{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,3,27]],"date-time":"2025-03-27T08:28:48Z","timestamp":1743064128327},"reference-count":47,"publisher":"Institute of Physiology of the Czech Academy of Sciences","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Physiol Res"],"abstract":"<jats:p>Hypoxia is one of the major pathological factors affecting brain function. The aim of the present study was to describe the effect of neonatal hypobaric hypoxia on the behavior of rats and to analyze its effect on hippocampal neurodegeneration. Hypobaric hypoxia at a simulated altitude of 9000 m was induced for one hour in neonatal rat pups (PND7 and PND9) of both sexes. Subsequently, the rats underwent behavioral testing on PND25 and PND35 using a LABORAS apparatus to assess spontaneous behavior. Hypoxia did not cause any morphological damage in the hippocampus of rats. However, hypoxia on PND7 led to less horizontal locomotor activity both in males (on PND25) and females (on PND35). Hypoxia on PND9 led to higher rearing in females on PND25. Hypoxic males exhibited higher grooming activity, while females lower grooming activity on PND35 following hypoxia induced on PND7. In females, hypoxia on PND9 resulted in higher grooming activity on PND25. Sex differences in the effect of hypoxia were observed on PND35, when hypoxic males compared to hypoxic females displayed more locomotor, rearing and grooming activity. Our data suggest that hypoxia on PND7 versus PND9 differently affects locomotion and grooming later in adolescence and these effects are sex-dependent.<\/jats:p>","DOI":"10.33549\/physiolres.934234","type":"journal-article","created":{"date-parts":[[2020,3,6]],"date-time":"2020-03-06T07:20:00Z","timestamp":1583479200000},"page":"165-179","source":"Crossref","is-referenced-by-count":10,"title":["Early Postnatal Hypoxia Induces Behavioral Deficits but not Morphological Damage in the Hippocampus in Adolescent Rats"],"prefix":"10.33549","author":[{"given":"V.","family":"RILJAK","sequence":"first","affiliation":[{"name":"Institute of Physiology, First Faculty of Medicine, Charles University, Prague, Czech Republic"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Z.","family":"LA\u0160T\u016eVKA","sequence":"additional","affiliation":[{"name":"Institute of Physiology, First Faculty of Medicine, Charles University, Prague, Czech Republic"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J.","family":"MYSLIVE\u010cEK","sequence":"additional","affiliation":[{"name":"Institute of Physiology, First Faculty of Medicine, Charles University, Prague, Czech Republic"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"V.","family":"BORB\u00c9LYOV\u00c1","sequence":"additional","affiliation":[{"name":"Institute of Molecular Biomedicine, Faculty of Medicine, Comenius University, Bratislava, Slovak Republic"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J.","family":"OT\u00c1HAL","sequence":"additional","affiliation":[{"name":"Laboratory of Developmental Epileptology, Institute of Physiology of the Czech Academy of Sciences, Prague, Czech Republic"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"19169","published-online":{"date-parts":[[2020,2,18]]},"reference":[{"key":"ref0","doi-asserted-by":"publisher","unstructured":"ARTENI NS, PEREIRA LO, RODRIGUES AL, LAVINSKY D, ACHAVAL ME, NETTO CA: Lateralized and sex-dependent behavioral and morphological effects of unilateral neonatal cerebral hypoxia-ischemia in the rat. Behav Brain Res 210: 92-98, 2010. https:\/\/doi.org\/10.1016\/j.bbr.2010.02.015","DOI":"10.1016\/j.bbr.2010.02.015"},{"key":"ref1","doi-asserted-by":"crossref","unstructured":"ARUMUGAM TV, BAIK SH, BALAGANAPATHY P, SOBEY CG, MATTSON MP, JO DG: Notch signaling and neuronal death in stroke. Prog Neurobiol 165-167: 103-116, 2018. https:\/\/doi.org\/10.1016\/j.pneurobio.2018.03.002","DOI":"10.1016\/j.pneurobio.2018.03.002"},{"key":"ref2","doi-asserted-by":"publisher","unstructured":"BERGER R, GARNIER Y, JENSEN A: Perinatal brain damage: underlying mechanisms and neuroprotective strategies. J Soc Gynecol Investig 9: 319-328, 2002. https:\/\/doi.org\/10.1177\/107155760200900601","DOI":"10.1177\/107155760200900601"},{"key":"ref3","doi-asserted-by":"publisher","unstructured":"BISWAL S, SHARMA D, KUMAR K, NAG TC, BARHWAL K, HOTA SK, KUMAR B: Global hypoxia induced impairment in learning and spatial memory is associated with precocious hippocampal aging. Neurobiol Learn Mem 133: 157-170, 2016. https:\/\/doi.org\/10.1016\/j.nlm.2016.05.011","DOI":"10.1016\/j.nlm.2016.05.011"},{"key":"ref4","doi-asserted-by":"publisher","unstructured":"BOGDANOVA OV, ABDULLAH O, KANEKAR S, BOGDANOV VB, PRESCOT AP, RENSHAW PF: Neurochemical alterations in frontal cortex of the rat after one week of hypobaric hypoxia. Behav Brain Res 263: 203-209, 2014. https:\/\/doi.org\/10.1016\/j.bbr.2014.01.027","DOI":"10.1016\/j.bbr.2014.01.027"},{"key":"ref5","doi-asserted-by":"publisher","unstructured":"BONA E, HAGBERG H, LOBERG EM, BAGENHOLM R, THORESEN M: Protective effects of moderate hypothermia after neonatal hypoxia-ischemia: short- and long-term outcome. Pediatr Res 43: 738-745, 1998. https:\/\/doi.org\/10.1203\/00006450-199806000-00005","DOI":"10.1203\/00006450-199806000-00005"},{"key":"ref6","doi-asserted-by":"publisher","unstructured":"CARTY ML, WIXEY JA, KESBY J, REINEBRANT HE, COLDITZ PB, GOBE G, BULLER KM: Long-term losses of amygdala corticotropin-releasing factor neurons are associated with behavioural outcomes following neonatal hypoxia-ischemia. Behav Brain Res 208: 609-618, 2010. https:\/\/doi.org\/10.1016\/j.bbr.2010.01.007","DOI":"10.1016\/j.bbr.2010.01.007"},{"key":"ref7","doi-asserted-by":"publisher","unstructured":"CLANCY B, DARLINGTON RB, FINLAY BL: Translating developmental time across mammalian species. Neuroscience 105: 7-17, 2001. https:\/\/doi.org\/10.1016\/S0306-4522(01)00171-3","DOI":"10.1016\/s0306-4522(01)00171-3"},{"key":"ref8","doi-asserted-by":"publisher","unstructured":"COSTELOE K, HENNESSY E, GIBSON AT, MARLOW N, WILKINSON AR: The EPICure study: outcomes to discharge from hospital for infants born at the threshold of viability. Pediatrics 106: 659-671, 2000. https:\/\/doi.org\/10.1542\/peds.106.4.659","DOI":"10.1542\/peds.106.4.659"},{"key":"ref9","doi-asserted-by":"publisher","unstructured":"CUAYCONG M, ENGEL M, WEINSTEIN SL, SALMON E, PERLMAN JM, SUNDERAM S, VANNUCCI SJ: A novel approach to the study of hypoxia-ischemia-induced clinical and subclinical seizures in the neonatal rat. Dev Neurosci 33: 241-250, 2011. https:\/\/doi.org\/10.1159\/000331646","DOI":"10.1159\/000331646"},{"key":"ref10","doi-asserted-by":"crossref","unstructured":"DOBLE A: The role of excitotoxicity in neurodegenerative disease: implications for therapy. Pharmacol Ther 81: 163-221, 1999. https:\/\/doi.org\/10.1016\/S0163-7258(98)00042-4","DOI":"10.1016\/S0163-7258(98)00042-4"},{"key":"ref11","doi-asserted-by":"publisher","unstructured":"DONDERS J, HOFFMAN NM: Gender differences in learning and memory after pediatric traumatic brain injury. Neuropsychology 16: 491-499, 2002. https:\/\/doi.org\/10.1037\/\/0894-4105.16.4.491","DOI":"10.1037\/0894-4105.16.4.491"},{"key":"ref12","doi-asserted-by":"publisher","unstructured":"ESTANISLAU C, DIAZ-MORAN S, CANETE T, BLAZQUEZ G, TOBENA A, FERNANDEZ-TERUEL A: Context-dependent differences in grooming behavior among the NIH heterogeneous stock and the Roman high- and low-avoidance rats. Neurosci Res 77: 187-201, 2013. https:\/\/doi.org\/10.1016\/j.neures.2013.09.012","DOI":"10.1016\/j.neures.2013.09.012"},{"key":"ref13","doi-asserted-by":"publisher","unstructured":"ESTANISLAU C, VELOSO AWN, FILGUEIRAS GB, MAIO TP, DAL-COL MLC, CUNHA DC, KLEIN R, CARMONA LF, FERNANDEZ-TERUEL A: Rat self-grooming and its relationships with anxiety, dearousal and perseveration: Evidence for a self-grooming trait. Physiol Behav 209: 112585, 2019. https:\/\/doi.org\/10.1016\/j.physbeh.2019.112585","DOI":"10.1016\/j.physbeh.2019.112585"},{"key":"ref14","doi-asserted-by":"publisher","unstructured":"GINET V, SPIEHLMANN A, RUMMEL C, RUDINSKIY N, GRISHCHUK Y, LUTHI-CARTER R, CLARKE PG, TRUTTMANN AC, PUYAL J: Involvement of autophagy in hypoxic-excitotoxic neuronal death. Autophagy 10: 846-860, 2014. https:\/\/doi.org\/10.4161\/auto.28264","DOI":"10.4161\/auto.28264"},{"key":"ref15","doi-asserted-by":"publisher","unstructured":"HILL CA, ALEXANDER ML, MCCULLOUGH LD, FITCH RH: Inhibition of X-linked inhibitor of apoptosis with embelin differentially affects male versus female behavioral outcome following neonatal hypoxia-ischemia in rats. Dev Neurosci 33: 494-504, 2011. https:\/\/doi.org\/10.1159\/000331651","DOI":"10.1159\/000331651"},{"key":"ref16","doi-asserted-by":"publisher","unstructured":"HILL CA, FITCH RH: Sex differences in mechanisms and outcome of neonatal hypoxia-ischemia in rodent models: implications for sex-specific neuroprotection in clinical neonatal practice. Neurol Res Int 2012: 867531, 2012. https:\/\/doi.org\/10.1155\/2012\/867531","DOI":"10.1155\/2012\/867531"},{"key":"ref17","doi-asserted-by":"publisher","unstructured":"HUANG HZ, WEN XH, LIU H: Sex differences in brain MRI abnormalities and neurodevelopmental outcomes in a rat model of neonatal hypoxia-ischemia. Int J Neurosci 126: 647-657, 2016. https:\/\/doi.org\/10.3109\/00207454.2015.1047016","DOI":"10.3109\/00207454.2015.1047016"},{"key":"ref18","doi-asserted-by":"publisher","unstructured":"CHEN PZ, HE WJ, ZHU ZR, E GJ, XU G, CHEN DW, GAO YQ: Adenosine A2A receptor involves in neuroinflammation-mediated cognitive decline through activating microglia under acute hypobaric hypoxia. Behav Brain Res 347: 99-107, 2018. https:\/\/doi.org\/10.1016\/j.bbr.2018.02.038","DOI":"10.1016\/j.bbr.2018.02.038"},{"key":"ref19","doi-asserted-by":"publisher","unstructured":"JAYALAKSHMI K, SINGH SB, KALPANA B, SAIRAM M, MUTHURAJU S, ILAVAZHAGAN G: N-acetyl cysteine supplementation prevents impairment of spatial working memory functions in rats following exposure to hypobaric hypoxia. Physiol Behav 92: 643-650, 2007. https:\/\/doi.org\/10.1016\/j.physbeh.2007.05.051","DOI":"10.1016\/j.physbeh.2007.05.051"},{"key":"ref20","doi-asserted-by":"publisher","unstructured":"LAN WC, PRIESTLEY M, MAYORAL SR, TIAN L, SHAMLOO M, PENN AA: Sex-specific cognitive deficits and regional brain volume loss in mice exposed to chronic, sublethal hypoxia. Pediatr Res 70: 15-20, 2011. https:\/\/doi.org\/10.1203\/PDR.0b013e31821b98a3","DOI":"10.1203\/pdr.0b013e31821b98a3"},{"key":"ref21","doi-asserted-by":"publisher","unstructured":"LAUTERBACH MD, RAZ S, SANDER CJ: Neonatal hypoxic risk in preterm birth infants: the influence of sex and severity of respiratory distress on cognitive recovery. Neuropsychology 15: 411-420, 2001. https:\/\/doi.org\/10.1037\/\/0894-4105.15.3.411","DOI":"10.1037\/0894-4105.15.3.411"},{"key":"ref22","doi-asserted-by":"publisher","unstructured":"MAYORAL SR, OMAR G, PENN AA: Sex differences in a hypoxia model of preterm brain damage. Pediatr Res 66: 248-253, 2009. https:\/\/doi.org\/10.1203\/PDR.0b013e3181b1bc34","DOI":"10.1203\/pdr.0b013e3181b1bc34"},{"key":"ref23","doi-asserted-by":"publisher","unstructured":"NEHLIG A, PEREIRA DE VASCONCELOS A: Glucose and ketone body utilization by the brain of neonatal rats. Prog Neurobiol 40: 163-221, 1993. https:\/\/doi.org\/10.1016\/0301-0082(93)90022-K","DOI":"10.1016\/0301-0082(93)90022-k"},{"key":"ref24","doi-asserted-by":"publisher","unstructured":"NETTO CA, SANCHES E, ODORCYK FK, DURAN-CARABALI LE, WEIS SN: Sex-dependent consequences of neonatal brain hypoxia-ischemia in the rat. J Neurosci Res 95: 409-421, 2017. https:\/\/doi.org\/10.1002\/jnr.23828","DOI":"10.1002\/jnr.23828"},{"key":"ref25","doi-asserted-by":"crossref","unstructured":"NYAKAS C, BUWALDA B, LUITEN PG: Hypoxia and brain development. Prog Neurobiol 49: 1-51, 1996. https:\/\/doi.org\/10.1016\/0301-0082(96)00007-X","DOI":"10.1016\/0301-0082(96)00007-X"},{"key":"ref26","doi-asserted-by":"publisher","unstructured":"PAPPAS A, SHANKARAN S, MCDONALD SA, VOHR BR, HINTZ SR, EHRENKRANZ RA, TYSON JE, YOLTON K, DAS A, BARA R, HAMMOND J, HIGGINS RD: Cognitive outcomes after neonatal encephalopathy. Pediatrics 135: e624-e634, 2015. https:\/\/doi.org\/10.1542\/peds.2014-1566","DOI":"10.1542\/peds.2014-1566"},{"key":"ref27","doi-asserted-by":"publisher","unstructured":"PETERSON BL, WON S, GEDDES RI, SAYEED I, STEIN DG: Sex-related differences in effects of progesterone following neonatal hypoxic brain injury. Behav Brain Res 286: 152-165, 2015. https:\/\/doi.org\/10.1016\/j.bbr.2015.03.005","DOI":"10.1016\/j.bbr.2015.03.005"},{"key":"ref28","doi-asserted-by":"publisher","unstructured":"POTTER M, ROSENKRANTZ T, FITCH RH: Behavioral and neuroanatomical outcomes in a rat model of preterm hypoxic-ischemic brain injury: Effects of caffeine and hypothermia. Int J Dev Neurosci 70: 46-55, 2018. https:\/\/doi.org\/10.1016\/j.ijdevneu.2018.02.001","DOI":"10.1016\/j.ijdevneu.2018.02.001"},{"key":"ref29","doi-asserted-by":"publisher","unstructured":"RAZ S, LAUTERBACH MD, HOPKINS TL, GLOGOWSKI BK, PORTER CL, RIGGS WW, SANDER CJ: A female advantage in cognitive recovery from early cerebral insult. Dev Psychol 31: 958, 1995. https:\/\/doi.org\/10.1037\/0012-1649.31.6.958","DOI":"10.1037\/0012-1649.31.6.958"},{"key":"ref30","doi-asserted-by":"crossref","unstructured":"RILJAK V, KRAF J, DARYANANI A, JIRUSKA P, OTAHAL J: Pathophysiology of perinatal hypoxic-ischemic encephalopathy - biomarkers, animal models and treatment perspectives. Physiol Res 65: S533-S545, 2016.","DOI":"10.33549\/physiolres.933541"},{"key":"ref31","unstructured":"RILJAK V, MARESOVA D, POKORNY J: Nicotine effects on rat seizures susceptibility and hippocampal neuronal degeneration. Neuro Endocrinol Lett 31: 792-795, 2010."},{"key":"ref32","doi-asserted-by":"crossref","unstructured":"RILJAK V, MILOTOVA M, JANDOVA K, POKORNY J, LANGMEIER M: Morphological changes in the hippocampus following nicotine and kainic acid administration. Physiol Res 56: 641-649, 2007.","DOI":"10.33549\/physiolres.931048"},{"key":"ref33","doi-asserted-by":"publisher","unstructured":"ROMIJN HJ, HOFMAN MA, GRAMSBERGEN A: At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Hum Dev 26: 61-67, 1991. https:\/\/doi.org\/10.1016\/0378-3782(91)90044-4","DOI":"10.1016\/0378-3782(91)90044-4"},{"key":"ref34","doi-asserted-by":"publisher","unstructured":"SANCHES EF, ARTENI N, NICOLA F, ARISTIMUNHA D, NETTO CA: Sexual dimorphism and brain lateralization impact behavioral and histological outcomes following hypoxia-ischemia in P3 and P7 rats. Neuroscience 290: 581-593, 2015. https:\/\/doi.org\/10.1016\/j.neuroscience.2014.12.074","DOI":"10.1016\/j.neuroscience.2014.12.074"},{"key":"ref35","doi-asserted-by":"publisher","unstructured":"SARNAT HB, SARNAT MS: Neonatal encephalopathy following fetal distress. A clinical and electroencephalographic study. Arch Neurol 33: 696-705, 1976. https:\/\/doi.org\/10.1001\/archneur.1976.00500100030012","DOI":"10.1001\/archneur.1976.00500100030012"},{"key":"ref36","doi-asserted-by":"publisher","unstructured":"SEMPLE BD, BLOMGREN K, GIMLIN K, FERRIERO DM, NOBLE-HAEUSSLEIN LJ: Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species. Prog Neurobiol 106-107: 1-16, 2013. https:\/\/doi.org\/10.1016\/j.pneurobio.2013.04.001","DOI":"10.1016\/j.pneurobio.2013.04.001"},{"key":"ref37","doi-asserted-by":"publisher","unstructured":"SHEN Y, LIU XB, PLEASURE DE, DENG W: Axon-glia synapses are highly vulnerable to white matter injury in the developing brain. J Neurosci Res 90: 105-121, 2012. https:\/\/doi.org\/10.1002\/jnr.22722","DOI":"10.1002\/jnr.22722"},{"key":"ref38","doi-asserted-by":"publisher","unstructured":"TOWFIGHI J, MAUGER D, VANNUCCI RC, VANNUCCI SJ: Influence of age on the cerebral lesions in an immature rat model of cerebral hypoxia-ischemia: a light microscopic study. Brain Res Dev Brain Res 100: 149-160, 1997. https:\/\/doi.org\/10.1016\/S0165-3806(97)00036-9","DOI":"10.1016\/s0165-3806(97)00036-9"},{"key":"ref39","doi-asserted-by":"publisher","unstructured":"VAN DE WEERD HA, BULTHUIS RJ, BERGMAN AF, SCHLINGMANN F, TOLBOOM J, VAN LOO PL, REMIE R, BAUMANS V, VAN ZUTPHEN LF: Validation of a new system for the automatic registration of behaviour in mice and rats. Behav Processes 53: 11-20, 2001. https:\/\/doi.org\/10.1016\/S0376-6357(00)00135-2","DOI":"10.1016\/s0376-6357(00)00135-2"},{"key":"ref40","doi-asserted-by":"publisher","unstructured":"VANNUCCI RC: Experimental biology of cerebral hypoxia-ischemia: relation to perinatal brain damage. Pediatr Res 27: 317-326, 1990. https:\/\/doi.org\/10.1203\/00006450-199004000-00001","DOI":"10.1203\/00006450-199004000-00001"},{"key":"ref41","doi-asserted-by":"publisher","unstructured":"VIRUES-ORTEGA J, BUELA-CASAL G, GARRIDO E, ALCAZAR B: Neuropsychological functioning associated with high-altitude exposure. Neuropsychol Rev 14: 197-224, 2004. https:\/\/doi.org\/10.1007\/s11065-004-8159-4","DOI":"10.1007\/s11065-004-8159-4"},{"key":"ref42","doi-asserted-by":"publisher","unstructured":"VOLPE JJ: Perinatal brain injury: from pathogenesis to neuroprotection. Ment Retard Dev Disabil Res Rev 7: 56-64, 2001. https:\/\/doi.org\/10.1002\/1098-2779(200102)7:1<56::AID-MRDD1008>3.0.CO;2-A","DOI":"10.1002\/1098-2779(200102)7:1<56::aid-mrdd1008>3.0.co;2-a"},{"key":"ref43","doi-asserted-by":"publisher","unstructured":"ZAYACHKIVSKY A, LEHMKUHLE MJ, EKSTRAND JJ, DUDEK FE: Ischemic injury suppresses hypoxia-induced electrographic seizures and the background EEG in a rat model of perinatal hypoxic-ischemic encephalopathy. J Neurophysiol 114: 2753-2763, 2015. https:\/\/doi.org\/10.1152\/jn.00796.2014","DOI":"10.1152\/jn.00796.2014"},{"key":"ref44","doi-asserted-by":"publisher","unstructured":"ZHANG XY, ZHANG XJ, XV J, JIA W, PU XY, WANG HY, LIANG H, ZHUOMA L, LU DX: Crocin attenuates acute hypobaric hypoxia-induced cognitive deficits of rats. Eur J Pharmacol 818: 300-305, 2018. https:\/\/doi.org\/10.1016\/j.ejphar.2017.10.042","DOI":"10.1016\/j.ejphar.2017.10.042"},{"key":"ref45","doi-asserted-by":"publisher","unstructured":"ZHU C, WANG X, XU F, BAHR BA, SHIBATA M, UCHIYAMA Y, HAGBERG H, BLOMGREN K: The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 12: 162-176, 2005. https:\/\/doi.org\/10.1038\/sj.cdd.4401545","DOI":"10.1038\/sj.cdd.4401545"},{"key":"ref46","doi-asserted-by":"publisher","unstructured":"ZHURAVIN IA, DUBROVSKAYA NM, VASILEV DS, POSTNIKOVA TY, ZAITSEV AV: Prenatal hypoxia produces memory deficits associated with impairment of long-term synaptic plasticity in young rats. Neurobiol Learn Mem 164: 107066, 2019. https:\/\/doi.org\/10.1016\/j.nlm.2019.107066","DOI":"10.1016\/j.nlm.2019.107066"}],"container-title":["Physiological Research"],"original-title":[],"language":"en","deposited":{"date-parts":[[2022,10,17]],"date-time":"2022-10-17T20:23:58Z","timestamp":1666038238000},"score":1,"resource":{"primary":{"URL":"http:\/\/www.biomed.cas.cz\/physiolres\/pdf\/2020\/69_165.pdf"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,18]]},"references-count":47,"URL":"https:\/\/doi.org\/10.33549\/physiolres.934234","relation":{},"ISSN":["1802-9973","0862-8408"],"issn-type":[{"value":"1802-9973","type":"electronic"},{"value":"0862-8408","type":"print"}],"subject":[],"published":{"date-parts":[[2020,2,18]]}}}