{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T02:59:09Z","timestamp":1792119549859,"version":"4.4.0"},"reference-count":49,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2025,11,1]],"date-time":"2025-11-01T00:00:00Z","timestamp":1761955200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2025,11,1]],"date-time":"2025-11-01T00:00:00Z","timestamp":1761955200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2025,9,12]],"date-time":"2025-09-12T00:00:00Z","timestamp":1757635200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003196","name":"Ministry of Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100003196","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100021856","name":"Ministero dell&apos;Universit\u00e0 e della Ricerca","doi-asserted-by":"publisher","award":["202277LAA7"],"award-info":[{"award-number":["202277LAA7"]}],"id":[{"id":"10.13039\/501100021856","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100021856","name":"Ministero dell&apos;Universit\u00e0 e della Ricerca","doi-asserted-by":"publisher","award":["2017AY8BP4"],"award-info":[{"award-number":["2017AY8BP4"]}],"id":[{"id":"10.13039\/501100021856","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100021856","name":"Ministero dell&apos;Universit\u00e0 e della Ricerca","doi-asserted-by":"publisher","award":["ARS01_01226"],"award-info":[{"award-number":["ARS01_01226"]}],"id":[{"id":"10.13039\/501100021856","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010661","name":"Horizon 2020 Framework Programme","doi-asserted-by":"publisher","award":["848158"],"award-info":[{"award-number":["848158"]}],"id":[{"id":"10.13039\/100010661","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Neurobiology of Stress"],"published-print":{"date-parts":[[2025,11]]},"DOI":"10.1016\/j.ynstr.2025.100761","type":"journal-article","created":{"date-parts":[[2025,9,17]],"date-time":"2025-09-17T05:41:37Z","timestamp":1758087697000},"page":"100761","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":5,"special_numbering":"C","title":["Exposure to early-life stress uncovers shared biological signatures underlying vulnerability in the habenula and insular cortex of male and female adult rats"],"prefix":"10.1016","volume":"39","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6628-5999","authenticated-orcid":false,"given":"Valentina","family":"Zonca","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Moira","family":"Marizzoni","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samantha","family":"Saleri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Monica","family":"Mazzelli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giulia","family":"Petrillo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Grazia","family":"Di Benedetto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Floriana","family":"De Cillis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marco Andrea","family":"Riva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Annamaria","family":"Cattaneo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"issue":"1","key":"10.1016\/j.ynstr.2025.100761_bib1","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1007\/s10142-021-00821-9","article-title":"BioNERO: an all-in-one R\/Bioconductor package for comprehensive and easy biological network reconstruction","volume":"22","author":"Almeida-Silva","year":"2022","journal-title":"Funct. Integr. Genomics"},{"key":"10.1016\/j.ynstr.2025.100761_bib2","doi-asserted-by":"crossref","first-page":"335","DOI":"10.3389\/fnins.2015.00335","article-title":"Oxytocin and vasopressin: linking pituitary neuropeptides and their receptors to social neurocircuits","volume":"9","author":"Baribeau","year":"2015","journal-title":"Front. Neurosci."},{"issue":"9\u201310","key":"10.1016\/j.ynstr.2025.100761_bib3","doi-asserted-by":"crossref","first-page":"2326","DOI":"10.1111\/ejn.15181","article-title":"High-fat diet during adulthood interacts with prenatal stress, affecting both brain inflammatory and neuroendocrine markers in male rats","volume":"55","author":"Berry","year":"2022","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.ynstr.2025.100761_bib4","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.euroneuro.2022.02.002","article-title":"Preclinical animal models of mental illnesses to translate findings from the bench to the bedside: molecular brain mechanisms and peripheral biomarkers associated to early life stress or immune challenges","volume":"58","author":"Cattane","year":"2022","journal-title":"Eur. Neuropsychopharmacol."},{"key":"10.1016\/j.ynstr.2025.100761_bib5","doi-asserted-by":"crossref","DOI":"10.1016\/j.pharmthera.2024.108686","article-title":"Early life adversities, psychopathologies and novel pharmacological strategies","volume":"260","author":"Cattaneo","year":"2024","journal-title":"Pharmacol. Ther."},{"key":"10.1016\/j.ynstr.2025.100761_bib6","doi-asserted-by":"crossref","first-page":"25","DOI":"10.3389\/fnint.2013.00025","article-title":"Serotonin modulation of cortical neurons and networks","volume":"7","author":"Celada","year":"2013","journal-title":"Front. Integr. Neurosci."},{"issue":"1","key":"10.1016\/j.ynstr.2025.100761_bib7","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-020-74481-3","article-title":"Repeated stress exposure in mid-adolescence attenuates behavioral, noradrenergic, and epigenetic effects of trauma-like stress in early adult male rats","volume":"10","author":"Chaby","year":"2020","journal-title":"Sci. Rep."},{"issue":"2","key":"10.1016\/j.ynstr.2025.100761_bib8","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.bpsgos.2022.02.009","article-title":"Adolescent stress confers resilience to traumatic stress later in life: role of the prefrontal cortex","volume":"3","author":"Cotella","year":"2023","journal-title":"Biol. Psychiatry Glob. Open Sci."},{"issue":"1","key":"10.1016\/j.ynstr.2025.100761_bib9","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1038\/s41398-023-02653-6","article-title":"Vulnerability and resilience to prenatal stress exposure: behavioral and molecular characterization in adolescent rats","volume":"13","author":"Creutzberg","year":"2023","journal-title":"Transl. Psychiatry"},{"key":"10.1016\/j.ynstr.2025.100761_bib10","doi-asserted-by":"crossref","DOI":"10.1016\/j.pnpbp.2025.111344","article-title":"Sex-specific metabolic and inflammatory alterations in adult animals vulnerable to prenatal stress exposure","volume":"138","author":"D'Aprile","year":"2025","journal-title":"Prog. Neuropsychopharmacol. Biol. Psychiatry"},{"issue":"6","key":"10.1016\/j.ynstr.2025.100761_bib11","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1001\/jamapsychiatry.2024.0039","article-title":"Adverse childhood experiences and adult mental health outcomes","volume":"81","author":"Danielsdottir","year":"2024","journal-title":"JAMA Psychiatry"},{"key":"10.1016\/j.ynstr.2025.100761_bib12","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/j.jpsychires.2023.06.014","article-title":"Reduced sociability in a prenatal immune activation model: modulation by a chronic blonanserin treatment through the amygdala-hippocampal axis","volume":"164","author":"Deriha","year":"2023","journal-title":"J. Psychiatr. Res."},{"issue":"1","key":"10.1016\/j.ynstr.2025.100761_bib13","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.neuropharm.2011.08.049","article-title":"Investigating anxiety and depressive-like phenotypes in genetic mouse models of serotonin depletion","volume":"62","author":"Fernandez","year":"2012","journal-title":"Neuropharmacology"},{"issue":"5","key":"10.1016\/j.ynstr.2025.100761_bib14","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1016\/j.neuron.2012.08.016","article-title":"Neural mechanisms of stress resilience and vulnerability","volume":"75","author":"Franklin","year":"2012","journal-title":"Neuron"},{"issue":"1","key":"10.1016\/j.ynstr.2025.100761_bib15","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1111\/gbb.12106","article-title":"Beyond modules and hubs: the potential of gene coexpression networks for investigating molecular mechanisms of complex brain disorders","volume":"13","author":"Gaiteri","year":"2014","journal-title":"Gene Brain Behav."},{"key":"10.1016\/j.ynstr.2025.100761_bib16","first-page":"364","article-title":"Ethological evaluation of the effects of social defeat stress in mice: beyond the social interaction ratio","volume":"9","author":"Henriques-Alves","year":"2015","journal-title":"Front. Behav. Neurosci."},{"issue":"6","key":"10.1016\/j.ynstr.2025.100761_bib17","doi-asserted-by":"crossref","first-page":"914","DOI":"10.1016\/S0893-133X(02)00374-3","article-title":"Evaluation of antidepressant-related behavioral responses in mice lacking the serotonin transporter","volume":"27","author":"Holmes","year":"2002","journal-title":"Neuropsychopharmacology"},{"issue":"2","key":"10.1016\/j.ynstr.2025.100761_bib18","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1007\/s00213-007-0895-8","article-title":"Acute and constitutive increases in central serotonin levels reduce social play behaviour in peri-adolescent rats","volume":"195","author":"Homberg","year":"2007","journal-title":"Psychopharmacology (Berl)"},{"key":"10.1016\/j.ynstr.2025.100761_bib19","doi-asserted-by":"crossref","DOI":"10.1016\/j.chiabu.2020.104361","article-title":"Child maltreatment and depression: a meta-analysis of studies using the childhood trauma questionnaire","volume":"102","author":"Humphreys","year":"2020","journal-title":"Child Abuse Negl."},{"key":"10.1016\/j.ynstr.2025.100761_bib20","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.neures.2015.01.005","article-title":"Lateralization, maturation, and anteroposterior topography in the lateral habenula revealed by ZIF268\/EGR1 immunoreactivity and labeling history of neuronal activity","volume":"95","author":"Ichijo","year":"2015","journal-title":"Neurosci. Res."},{"key":"10.1016\/j.ynstr.2025.100761_bib21","doi-asserted-by":"crossref","DOI":"10.1016\/j.archoralbio.2021.105245","article-title":"Maternal chewing improves prenatal stress-induced cognitive deficit and anxiety-like behavior associated with alterations of the apoptotic response and serotonin pathway in mouse offspring","volume":"130","author":"Kajimoto","year":"2021","journal-title":"Arch. Oral Biol."},{"issue":"4","key":"10.1016\/j.ynstr.2025.100761_bib22","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1111\/j.1601-183X.2006.00270.x","article-title":"Hypolocomotion, anxiety and serotonin syndrome-like behavior contribute to the complex phenotype of serotonin transporter knockout mice","volume":"6","author":"Kalueff","year":"2007","journal-title":"Gene Brain Behav."},{"issue":"1","key":"10.1016\/j.ynstr.2025.100761_bib23","doi-asserted-by":"crossref","first-page":"6329","DOI":"10.1038\/s41467-021-26569-1","article-title":"A habenula-insular circuit encodes the willingness to act","volume":"12","author":"Khalighinejad","year":"2021","journal-title":"Nat. Commun."},{"issue":"4","key":"10.1016\/j.ynstr.2025.100761_bib24","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1093\/bioinformatics\/btt703","article-title":"Causal analysis approaches in ingenuity pathway analysis","volume":"30","author":"Kramer","year":"2014","journal-title":"Bioinformatics"},{"issue":"4","key":"10.1016\/j.ynstr.2025.100761_bib25","doi-asserted-by":"crossref","DOI":"10.1523\/ENEURO.0166-18.2018","article-title":"Genetic control of Myelin plasticity after chronic psychosocial stress","volume":"5","author":"Laine","year":"2018","journal-title":"eNeuro"},{"key":"10.1016\/j.ynstr.2025.100761_bib26","doi-asserted-by":"crossref","DOI":"10.1016\/j.psyneuen.2020.104794","article-title":"Alterations in 'inflammatory' pathways in the rat prefrontal cortex as early biological predictors of the long-term negative consequences of exposure to stress early in life","volume":"124","author":"Lopizzo","year":"2021","journal-title":"Psychoneuroendocrinology"},{"issue":"12","key":"10.1016\/j.ynstr.2025.100761_bib27","doi-asserted-by":"crossref","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":"10.1016\/j.ynstr.2025.100761_bib28","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1016\/j.bbi.2023.07.022","article-title":"Multi-omics approaches in psychoneuroimmunology and health research: conceptual considerations and methodological recommendations","volume":"114","author":"Mengelkoch","year":"2023","journal-title":"Brain Behav. Immun."},{"issue":"9","key":"10.1016\/j.ynstr.2025.100761_bib29","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1008358","article-title":"Multi-omics analysis identifies mitochondrial pathways associated with anxiety-related behavior","volume":"15","author":"Misiewicz","year":"2019","journal-title":"PLoS Genet."},{"issue":"1","key":"10.1016\/j.ynstr.2025.100761_bib30","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1038\/s41398-021-01774-0","article-title":"Reward and aversion encoding in the lateral habenula for innate and learned behaviours","volume":"12","author":"Mondoloni","year":"2022","journal-title":"Transl. Psychiatry"},{"key":"10.1016\/j.ynstr.2025.100761_bib31","doi-asserted-by":"crossref","DOI":"10.1016\/j.pnpbp.2023.110783","article-title":"Early life stress impairs brain and mental development during childhood increasing the risk of developing psychiatric disorders","volume":"126","author":"Nakama","year":"2023","journal-title":"Prog. Neuropsychopharmacol. Biol. Psychiatry"},{"issue":"4","key":"10.1016\/j.ynstr.2025.100761_bib32","doi-asserted-by":"crossref","first-page":"E480","DOI":"10.1503\/jpn.200226","article-title":"Early-life experiences altered the maturation of the lateral habenula in mouse models, resulting in behavioural disorders in adulthood","volume":"46","author":"Nakamura","year":"2021","journal-title":"J. Psychiatry Neurosci."},{"issue":"8","key":"10.1016\/j.ynstr.2025.100761_bib33","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1176\/appi.ajp.2020.20091340","article-title":"Disrupted dorsal mid-insula activation during interoception across psychiatric disorders","volume":"178","author":"Nord","year":"2021","journal-title":"Am. J. Psychiatr."},{"issue":"1","key":"10.1016\/j.ynstr.2025.100761_bib34","doi-asserted-by":"crossref","first-page":"104","DOI":"10.3390\/neurosci3010008","article-title":"Early life stress and brain plasticity: from alterations of brain morphology to development of psychopathology","volume":"3","author":"Oginga","year":"2022","journal-title":"NeuroSci"},{"key":"10.1016\/j.ynstr.2025.100761_bib35","article-title":"Emotional dysregulation following prenatal stress is associated with altered prefrontal cortex responsiveness to an acute challenge in adolescence","volume":"136","author":"Orso","year":"2024","journal-title":"Prog. Neuropsychopharmacol. Biol. Psychiatry"},{"key":"10.1016\/j.ynstr.2025.100761_bib36","doi-asserted-by":"crossref","DOI":"10.1016\/j.pnpbp.2024.111162","article-title":"Emotional dysregulation following prenatal stress is associated with altered prefrontal cortex responsiveness to an acute challenge in adolescence","volume":"136","author":"Orso","year":"2025","journal-title":"Prog. Neuropsychopharmacol. Biol. Psychiatry"},{"issue":"9","key":"10.1016\/j.ynstr.2025.100761_bib37","doi-asserted-by":"crossref","first-page":"1146","DOI":"10.1038\/nn.3779","article-title":"Reward processing by the lateral habenula in normal and depressive behaviors","volume":"17","author":"Proulx","year":"2014","journal-title":"Nat. Neurosci."},{"issue":"6","key":"10.1016\/j.ynstr.2025.100761_bib38","doi-asserted-by":"crossref","first-page":"1156","DOI":"10.1038\/s41386-022-01292-7","article-title":"Insular cortex corticotropin-releasing factor integrates stress signaling with social affective behavior","volume":"47","author":"Rieger","year":"2022","journal-title":"Neuropsychopharmacology"},{"key":"10.1016\/j.ynstr.2025.100761_bib39","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.neubiorev.2019.06.005","article-title":"An insular view of the social decision-making network","volume":"103","author":"Rogers-Carter","year":"2019","journal-title":"Neurosci. Biobehav. Rev."},{"issue":"44","key":"10.1016\/j.ynstr.2025.100761_bib40","doi-asserted-by":"crossref","first-page":"8717","DOI":"10.1523\/JNEUROSCI.0316-19.2019","article-title":"Insular Cortex projections to nucleus accumbens core mediate social approach to stressed Juvenile rats","volume":"39","author":"Rogers-Carter","year":"2019","journal-title":"J. Neurosci."},{"key":"10.1016\/j.ynstr.2025.100761_bib41","series-title":"RRHO: Test Overlap Using the Rank-Rank Hypergeometric Test","author":"Rosenblatt","year":"2014"},{"issue":"Suppl. l_1","key":"10.1016\/j.ynstr.2025.100761_bib42","article-title":"How is prenatal stress transmitted from the mother to the fetus?","volume":"227","author":"Sze","year":"2024","journal-title":"J. Exp. Biol."},{"issue":"D1","key":"10.1016\/j.ynstr.2025.100761_bib43","doi-asserted-by":"crossref","first-page":"D638","DOI":"10.1093\/nar\/gkac1000","article-title":"The STRING database in 2023: protein-protein association networks and functional enrichment analyses for any sequenced genome of interest","volume":"51","author":"Szklarczyk","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.ynstr.2025.100761_bib44","doi-asserted-by":"crossref","first-page":"34","DOI":"10.3389\/fnsyn.2016.00034","article-title":"Can the lateral habenula crack the Serotonin code?","volume":"8","author":"Tchenio","year":"2016","journal-title":"Front. Synaptic Neurosci."},{"issue":"11","key":"10.1016\/j.ynstr.2025.100761_bib45","doi-asserted-by":"crossref","DOI":"10.3390\/ijms24119647","article-title":"Pro- and anti-inflammatory prostaglandins and cytokines in humans: a mini review","volume":"24","author":"Wautier","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"10.1016\/j.ynstr.2025.100761_bib46","doi-asserted-by":"crossref","DOI":"10.3389\/fnbeh.2021.786011","article-title":"Inhibition within the lateral habenula-implications for affective disorders","volume":"15","author":"Webster","year":"2021","journal-title":"Front. Behav. Neurosci."},{"key":"10.1016\/j.ynstr.2025.100761_bib47","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1016\/j.bbi.2024.02.006","article-title":"Hyperactive lateral habenula mediates the comorbidity between rheumatoid arthritis and depression-like behaviors","volume":"117","author":"Wu","year":"2024","journal-title":"Brain Behav. Immun."},{"key":"10.1016\/j.ynstr.2025.100761_bib48","article-title":"Activation of AMPA receptors in the lateral habenula produces anxiolytic effects in a rat model of Parkinson's disease","volume":"13","author":"Zhang","year":"2022","journal-title":"Front. Pharmacol."},{"issue":"1","key":"10.1016\/j.ynstr.2025.100761_bib49","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/s11427-023-2406-3","article-title":"Potentiation of the lateral habenula-ventral tegmental area pathway underlines the susceptibility to depression in mice with chronic pain","volume":"67","author":"Zhang","year":"2024","journal-title":"Sci. China Life Sci."}],"container-title":["Neurobiology of Stress"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2352289525000554?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2352289525000554?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2026,5,15]],"date-time":"2026-05-15T19:14:32Z","timestamp":1778872472000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S2352289525000554"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11]]},"references-count":49,"alternative-id":["S2352289525000554"],"URL":"https:\/\/doi.org\/10.1016\/j.ynstr.2025.100761","relation":{},"ISSN":["2352-2895"],"issn-type":[{"value":"2352-2895","type":"print"}],"subject":[],"published":{"date-parts":[[2025,11]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Exposure to early-life stress uncovers shared biological signatures underlying vulnerability in the habenula and insular cortex of male and female adult rats","name":"articletitle","label":"Article Title"},{"value":"Neurobiology of Stress","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.ynstr.2025.100761","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2025 The Authors. Published by Elsevier Inc.","name":"copyright","label":"Copyright"}],"article-number":"100761"}}