ Lucassen","year":"2014","journal-title":"Acta Neuropathol"},{"key":"ref68","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.biopsych.2015.12.022","article-title":"Cocaine Self-Administration and Extinction Leads to Reduced Glial Fibrillary Acidic Protein Expression and Morphometric Features of Astrocytes in the Nucleus Accumbens Core","volume":"80","author":"MD Scofield","year":"2016","journal-title":"Biol Psychiatry"},{"key":"ref69","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1007\/s00441-014-1988-4","article-title":"Immunocytochemical markers of neuronal maturation in human diagnostic neuropathology.","volume":"359","author":"HB Sarnat","year":"2015","journal-title":"Cell Tissue Res"},{"key":"ref70","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1002\/hipo.20655","article-title":"Chronic social stress during adolescence induces cognitive impairment in aged mice","volume":"20","author":"V Sterlemann","year":"2010","journal-title":"Hippocampus"},{"key":"ref71","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/S0924-977X(97)00051-5","article-title":"Effects of risperidone and SCH 23390 on isolation-induced aggression in male mice","volume":"8","author":"M Rodr\u0131guez-Arias","year":"1998","journal-title":"European neuropsychopharmacology"},{"key":"ref72","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.physbeh.2014.05.028","article-title":"Capacity of novelty-induced locomotor activity and the hole-board test to predict sensitivity to the conditioned rewarding effects of cocaine","volume":"133","author":"MC Arenas","year":"2014","journal-title":"Physiol Behav"},{"key":"ref73","doi-asserted-by":"crossref","first-page":"e92576","DOI":"10.1371\/journal.pone.0092576","article-title":"The novelty-seeking phenotype modulates the long-lasting effects of intermittent ethanol administration during adolescence","volume":"9","author":"S Montagud-Romero","year":"2014","journal-title":"PloS one"},{"key":"ref74","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.pbb.2012.03.031","article-title":"High novelty-seeking predicts greater sensitivity to the conditioned rewarding effects of cocaine","volume":"102","author":"A Vidal-Infer","year":"2012","journal-title":"Pharmacol Biochem Behav"},{"key":"ref75","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1016\/j.physbeh.2008.12.011","article-title":"Effects of extended cocaine conditioning in the reinstatement of placepreference","volume":"96","author":"M Rodr\u00edguez-Arias","year":"2009","journal-title":"Physiol Behav"},{"key":"ref76","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1007\/s002130100858","article-title":"Repeated social-defeat stress, cocaine or morphine","volume":"158","author":"HE Covington","year":"2001","journal-title":"Psychopharmacology"},{"key":"ref77","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1097\/01.fbp.0000190685.84984.ec","article-title":"Minarro. Gammahydroxybutyric acid affects the acquisition and reinstatement of cocaine-induced conditioned place preference in mice","volume":"17","author":"C Maldonado","year":"2006","journal-title":"Behav Pharmacol"},{"key":"ref78","author":"G. Paxinos","unstructured":"Paxinos: <name name-style=\"western\"><surname>Paxinos<\/surname> <given-names>G.<\/given-names><\/name>, <name name-style=\"western\"><surname>Franklin<\/surname> <given-names>K.B.J.<\/given-names><\/name> 208. <chapter-title>The mouse brain in stereotaxic coordinates<\/chapter-title>. <edition>3rd Ed<\/edition>. <publisher-name>Academic Press<\/publisher-name>, <publisher-loc>New York<\/publisher-loc>."},{"key":"ref79","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1002\/glia.20445","article-title":"S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage","volume":"55","author":"E Raponi","year":"2007","journal-title":"Glia"},{"key":"ref80","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1523\/JNEUROSCI.2276-17.2017","article-title":"Synaptic Regulator \u03b1-Synuclein in Dopaminergic Fibers Is Essentially Required for the Maintenance of Subependymal Neural Stem Cells","volume":"38","author":"A Perez-Villalba","year":"2018","journal-title":"J Neurosci"},{"key":"ref81","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.schres.2015.01.015","article-title":"Decreased glial reactivity could be involved in the antipsychotic-like effect of cannabidiol","volume":"164","author":"FV Gomes","year":"2015","journal-title":"Schizophr Res"},{"key":"ref82","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1742-2094-9-71","article-title":"Prenatal stress causes alterations in the morphology of microglia and the inflammatory response of the hippocampus of adult female mice","volume":"9","author":"Y Diz-Chaves","year":"2012","journal-title":"Journal Neuroinflammation"},{"key":"ref83","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.nbd.2014.07.004","article-title":"Sex differences in the neurobiology of epilepsy: a preclinical perspective","volume":"72","author":"HE Scharfman","year":"2014","journal-title":"Neurobiol Disease"},{"key":"ref84","doi-asserted-by":"crossref","first-page":"42","DOI":"10.32607\/20758251-2015-7-2-42-47","article-title":"NeuN as a neuronal nuclear antigen and neuron differentiation marker","volume":"7","author":"VV Guselnikova","year":"2015","journal-title":"Acta Naturae"},{"key":"ref85","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.brainres.2010.06.062","article-title":"Adolescent social defeat alters neural, endocrine and behavioral responses to amphetamine in adult male rats","volume":"1352","author":"AR Burke","year":"2010","journal-title":"Brain Res"},{"key":"ref86","doi-asserted-by":"crossref","first-page":"6277","DOI":"10.1523\/JNEUROSCI.0450-11.2011","article-title":"\u03b2-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat","volume":"31","author":"ES Wohleb","year":"2011","journal-title":"J Neurosci"},{"key":"ref87","doi-asserted-by":"crossref","first-page":"1491","DOI":"10.1016\/j.psyneuen.2012.02.003","article-title":"Peripheral innate immune challenge exaggerated microglia activation, increased the number of inflammatory CNS macrophages, and prolonged social withdrawal in socially defeated mice","volume":"37","author":"ES Wohleb","year":"2012","journal-title":"Psychoneuroendocrinology"},{"key":"ref88","doi-asserted-by":"crossref","first-page":"1784","DOI":"10.1093\/cercor\/bhs151","article-title":"Chronic stress induced remodeling of the prefrontal cortex: structural re-organization of microglia and the inhibitory effect of minocycline","volume":"23","author":"M Hinwood","year":"2013","journal-title":"Cereb Cortex"},{"key":"ref89","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1038\/mp.2013.155","article-title":"Dynamic microglial alterations underlie stress-induced depressive-like behavior and suppressed neurogenesis","volume":"19","author":"T Kreisel","year":"2014","journal-title":"Mol Psychiatry"},{"key":"ref90","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.bbi.2015.10.003","article-title":"Differential effects of stress on microglial cell activation in male and female medial prefrontal cortex","volume":"52","author":"JL Bollinger","year":"2016","journal-title":"Brain Behav Immun"},{"key":"ref91","doi-asserted-by":"crossref","first-page":"13820","DOI":"10.1523\/JNEUROSCI.1671-13.2013","article-title":"Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior","volume":"33","author":"ES Wohleb","year":"2013","journal-title":"J Neurosci"},{"key":"ref92","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1006\/frne.1996.0005","article-title":"Endocrine glia: roles of glial cells in the brain actions of steroid and thyroid hormones and in the regulation of hormone secretion","volume":"17","author":"LM Garcia- Segura","year":"1996","journal-title":"Frontiers Neuroendocrinol"},{"key":"ref93","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0169-328X(90)90066-M","article-title":"Messenger RNA for glial fibrillary acidic protein is decreased in rat brain following acute and chronic corticosterone treatment","volume":"7","author":"NR Nichols","year":"1990","journal-title":"Brain Res Mol Brain Res"},{"key":"ref94","doi-asserted-by":"crossref","first-page":"860","DOI":"10.1111\/j.1471-4159.1991.tb08230.x","article-title":"Glucocorticoids regulate the synthesis of glial fibrillary acidic protein in intact and adrenalectomized rats but do not affect its expression following brain injury","volume":"57","author":"JP O'Callaghan","year":"1991","journal-title":"J Neurochem"},{"key":"ref95","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1007\/s00213-012-2741-x","article-title":"Chronic psychosocial stress and citalopram modulate the expression of the glial proteins GFAP and NDRG2 in the hippocampus","volume":"224","author":"C Araya-Call\u00eds","year":"2012","journal-title":"Psychopharmacology"},{"key":"ref96","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1016\/0306-4522(92)90277-9","article-title":"Acute systemic heat stress increases glial fibrillary acidic protein immunoreactivity in brain: experimental observations in conscious normotensive young rats","volume":"48","author":"HS Sharma","year":"1992","journal-title":"Neuroscience"},{"key":"ref97","doi-asserted-by":"crossref","first-page":"275","DOI":"10.3109\/10253890009001133","article-title":"Activity-stress increases density of GFAP-immunoreactive astrocytes in the rat hippocampus","volume":"3","author":"KG Lambert","year":"2000","journal-title":"Stress"},{"key":"ref98","doi-asserted-by":"crossref","first-page":"159","DOI":"10.3389\/fnagi.2015.00159","article-title":"Hippocampal cytogenesis and spatial learning in senile rats exposed to chronic variable stress: effects of previous early life exposure to mild stress","volume":"7","author":"F Jauregui-Huerta","year":"2015","journal-title":"Front Aging Neurosci"},{"key":"ref99","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/j.neuroscience.2009.02.074","article-title":"Juvenile separation stress induces rapid region- and layer-specific changes in S100ss- and glial fibrillary acidic protein-immunoreactivity in astrocytes of the rodent medial prefrontal cortex","volume":"160","author":"K Braun","year":"2009","journal-title":"Neuroscience"},{"key":"ref100","doi-asserted-by":"crossref","first-page":"1616","DOI":"10.1038\/sj.npp.1300982","article-title":"Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment","volume":"31","author":"B Cz\u00e9h","year":"2006","journal-title":"Neuropsychopharmacology"},{"key":"ref101","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1038\/mp.2008.106","article-title":"Glial pathology in an animal model of depression: reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole","volume":"15","author":"M Banasr","year":"2010","journal-title":"Mol Psychiatry"},{"key":"ref102","doi-asserted-by":"crossref","first-page":"2590","DOI":"10.1523\/JNEUROSCI.2394-15.2016","article-title":"Neuroinflammatory dynamics underlie memory impairments after repeated social defeat","volume":"36","author":"DB McKim","year":"2016","journal-title":"J Neurosci"},{"key":"ref103","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.jpsychires.2017.06.012","article-title":"Brain-derived neurotrophic factor signaling plays a role in resilience to stress promoted by isoquinoline in defeated mice","volume":"94","author":"AP Pesarico","year":"2017","journal-title":"J Psychiatr Res"},{"key":"ref104","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1515\/RNS.2011.044","article-title":"Structural and synaptic plasticity in stress-related disorders","volume":"22","author":"DJ Christoffel","year":"2011","journal-title":"Rev Neurosci"},{"key":"ref105","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.1002\/mnfr.201400753","article-title":"Orientin improves depression-like behavior and BDNF in chronic stressed mice","volume":"59","author":"Y Liu","year":"2015","journal-title":"Mol Nutr Food Res"},{"key":"ref106","doi-asserted-by":"crossref","first-page":"1300","DOI":"10.1002\/hipo.20966","article-title":"Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces deficits in spatial location memory in adulthood","volume":"22","author":"CM McCormick","year":"2012","journal-title":"Hippocampus"},{"key":"ref107","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1002\/syn.20483","article-title":"The enduring effects of an adolescent social stressor on synaptic density, part II: Poststress reversal of synaptic loss in the cortex by adinazolam and MK-801","volume":"62","author":"MP Leussis","year":"2008","journal-title":"Synapse"},{"key":"ref108","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1007\/s00213-014-3632-0","article-title":"Effects of acute and repeated cocaine on markers for neural plasticity within the mesolimbic system in rats","volume":"232","author":"N Rodriguez-Espinosa","year":"2015","journal-title":"Psychopharmacology"},{"key":"ref109","doi-asserted-by":"crossref","first-page":"2749","DOI":"10.5762\/KAIS.2013.14.6.2749","article-title":"The relationship between emotional intelligence and communication skill, clinical competence &amp; clinical practice stress in nursing students","volume":"14","author":"OS Lee","year":"2013","journal-title":"J Korea Acad Industr Coop Soc"},{"key":"ref110","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.neubiorev.2015.10.006","article-title":"Defeat stress in rodents: from behavior to molecules","volume":"59","author":"C Hammels","year":"2015","journal-title":"Neurosci Biobehav Rev"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0206421","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,11]],"date-time":"2024-07-11T20:26:34Z","timestamp":1720729594000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0206421"}},"subtitle":[],"editor":[{"given":"Sergio D.","family":"I\u00f1iguez","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2018,10,26]]},"references-count":110,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2018,10,26]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0206421","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,10,26]]}}}