{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,2]],"date-time":"2026-04-02T03:53:50Z","timestamp":1775102030514,"version":"3.50.1"},"reference-count":48,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,6,9]],"date-time":"2023-06-09T00:00:00Z","timestamp":1686268800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100005635","name":"Funda\u00e7\u00e3o Calouste Gulbenkian","doi-asserted-by":"publisher","award":["P-139977"],"award-info":[{"award-number":["P-139977"]}],"id":[{"id":"10.13039\/501100005635","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100019370","name":"Foundation for Science and Technology","doi-asserted-by":"publisher","award":["PTDC\/MED-NEU\/29071\/2017"],"award-info":[{"award-number":["PTDC\/MED-NEU\/29071\/2017"]}],"id":[{"id":"10.13039\/501100019370","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100019370","name":"Foundation for Science and Technology","doi-asserted-by":"publisher","award":["UIDB\/50026\/2020"],"award-info":[{"award-number":["UIDB\/50026\/2020"]}],"id":[{"id":"10.13039\/501100019370","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100019370","name":"Foundation for Science and Technology","doi-asserted-by":"publisher","award":["UIDP\/50026\/2020"],"award-info":[{"award-number":["UIDP\/50026\/2020"]}],"id":[{"id":"10.13039\/501100019370","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Behav. Neurosci."],"abstract":"<jats:p>Being social animals, rats exhibit a range of social behaviors that help them build social bonds and maintain group cohesion. Behavior is influenced by multiple factors, including stress exposure, and the expression of the impact of stress on both social and non-social behaviors may also be affected by the living conditions of rats. In this study, we explored the physiological and behavioral effects of chronic unpredictable stress on group-housed rats in the PhenoWorld (PhW), a socially and physically enriched environment closer to real-life conditions. Two independent experiments were performed: one in the control condition (PhW control, n = 8) and one in the stress condition (PhW stress, n = 8). Control animals remained undisturbed except for cage cleaning and daily handling procedures. Stress group animals were all exposed to chronic unpredictable stress. Data confirm that stress exposure triggers anxiety-like behavior in the PhW. In terms of home-cage behaviors, we found that stress affects social behaviors (by decreased playing and increased huddling behaviors) and non-social behaviors (as shown by the decrease in rearing and walking behaviors). These results are of relevance to expand our knowledge on the influence of stress on social and non-social behaviors, which are of importance to understand better species-typical behaviors.<\/jats:p>","DOI":"10.3389\/fnbeh.2023.1195011","type":"journal-article","created":{"date-parts":[[2023,6,9]],"date-time":"2023-06-09T04:31:10Z","timestamp":1686285070000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":11,"title":["Home-cage behavior is impacted by stress exposure in rats"],"prefix":"10.3389","volume":"17","author":[{"given":"Evren","family":"Eraslan","sequence":"first","affiliation":[]},{"given":"Magda Jo\u00e3o","family":"Castelhano-Carlos","sequence":"additional","affiliation":[]},{"given":"Liliana","family":"Amorim","sequence":"additional","affiliation":[]},{"given":"Carina","family":"Soares-Cunha","sequence":"additional","affiliation":[]},{"given":"Ana Jo\u00e3o","family":"Rodrigues","sequence":"additional","affiliation":[]},{"given":"Nuno","family":"Sousa","sequence":"additional","affiliation":[]}],"member":"1965","published-online":{"date-parts":[[2023,6,9]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1016\/j.beproc.07002","article-title":"The effects of enhancing cage complexity on the behaviour and welfare of laboratory rats","volume":"85","author":"Abou-Ismail","year":"2010","journal-title":"Behav. Processes"},{"key":"B2","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.beproc.11011","article-title":"Play and optimal welfare: Does play indicate the presence of positive affective states?","volume":"156","author":"Ahloy-Dallaire","year":"2018","journal-title":"Behav. Processes"},{"key":"B3","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1007\/BF03349373","article-title":"Circadian rhythmicity of ACTH and corticosterone in the rat","volume":"3","author":"Allen-Rowlands","year":"1980","journal-title":"J. Endocrinol. Investig. Off. J. Ital. Soc. Endocrinol"},{"key":"B4","doi-asserted-by":"publisher","first-page":"e1058","DOI":"10.1038\/tp.2017.29","article-title":"Adult hippocampal neuroplasticity triggers susceptibility to recurrent depression","volume":"7","author":"Alves","year":"2017","journal-title":"Transl. Psychiatry"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.3389\/fnbeh.2022.999325","article-title":"Shaping social behavior in an enriched environment","author":"Amorim","year":"2022","journal-title":"Front. Behav. Neurosci"},{"key":"B6","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/jne.12383","article-title":"Paper or Plastic? Exploring the effects of natural enrichment on behavioural and neuroendocrine responses in Long-Evans rats","volume":"28","author":"Bardi","year":"2016","journal-title":"J. Neuroendocrinol"},{"key":"B7","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1007\/BF00181937","article-title":"The effects of chronic antidepressant treatment in an animal model of anxiety","volume":"95","author":"Bodnoff","year":"1988","journal-title":"Psychopharmacology"},{"key":"B8","doi-asserted-by":"publisher","first-page":"8483","DOI":"10.1371.\/journal.pone.0068483","article-title":"Defensive aggregation (Huddling) in Rattus Norvegicus toward predator odor : Individual differences, social buffering effects and neural correlates","volume":"8","author":"Bowen","year":"2013","journal-title":"PLoS ONE"},{"key":"B9","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12915-021-01184-0","article-title":"Conventional laboratory housing increases morbidity and mortality in research rodents: Results of a meta-analysis","volume":"20","author":"Cait","year":"2022","journal-title":"BMC Biol"},{"key":"B10","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1017\/s096272860002248x","article-title":"Repetitive backflipping behaviour in captive roof rats (Rattus rattus) and the effects of cage enrichment","volume":"9","author":"Callard","year":"2000","journal-title":"Anim. Welf"},{"key":"B11","doi-asserted-by":"publisher","first-page":"e399","DOI":"10.1038\/tp.2014.40","article-title":"PhenoWorld: a new paradigm to screen rodent behavior","volume":"4","author":"Castelhano-Carlos","year":"2014","journal-title":"Transl. Psychiatry"},{"key":"B12","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/0091-3057(95)02169-8","article-title":"Affiliation in periadolescent rats: Behavioral and corticosterone response to social reunion with familiar or unfamiliar partners","volume":"54","author":"Cirulli","year":"1996","journal-title":"Pharmacol. Biochem. Behav"},{"key":"B13","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.psyneuen.10021","article-title":"Environmental enrichment models a naturalistic form of maternal separation and shapes the anxiety response patterns of offspring","volume":"52","author":"Connors","year":"2015","journal-title":"Psychoneuroendocrinology"},{"key":"B14","doi-asserted-by":"publisher","author":"Crockford","year":"2017","DOI":"10.1007.\/7854_2017_12"},{"key":"B15","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1016\/S0006-8993(00)03000-6","article-title":"Chronic stress regulates levels of mRNA transcripts encoding \u03b2 subunits of the GABAA receptor in the rat stress axis","volume":"887","author":"Cullinan","year":"2000","journal-title":"Brain Res"},{"key":"B16","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1163\/156853967X00055","article-title":"A behavioural study of the home-cage activity of the white rat","volume":"28","author":"Draper","year":"1967","journal-title":"Behaviour"},{"key":"B17","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1016\/j.bbr.06007","article-title":"(2012). Cage-induced stereotypies, perseveration and the effects of environmental enrichment in laboratory mice","volume":"234","author":"Gross","year":"2012","journal-title":"Behav. Brain Res"},{"key":"B18","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1080\/10253890.2019.1702642","article-title":"The effect of traumatic-like stress exposure on alterations in the temporal social behavior of a rodent population","volume":"23","author":"Han","year":"2020","journal-title":"Stress"},{"key":"B19","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1016\/j.bbr.08004","article-title":"(2016). Effects of environmental enrichment on anxiety-like behavior, sociability, sensory gating, and spatial learning in male and female C57BL\/6J mice","volume":"314","author":"Hendershott","year":"2016","journal-title":"Behav. Brain Res"},{"key":"B20","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1016\/j.expneurol.12003","article-title":"The habenula as a critical node in chronic stress-related anxiety","volume":"289","author":"Jacinto","year":"2017","journal-title":"Exp. Neurol"},{"key":"B21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/ani9121026","article-title":"Assessing affective state in laboratory rodents to promote animal welfare\u2014what is the progress in applied refinement research?","volume":"9","author":"Jirkof","year":"2019","journal-title":"Animals"},{"key":"B22","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1016\/j.neuroscience.11035","article-title":"Complex environmental rearing enhances social salience and affects hippocampal corticotropin releasing hormone receptor expression in a sex-specific manner","volume":"369","author":"Kentner","year":"2018","journal-title":"Neuroscience"},{"key":"B23","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1002\/dev.20413","article-title":"The effects of stress on play and home cage behaviors in adolescent male rats","volume":"52","author":"Klein","year":"2010","journal-title":"Dev. Psychobiol"},{"key":"B24","doi-asserted-by":"publisher","first-page":"1291","DOI":"10.1016\/j.neubiorev.02003","article-title":"E. (2011). Stress revisited: a critical evaluation of the stress concept","volume":"35","author":"Koolhaas","year":"2011","journal-title":"Neurosci. Biobehav. Rev"},{"key":"B25","doi-asserted-by":"crossref","first-page":"11","DOI":"10.3758\/BF03331885","article-title":"A pheromone associated with social dominance among male rats","volume":"16","author":"Kramess","year":"1969","journal-title":"Psychon. Sci"},{"key":"B26","doi-asserted-by":"publisher","first-page":"1","DOI":"10.7554\/eLife.27438","article-title":"Point of view: Unbridle biomedical research from the laboratory cage","volume":"6","author":"Lahvis","year":"2017","journal-title":"Elife"},{"key":"B27","doi-asserted-by":"publisher","first-page":"386","DOI":"10.1016\/j.neuroscience.05037","article-title":"Natural-enriched environments lead to enhanced environmental engagement and altered neurobiological resilience","volume":"330","author":"Lambert","year":"2016","journal-title":"Neuroscience"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1038.\/mp.2017.244","article-title":"The dynamics of stress : a longitudinal MRI study of rat brain structure and connectome","author":"Magalh\u00e3es","year":"2017","journal-title":"Nat. Publ. Gr"},{"key":"B29","doi-asserted-by":"publisher","first-page":"116","DOI":"10.1111\/j.1365-2006,01515.x","article-title":"Social instability in adolescence alters the central and peripheral hypothalamic-pituitary-adrenal responses to a repeated homotypic stressor in male and female rats","volume":"19","author":"McCormick","year":"2007","journal-title":"J. Neuroendocrinol"},{"key":"B30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fpsyt.2015.00006","article-title":"An efficient chronic unpredictable stress protocol to induce stress-related responses in C57BL\/6 mice","volume":"6","author":"Monteiro","year":"2015","journal-title":"Front. Psychiatry"},{"key":"B31","doi-asserted-by":"publisher","first-page":"2160","DOI":"10.1038\/npp.2016.16","article-title":"Moderate stress-induced social bonding and oxytocin signaling are disrupted by predator odor in male rats","volume":"41","author":"Muroy","year":"2016","journal-title":"Neuropsychopharmacology"},{"key":"B32","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1016\/0031-9384(82)90331-6","article-title":"Short-term isolation increases social interactions of male rats: a parametric analysis","volume":"29","author":"Niesink","year":"1982","journal-title":"Physiol. Behav"},{"key":"B33","doi-asserted-by":"publisher","first-page":"1503","DOI":"10.1111\/j.1460-9568.2008.06112.x","article-title":"Dissociation of the morphological correlates of stress-induced anxiety and fear","volume":"27","author":"P\u00eago","year":"2008","journal-title":"Eur. J. Neurosci"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.3389.\/fnbeh.2022.1033999","article-title":"The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain","author":"Pellis","year":"2022","journal-title":"Front. Behav. Neurosci"},{"key":"B35","doi-asserted-by":"publisher","first-page":"44","DOI":"10.3390.\/ani7060044","article-title":"Long term physiologic and behavioural effects of housing density and environmental resource provision for adult male and female Sprague Dawley rats","volume":"7","author":"Pinelli","year":"2017","journal-title":"Animals"},{"key":"B36","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1016\/j.yhbeh.06002","article-title":"Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor","volume":"50","author":"Romeo","year":"2006","journal-title":"Horm. Behav."},{"key":"B37","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1258\/002367796780744875","article-title":"Behaviour of rats in their home cages: daytime variations and effects of routine husbandry procedures analysed by time sampling techniques","volume":"30","author":"Saibaba","year":"1996","journal-title":"Lab. Anim"},{"key":"B38","doi-asserted-by":"publisher","first-page":"474","DOI":"10.1080\/10253890.2020.1855421","article-title":"The same stress has divergent effects on social versus asocial manifestations of anxiety-like behavior over time","volume":"24","author":"Saxena","year":"2021","journal-title":"Stress"},{"key":"B39","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-017-03841-3","article-title":"Experimental evidence for reciprocity in allogrooming among wild-type Norway rats","volume":"7","author":"Schweinfurth","year":"2017","journal-title":"Sci. Rep"},{"key":"B40","doi-asserted-by":"publisher","first-page":"S9","DOI":"10.1017\/S0962728600014329","article-title":"The influences of standard laboratory cages on rodents and the validity of research data","volume":"13","author":"Sherwin","year":"2004","journal-title":"Anim. Welf"},{"key":"B41","doi-asserted-by":"publisher","first-page":"246","DOI":"10.1016\/j.bbr.04002","article-title":"(2011). The impact of environmental enrichment in laboratory rats-Behavioural and neurochemical aspects","volume":"222","author":"Simpson","year":"2011","journal-title":"Behav. Brain Res"},{"key":"B42","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.pbb.2020.172993","article-title":"Differential impact of stress and environmental enrichment on corticolimbic circuits","volume":"197","author":"Smail","year":"2020","journal-title":"Pharmacol. Biochem. Behav"},{"key":"B43","doi-asserted-by":"publisher","first-page":"237","DOI":"10.3109\/10253899809167288","article-title":"Maintenance of hippocampal cell numbers in young and aged rats submitted to chronic unpredictable stress. Comparison with the effects of corticosterone treatment","volume":"2","author":"Sousa","year":"1998","journal-title":"Stress"},{"key":"B44","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1152\/ajpendo.00070.2006","article-title":"Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner","volume":"291","author":"Ulrich-Lai","year":"2006","journal-title":"Am. J. Physiol. Endocrinol. Metab"},{"key":"B45","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/S0149-7634(96)00020-6","article-title":"The neurobiology of social play behavior in rats","volume":"21","author":"Vanderschuren","year":"1997","journal-title":"Neurosci. Biobehav. Rev"},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2019.146622","article-title":"Amygdalar corticotropin-releasing factor mediates stress-induced anxiety","author":"Ventura-Silva","year":"2020","journal-title":"Brain Res"},{"key":"B47","doi-asserted-by":"publisher","first-page":"620","DOI":"10.1016\/j.yhbeh.01004","article-title":"Pair-housing of male and female rats during chronic stress exposure results in gender-specific behavioral responses","volume":"47","author":"Westenbroek","year":"2005","journal-title":"Horm. Behav"},{"key":"B48","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1016\/0376-6357(94)90011-6","article-title":"Social and non-social open field behaviour of rats under light and noise stimulation","volume":"31","author":"Weyers","year":"1994","journal-title":"Behav. Processes"}],"container-title":["Frontiers in Behavioral Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnbeh.2023.1195011\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,6,9]],"date-time":"2023-06-09T04:31:15Z","timestamp":1686285075000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnbeh.2023.1195011\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,9]]},"references-count":48,"alternative-id":["10.3389\/fnbeh.2023.1195011"],"URL":"https:\/\/doi.org\/10.3389\/fnbeh.2023.1195011","relation":{},"ISSN":["1662-5153"],"issn-type":[{"value":"1662-5153","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,9]]},"article-number":"1195011"}}