{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2023,9,8]],"date-time":"2023-09-08T04:40:45Z","timestamp":1694148045893},"reference-count":39,"publisher":"Wiley","issue":"3","license":[{"start":{"date-parts":[[2009,6,12]],"date-time":"2009-06-12T00:00:00Z","timestamp":1244764800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Intl J of Devlp Neuroscience"],"published-print":{"date-parts":[[2010,5]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Fetal asphyxic insults in the brain are known to be associated with developmental and neurological problems like neuromotor disorders and cognitive deficits. Little is known, however, about the long\u2010term consequences of fetal asphyxia contributing to the development of different neurological diseases common in the adult or the aging brain. For that reason the present study aimed to investigate the long\u2010term effects of fetal asphyxia on synaptic organization within the adult rat brain. Fetal asphyxia was induced at embryonic day 17 by 75\u2010min clamping of the uterine and ovarian arteries. Presynaptic bouton densities and numbers were analyzed in the striatum and prefrontal cortex at the age of 19 months. A substantial decrease in presynaptic bouton density and number was observed in the striatum of fetal asphyxia rats compared to control rats, while an increase was found in the fifth layer of the prefrontal cortex. These results suggest that fetal asphyxia can have long\u2010lasting effects on synaptic organization that might contribute to a developmental etiology of different neurological disorders and aging.<\/jats:p>","DOI":"10.1016\/j.ijdevneu.2009.05.010","type":"journal-article","created":{"date-parts":[[2009,6,13]],"date-time":"2009-06-13T08:48:31Z","timestamp":1244882911000},"page":"277-281","update-policy":"http:\/\/dx.doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Fetal asphyxia leads to the loss of striatal presynaptic boutons in adult rats"],"prefix":"10.1002","volume":"28","author":[{"given":"E.","family":"Strackx","sequence":"first","affiliation":[{"name":"School of Mental Health and Neuroscience Faculty of Health, Medicine and Life Science Maastricht University European Graduate School of Neuroscience (EURON) Maastricht The Netherlands"},{"name":"Department of Child Neurology Maastricht University Medical Center Maastricht The Netherlands"},{"name":"Department of Pediatrics \u2010 Division of Neonatology Maastricht University Medical Center Maastricht The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"D.L.A.","family":"Van den Hove","sequence":"additional","affiliation":[{"name":"School of Mental Health and Neuroscience Faculty of Health, Medicine and Life Science Maastricht University European Graduate School of Neuroscience (EURON) Maastricht The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"H.P.","family":"Steinbusch","sequence":"additional","affiliation":[{"name":"School of Mental Health and Neuroscience Faculty of Health, Medicine and Life Science Maastricht University European Graduate School of Neuroscience (EURON) Maastricht The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"H.W.M.","family":"Steinbusch","sequence":"additional","affiliation":[{"name":"School of Mental Health and Neuroscience Faculty of Health, Medicine and Life Science Maastricht University European Graduate School of Neuroscience (EURON) Maastricht The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J.S.H.","family":"Vles","sequence":"additional","affiliation":[{"name":"Department of Child Neurology Maastricht University Medical Center Maastricht The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"C.E.","family":"Blanco","sequence":"additional","affiliation":[{"name":"Department of Pediatrics \u2010 Division of Neonatology Maastricht University Medical Center Maastricht The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"A.W.D.","family":"Gavilanes","sequence":"additional","affiliation":[{"name":"Department of Pediatrics \u2010 Division of Neonatology Maastricht University Medical Center Maastricht The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"311","published-online":{"date-parts":[[2009,6,12]]},"reference":[{"issue":"3","key":"e_1_2_7_2_1","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1002\/bdrc.20095","article-title":"Destruction and reconstruction: hypoxia and the developing brain","volume":"81","author":"Barrett R.D.","year":"2007","journal-title":"Birth Defects Res. C: Embryo Today"},{"issue":"5","key":"e_1_2_7_3_1","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1016\/j.neuro.2007.01.014","article-title":"Extrapolating brain development from experimental species to humans","volume":"28","author":"Clancy B.","year":"2007","journal-title":"Neurotoxicology"},{"issue":"1","key":"e_1_2_7_4_1","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/PL00005670","article-title":"Delayed neuronal death following perinatal asphyxia in rat","volume":"115","author":"Dell'Anna E.","year":"1997","journal-title":"Exp. Brain Res."},{"issue":"1","key":"e_1_2_7_5_1","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1016\/S0014-4886(03)00079-7","article-title":"Differential vulnerability of male versus female rats to long\u2010term effects of birth insult on brain catecholamine levels","volume":"182","author":"El\u2010Khodor B.F.","year":"2003","journal-title":"Exp. Neurol."},{"issue":"1","key":"e_1_2_7_6_1","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1590\/S0100-879X2007000100012","article-title":"Neuroprotective effect of ketamine\/xylazine on two rat models of Parkinson's disease","volume":"40","author":"Ferro M.M.","year":"2007","journal-title":"Braz. J. Med. Biol. Res."},{"issue":"1","key":"e_1_2_7_7_1","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/S0165-0173(02)00158-3","article-title":"Dendritic spine pathology: cause or consequence of neurological disorders?","volume":"39","author":"Fiala J.C.","year":"2002","journal-title":"Brain Res. Brain Res. Rev."},{"issue":"1","key":"e_1_2_7_8_1","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/j.expneurol.2006.07.024","article-title":"Induced cerebral hypothermia reduces post\u2010hypoxic loss of phenotypic striatal neurons in preterm fetal sheep","volume":"203","author":"George S.","year":"2007","journal-title":"Exp. Neurol."},{"key":"e_1_2_7_9_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2007.03.013"},{"issue":"6","key":"e_1_2_7_10_1","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1162\/neco.1996.8.6.1227","article-title":"Neuronal\u2010based synaptic compensation: a computational study in Alzheimer's disease","volume":"8","author":"Horn D.","year":"1996","journal-title":"Neural Comput."},{"issue":"12","key":"e_1_2_7_11_1","doi-asserted-by":"crossref","first-page":"3913","DOI":"10.1046\/j.1460-9568.1998.00435.x","article-title":"Hippocampal synaptic density and glutamate immunoreactivity following transient cerebral ischaemia in the chick","volume":"10","author":"Horner C.H.","year":"1998","journal-title":"Eur. J. Neurosci."},{"issue":"3","key":"e_1_2_7_12_1","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.bpobgyn.2004.02.002","article-title":"Reflections on the occurrence and significance of antepartum fetal asphyxia","volume":"18","author":"Low J.A.","year":"2004","journal-title":"Best Pract. Res. Clin. Obstet. Gynaecol."},{"issue":"3","key":"e_1_2_7_13_1","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1016\/0306-4522(94)00504-X","article-title":"Repeated asphyxia causes loss of striatal projection neurons in the fetal sheep brain","volume":"65","author":"Mallard E.C.","year":"1995","journal-title":"Neuroscience"},{"issue":"6","key":"e_1_2_7_14_1","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1203\/00006450-199506000-00006","article-title":"Repeated episodes of umbilical cord occlusion in fetal sheep lead to preferential damage to the striatum and sensitize the heart to further insults","volume":"37","author":"Mallard E.C.","year":"1995","journal-title":"Pediatr. Res."},{"issue":"5","key":"e_1_2_7_15_1","doi-asserted-by":"crossref","first-page":"F380","DOI":"10.1136\/adc.2004.067520","article-title":"Neuropsychological and educational problems at school age associated with neonatal encephalopathy","volume":"90","author":"Marlow N.","year":"2005","journal-title":"Arch. Dis. Child Fetal Neonatal Ed."},{"issue":"2","key":"e_1_2_7_16_1","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/j.brainresrev.2007.01.002","article-title":"The dorsal raphe nucleus\u2014from silver stainings to a role in depression","volume":"55","author":"Michelsen K.A.","year":"2007","journal-title":"Brain Res. Rev."},{"key":"e_1_2_7_17_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.283.5400.401"},{"issue":"3","key":"e_1_2_7_18_1","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1016\/S0168-0102(03)00100-7","article-title":"Neonatal hypoxia\u2010ischemia reduces ganglioside, phospholipid and cholesterol contents in the rat hippocampus","volume":"46","author":"Ramirez M.R.","year":"2003","journal-title":"Neurosci. Res."},{"issue":"5","key":"e_1_2_7_19_1","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1016\/j.siny.2007.07.006","article-title":"Outcome after intrapartum hypoxic ischaemia at term","volume":"12","author":"Rennie J.M.","year":"2007","journal-title":"Semin. Fetal Neonatal Med."},{"issue":"4","key":"e_1_2_7_20_1","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/S0168-0102(99)00060-7","article-title":"Anatomical re\u2010evaluation of the corticostriatal projections to the caudate nucleus: a retrograde labeling study in the cat","volume":"34","author":"Rosell A.","year":"1999","journal-title":"Neurosci. Res."},{"issue":"4","key":"e_1_2_7_21_1","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1515\/JBCPP.2005.16.4.231","article-title":"Single\u2010dose ketamine administration induces apoptosis in neonatal mouse brain","volume":"16","author":"Rudin M.","year":"2005","journal-title":"J. Basic Clin. Physiol. Pharmacol."},{"issue":"2","key":"e_1_2_7_22_1","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1016\/S0969-9961(02)00015-3","article-title":"No alterations of hippocampal neuronal number and synaptic bouton number in a transgenic mouse model expressing the beta\u2010cleaved C\u2010terminal APP fragment","volume":"12","author":"Rutten B.P.","year":"2003","journal-title":"Neurobiol. Dis."},{"issue":"1","key":"e_1_2_7_23_1","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/S0002-9440(10)62963-X","article-title":"Age\u2010related loss of synaptophysin immunoreactive presynaptic boutons within the hippocampus of APP751SL, PS1M146L, and APP751SL\/PS1M146L transgenic mice","volume":"167","author":"Rutten B.P.","year":"2005","journal-title":"Am. J. Pathol."},{"issue":"4","key":"e_1_2_7_24_1","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1016\/j.neuroscience.2004.08.050","article-title":"Design\u2010based stereology in neuroscience","volume":"130","author":"Schmitz C.","year":"2005","journal-title":"Neuroscience"},{"issue":"17","key":"e_1_2_7_25_1","doi-asserted-by":"crossref","first-page":"6587","DOI":"10.1523\/JNEUROSCI.20-17-06587.2000","article-title":"Circuit\u2010specific alterations in hippocampal synaptophysin immunoreactivity predict spatial learning impairment in aged rats","volume":"20","author":"Smith T.D.","year":"2000","journal-title":"J. Neurosci."},{"issue":"1","key":"e_1_2_7_26_1","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/S0300-9572(98)00103-8","article-title":"An ultrastructural study into the effect of global transient cerebral ischaemia on the synaptic population of the cerebellar cortex in rats","volume":"39","author":"Stepanov S.S.","year":"1998","journal-title":"Resuscitation"},{"issue":"2","key":"e_1_2_7_27_1","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1016\/j.expneurol.2008.02.006","article-title":"A combined behavioral and morphological study on the effects of fetal asphyxia on the nigrostriatal dopaminergic system in adult rats","volume":"211","author":"Strackx E.","year":"2008","journal-title":"Exp. Neurol."},{"issue":"5","key":"e_1_2_7_28_1","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1159\/000155218","article-title":"Fetal asphyxia leads to a decrease in dorsal raphe serotonergic neurons","volume":"30","author":"Strackx E.","year":"2008","journal-title":"Dev. Neurosci."},{"issue":"1","key":"e_1_2_7_29_1","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/0304-3940(92)90765-Y","article-title":"Increase in synaptophysin immunoreactivity following cortical infarction","volume":"147","author":"Stroemer R.P.","year":"1992","journal-title":"Neurosci. Lett."},{"issue":"1","key":"e_1_2_7_30_1","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/S0006-8993(98)01068-3","article-title":"Synaptic density of the prefrontal cortex regulated by dopamine instead of serotonin in rats","volume":"814","author":"Sugahara M.","year":"1998","journal-title":"Brain Res."},{"issue":"12","key":"e_1_2_7_31_1","doi-asserted-by":"crossref","first-page":"4095","DOI":"10.1523\/JNEUROSCI.07-12-04095.1987","article-title":"Differential laminar distribution of corticostriatal neurons in the prefrontal and pericruciate gyri of the dog","volume":"7","author":"Tanaka D.","year":"1987","journal-title":"J. Neurosci."},{"issue":"6","key":"e_1_2_7_32_1","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1016\/j.pneurobio.2005.09.005","article-title":"The functional role of the subthalamic nucleus in cognitive and limbic circuits","volume":"76","author":"Temel Y.","year":"2005","journal-title":"Prog. Neurobiol."},{"issue":"1","key":"e_1_2_7_33_1","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1093\/cercor\/13.1.5","article-title":"Interlaminar connections in the neocortex","volume":"13","author":"Thomson A.M.","year":"2003","journal-title":"Cereb. Cortex"},{"issue":"2","key":"e_1_2_7_34_1","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.devbrainres.2005.07.004","article-title":"Beneficial effects of melatonin on morphological changes in postnatal cerebellar tissue owing to epileptiform activity during pregnancy in rats: light and immunohistochemical study","volume":"159","author":"Uyanikgil Y.","year":"2005","journal-title":"Brain Res. Dev. Brain Res."},{"issue":"1","key":"e_1_2_7_35_1","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/S0891-0618(00)00078-8","article-title":"Perinatal asphyxia results in changes in presynaptic bouton number in striatum and cerebral cortex\u2010a stereological and behavioral analysis","volume":"20","author":"Van de Berg W.D.","year":"2000","journal-title":"J. Chem. Neuroanat."},{"issue":"1","key":"e_1_2_7_36_1","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1006\/exnr.2001.7855","article-title":"Perinatal asphyxia induced neuronal loss by apoptosis in the neonatal rat striatum: a combined TUNEL and stereological study","volume":"174","author":"Van de Berg W.D.","year":"2002","journal-title":"Exp. Neurol."},{"issue":"1","key":"e_1_2_7_37_1","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/S0306-4522(02)00787-X","article-title":"Impact of perinatal asphyxia on the GABAergic and locomotor system","volume":"117","author":"Van de Berg W.D.","year":"2003","journal-title":"Neuroscience"},{"issue":"2","key":"e_1_2_7_38_1","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0306-4522(97)00485-5","article-title":"Synaptic numbers across cortical laminae and cognitive performance of the rat during ageing","volume":"84","author":"Wong T.P.","year":"1998","journal-title":"Neuroscience"},{"issue":"2","key":"e_1_2_7_39_1","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1038\/sj.bjp.0706301","article-title":"Potential of ketamine and midazolam, individually or in combination, to induce apoptotic neurodegeneration in the infant mouse brain","volume":"146","author":"Young C.","year":"2005","journal-title":"Br. J. Pharmacol."},{"issue":"1","key":"e_1_2_7_40_1","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/S0006-8993(97)00502-7","article-title":"Effects of gender and estradiol treatment on focal brain ischemia","volume":"784","author":"Zhang Y.Q.","year":"1998","journal-title":"Brain Res."}],"container-title":["International Journal of Developmental Neuroscience"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0736574809000768?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0736574809000768?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1016%2Fj.ijdevneu.2009.05.010","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1016\/j.ijdevneu.2009.05.010","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1016\/j.ijdevneu.2009.05.010","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1016\/j.ijdevneu.2009.05.010","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,7]],"date-time":"2023-09-07T07:10:39Z","timestamp":1694070639000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1016\/j.ijdevneu.2009.05.010"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,6,12]]},"references-count":39,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2010,5]]}},"alternative-id":["10.1016\/j.ijdevneu.2009.05.010"],"URL":"https:\/\/doi.org\/10.1016\/j.ijdevneu.2009.05.010","archive":["Portico"],"relation":{},"ISSN":["0736-5748","1873-474X"],"issn-type":[{"value":"0736-5748","type":"print"},{"value":"1873-474X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,6,12]]},"assertion":[{"value":"2009-02-11","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2009-05-23","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2009-06-12","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}