{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T18:44:49Z","timestamp":1790707489648,"version":"4.1.0"},"reference-count":96,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,3,16]],"date-time":"2023-03-16T00:00:00Z","timestamp":1678924800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurosci."],"abstract":"<jats:p>Intrauterine growth restriction (IUGR) complicates up to 10% of human pregnancies and is the second leading cause of perinatal morbidity and mortality after prematurity. The most common etiology of IUGR in developed countries is uteroplacental insufficiency (UPI). For survivors of IUGR pregnancies, long-term studies consistently show a fivefold increased risk for impaired cognition including learning and memory deficits. Among these, only a few human studies have highlighted sex differences with males and females having differing susceptibilities to different impairments. Moreover, it is well established from brain magnetic resonance imaging that IUGR affects both white and gray matter. The hippocampus, composed of the dentate gyrus (DG) and cornu ammonis (CA) subregions, is an important gray matter structure critical to learning and memory, and is particularly vulnerable to the chronic hypoxic-ischemic effects of UPI. Decreased hippocampal volume is a strong predictor for learning and memory deficits. Decreased neuron number and attenuated dendritic and axonal morphologies in both the DG and CA are additionally seen in animal models. What is largely unexplored is the prenatal changes that predispose an IUGR offspring to postnatal learning and memory deficits. This lack of knowledge will continue to hinder the design of future therapy to improve learning and memory. In this review, we will first present the clinical susceptibilities and human epidemiology data regarding the neurological sequelae after IUGR. We will follow with data generated using our laboratory\u2019s mouse model of IUGR, that mimics the human IUGR phenotype, to dissect at the cellular and molecular alterations in embryonic hippocampal DG neurogenesis. We will lastly present a newer topic of postnatal neuron development, namely the critical period of synaptic plasticity that is crucial in achieving an excitatory\/inhibitory balance in the developing brain. To our knowledge, these findings are the first to describe the prenatal changes that lead to an alteration in postnatal hippocampal excitatory\/inhibitory imbalance, a mechanism that is now recognized to be a cause of neurocognitive\/neuropsychiatric disorders in at-risk individuals. Studies are ongoing in our laboratory to elucidate additional mechanisms that underlie IUGR-induced learning and memory impairment and to design therapy aimed at ameliorating such impairment.<\/jats:p>","DOI":"10.3389\/fnins.2023.1092357","type":"journal-article","created":{"date-parts":[[2023,3,16]],"date-time":"2023-03-16T05:40:05Z","timestamp":1678945205000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":12,"title":["Effects of intrauterine growth restriction on embryonic hippocampal dentate gyrus neurogenesis and postnatal critical period of synaptic plasticity that govern learning and memory function"],"prefix":"10.3389","volume":"17","author":[{"given":"Camille M.","family":"Fung","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,3,16]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"805","DOI":"10.1016\/j.biopsych.2014.08.001","article-title":"Syngap1 haploinsufficiency damages a postnatal critical period of pyramidal cell structural maturation linked to cortical circuit assembly.","volume":"77","author":"Aceti","year":"2015","journal-title":"Biol. Psychiatry"},{"key":"B2","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1016\/j.bbr.2013.07.005","article-title":"Hippocampal and subicular efferents and afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat.","volume":"254","author":"Agster","year":"2013","journal-title":"Behav. Brain Res."},{"key":"B3","doi-asserted-by":"publisher","first-page":"5783","DOI":"10.1523\/JENUROSCI.0324-17.2017","article-title":"Infantile amnesia: a critical period of learning to learn and remember","volume":"37","author":"Alberini","year":"2017","journal-title":"J. Neurosci"},{"key":"B4","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1002\/uog.9008","article-title":"Neurodevelopment following fetal growth restriction and its relationship with antepartum parameters of placental dysfunction.","volume":"37","author":"Baschat","year":"2011","journal-title":"Ultras. Obstet. Gynecol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1352","DOI":"10.1016\/j.neuroimage.2012.01.059","article-title":"Altered small-world topology of structural brain networks in infants with intrauterine growth restriction and its association with later neurodevelopmental outcome.","volume":"60","author":"Batalle","year":"2012","journal-title":"Neuroimage"},{"key":"B6","doi-asserted-by":"publisher","first-page":"14964","DOI":"10.1523\/JNEUROSCI.4812-10.2010","article-title":"Removing brakes on adult brain plasticity: From molecular to behaviorl interventions","volume":"30","author":"Bavelier","year":"2010","journal-title":"J. Neurosci"},{"key":"B7","doi-asserted-by":"publisher","first-page":"e521","DOI":"10.1016\/j.ajog.2014.10.1103","article-title":"Fetal growth restriction and risk of cerebral palsy in singletons born after at least 35 weeks\u2019 gestation.","volume":"212","author":"Blair","year":"2015","journal-title":"Am. J. Obstet. Gynecol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"ENEURO.62","DOI":"10.1523\/ENEURO.0062-21.2021","article-title":"Intrauterine growth restriction causes abnormal embryonic dentate gyrus neurogenesis in mouse offspring that leads to adult learning and memory deficits.","volume":"8","author":"Brown","year":"2021","journal-title":"eNeuro"},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.1002\/brb3.631","article-title":"Learning and memory disabilities in IUGR babies: functional and molecular analysis in a rat model.","volume":"7","author":"Camprubi Camprubi","year":"2017","journal-title":"Brain Behav."},{"key":"B10","doi-asserted-by":"publisher","first-page":"6312","DOI":"10.1523\/JNEUROSCI.0245-16.2016","article-title":"Perineuronal nets suppress plasticity of excitatory synapses on CA2 pyramidal neurons.","volume":"36","author":"Carstens","year":"2016","journal-title":"J Neurosci"},{"key":"B11","doi-asserted-by":"publisher","first-page":"344","DOI":"10.1159\/000494273","article-title":"Intrauterine growth restriction and hyperoxia as a cause of white matter injury.","volume":"40","author":"Chang","year":"2018","journal-title":"Dev. Neurosci."},{"key":"B12","doi-asserted-by":"publisher","first-page":"ENEURO.263","DOI":"10.1523\/ENEURO.0263-20.2021","article-title":"Intrauterine growth restriction followed by oxygen support uniquely interferes with genetic regulators of myelination.","volume":"8","author":"Chang","year":"2021","journal-title":"eNeuro"},{"key":"B13","doi-asserted-by":"publisher","first-page":"982","DOI":"10.1016\/j.ijcard.2015.11.109","article-title":"Metabolic syndrome in the non-pregnant state is associated with the development of preeclampsia.","volume":"203","author":"Cho","year":"2016","journal-title":"Int. J. Cardiol."},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.3389\/fcell.2022.821848","article-title":"Impaired cell cycle progression and self-renewal of fetal neural stem and progenitor cells in a murine model of intrauterine growth restriction.","volume":"10","author":"Chou","year":"2022","journal-title":"Front. Cell Dev. Biol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1002\/neu.10194","article-title":"Dendritic morphology is altered in hippocampal neurons following prenatal compromise.","volume":"55","author":"Dieni","year":"2003","journal-title":"J. Neurobiol."},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0177468","article-title":"Influence of catch up growth on spatial learning and memory in a mouse model of intrauterine growth restriction.","volume":"12","author":"Duran Fernandez-Feijoo","year":"2017","journal-title":"PLoS One"},{"key":"B17","doi-asserted-by":"publisher","first-page":"846","DOI":"10.1177\/0883073808331082","article-title":"Growth patterns in children with intrauterine growth retardation and their correlation to neurocognitive development.","volume":"24","author":"Fattal-Valevski","year":"2009","journal-title":"J. Child Neurol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"288","DOI":"10.1016\/j.ajog.2010.08.055","article-title":"Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management.","volume":"204","author":"Figueras","year":"2011","journal-title":"Am. J. Obstet. Gynecol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1159\/000357592","article-title":"Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol.","volume":"36","author":"Figueras","year":"2014","journal-title":"Fetal Diagn. Ther."},{"key":"B20","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1002\/uog.4084","article-title":"Doppler changes in the main fetal brain arteries at different stages of hemodynamic adaptation in severe intrauterine growth restriction.","volume":"30","author":"Figueroa-Diesel","year":"2007","journal-title":"Ultras. Obstet. Gynecol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"2793","DOI":"10.1093\/cercor\/bhu073","article-title":"Structural brain connectivity in school-age preterm infants provides evidence for impaired networks relevant for higher order cognitive skills and social cognition.","volume":"25","author":"Fischi-Gomez","year":"2015","journal-title":"Cereb. Cortex"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0146542","article-title":"Intrauterine growth restriction alters mouse intestinal architecture during development.","volume":"11","author":"Fung","year":"2016","journal-title":"PLoS One"},{"key":"B23","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1038\/pr.2015.70","article-title":"IUGR prevents IGF-1 upregulation in juvenile male mice by perturbing postnatal IGF-1 chromatin remodeling.","volume":"78","author":"Fung","year":"2015","journal-title":"Pediatr. Res."},{"key":"B24","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1016\/j.ogc.2021.02.004","article-title":"Short- and long-term implications of small for gestational age.","volume":"48","author":"Fung","year":"2021","journal-title":"Obstet. Gynecol. Clin. North Am."},{"key":"B25","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1017\/S2040174411000535","article-title":"Novel thromboxane A2 analog-induced IUGR mouse model.","volume":"2","author":"Fung","year":"2011","journal-title":"J. Dev. Origins Health Dis."},{"key":"B26","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1038\/pr.2012.32","article-title":"Uteroplacental insufficiency alters rat hippocampal cellular phenotype in conjunction with ErbB receptor expression.","volume":"72","author":"Fung","year":"2012","journal-title":"Pediatr. Res."},{"key":"B27","doi-asserted-by":"publisher","first-page":"S99","DOI":"10.1016\/S0301-2115(03)00179-9","article-title":"Placental insufficiency and its consequences.","volume":"110","author":"Gagnon","year":"2003","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1486","DOI":"10.1542\/peds.2005-2629","article-title":"The influence of head growth in fetal life, infancy, and childhood on intelligence at the ages of 4 and 8 years.","volume":"118","author":"Gale","year":"2006","journal-title":"Pediatrics"},{"key":"B29","doi-asserted-by":"publisher","first-page":"12531","DOI":"10.1073\/pnas.1810125115","article-title":"Arc\/Arg3.1 mediates a critical period for spatial learning and hippocampal networks.","volume":"115","author":"Gao","year":"2018","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B30","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1542\/peds.2005-2343","article-title":"Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study.","volume":"118","author":"Geva","year":"2006","journal-title":"Pediatrics"},{"key":"B31","doi-asserted-by":"publisher","first-page":"695","DOI":"10.1093\/biolre\/ioy006","article-title":"Effects of excess thromboxane A2 on placental development and nutrient transporters in a Mus musculus model of fetal growth restriction.","volume":"98","author":"Gibbins","year":"2018","journal-title":"Biol. Reprod."},{"key":"B32","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1016\/S2352-4642(18)30245-1","article-title":"Intrauterine growth restriction and development of the hippocampus: implications for learning and memory in children and adolescents.","volume":"2","author":"Gilchrist","year":"2018","journal-title":"Lancet Child Adolesc. Health"},{"key":"B33","doi-asserted-by":"publisher","first-page":"260","DOI":"10.1038\/6365","article-title":"Learning enhances adult neurogenesis in the hippocampal formation.","volume":"2","author":"Gould","year":"1999","journal-title":"Nat. Neurosci."},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pmed.1002710","article-title":"Metabolic syndrome in pregnancy and risk for adverse pregnancy outcomes: a prospective cohort of nulliparous women.","volume":"15","author":"Grieger","year":"2018","journal-title":"PLoS Med."},{"key":"B35","doi-asserted-by":"publisher","first-page":"2315","DOI":"10.1242\/dev.125.12.2315","article-title":"The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice.","volume":"125","author":"Grove","year":"1998","journal-title":"Development"},{"key":"B36","doi-asserted-by":"publisher","first-page":"e883","DOI":"10.1542\/peds.2010-2442","article-title":"Neurologic outcomes at school age in very preterm infants born with severe or mild growth restriction.","volume":"127","author":"Guellec","year":"2011","journal-title":"Pediatrics"},{"key":"B37","doi-asserted-by":"publisher","first-page":"549","DOI":"10.1146\/annurev.neuro.27.070203.144327","article-title":"Critical period regulation.","volume":"27","author":"Hensch","year":"2004","journal-title":"Annu. Rev. Neurosci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1038\/nrn1787","article-title":"Critical period plasticity in local cortical circuits.","volume":"6","author":"Hensch","year":"2005","journal-title":"Nat. Rev. Neurosci."},{"key":"B39","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1002\/pd.2913","article-title":"Can anomalies of fetal brain circulation be useful in the management of growth restricted fetuses?","volume":"32","author":"Hernandez-Andrade","year":"2012","journal-title":"Prenat. Diagn."},{"key":"B40","doi-asserted-by":"publisher","first-page":"6275","DOI":"10.1523\/JNEUROSCI.0532-12.2012","article-title":"Tbr2 is essential for hippocampal lineage progression from neural stem cells to intermediate progenitors and neurons.","volume":"32","author":"Hodge","year":"2012","journal-title":"J. Neurosci."},{"key":"B41","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1113\/jphysiol.1962.sp006837","article-title":"Receptive fields, binocular interaction and functional architecture in the cat\u2019s visual cortex.","volume":"160","author":"Hubel","year":"1962","journal-title":"J. Physiol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1106","DOI":"10.1016\/S0140-6736(03)14466-2","article-title":"Cerebral palsy and intrauterine growth in single births: European collaborative study.","volume":"362","author":"Jarvis","year":"2003","journal-title":"Lancet"},{"key":"B43","article-title":"Learning and memory","author":"Kandel","year":"2000","journal-title":"Principles of neural science"},{"key":"B44","first-page":"525","article-title":"Embryology of the human fetal hippocampus: MR imaging, anatomy, and histology.","volume":"18","author":"Kier","year":"1997","journal-title":"Am. J. Neuroradiol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1007\/978-1-4471-0735-4_13","article-title":"Diagnosis and management of IUGR","author":"Kingdom","year":"2000","journal-title":"Intrauterine growth restriction aetiology and management"},{"key":"B46","doi-asserted-by":"publisher","first-page":"1429","DOI":"10.1161\/HYPERTENSIONAHA.119.14140","article-title":"Maternal hypertensive pregnancy disorders and mental disorders in children.","volume":"75","author":"Lahti-Pulkkinen","year":"2020","journal-title":"Hypertension"},{"key":"B47","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1542\/peds.2014-1143","article-title":"Early childhood neurodevelopment after intrauterine growth restriction: a systematic review.","volume":"135","author":"Levine","year":"2015","journal-title":"Pediatrics"},{"key":"B48","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1038\/nrn3192","article-title":"Mechanisms of CaMKII action in long-term potentiation.","volume":"13","author":"Lisman","year":"2012","journal-title":"Nat. Rev. Neurosci."},{"key":"B49","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0020-7292(98)00101-5","article-title":"Thromboxane and prostacyclin in maternal and fetal circulation in pre-eclampsia.","volume":"63","author":"Liu","year":"1998","journal-title":"Int. J. Gynaecol. Obstet."},{"key":"B50","doi-asserted-by":"publisher","first-page":"438","DOI":"10.1203\/PDR.0b013e318165c005","article-title":"Intrauterine growth restriction affects the preterm infant\u2019s hippocampus.","volume":"63","author":"Lodygensky","year":"2008","journal-title":"Pediatr. Res."},{"key":"B51","doi-asserted-by":"publisher","first-page":"1357","DOI":"10.1126\/science.1220845","article-title":"A critical period for social experience-dependent oligodendrocyte maturation and myelination.","volume":"337","author":"Makinodan","year":"2012","journal-title":"Science"},{"key":"B52","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/S0306-4522(00)00271-2","article-title":"Reduced number of neurons in the hippocampus and the cerebellum in the postnatal guinea-pig following intrauterine growth-restriction.","volume":"100","author":"Mallard","year":"2000","journal-title":"Neuroscience"},{"key":"B53","doi-asserted-by":"publisher","first-page":"262","DOI":"10.1203\/00006450-199802000-00018","article-title":"Effects of chronic placental insufficiency on brain development in fetal sheep.","volume":"43","author":"Mallard","year":"1998","journal-title":"Pediatr. Res."},{"key":"B54","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/S0920-9964(99)00041-9","article-title":"Ventriculomegaly and reduced hippocampal volume following intrauterine growth-restriction: implications for the aetiology of schizophrenia.","volume":"40","author":"Mallard","year":"1999","journal-title":"Schizophr. Res."},{"key":"B55","first-page":"1","article-title":"Hypertensive disorders of pregnancy.","volume":"3","author":"Mammaro","year":"2009","journal-title":"J. Prenat. Med."},{"key":"B56","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1515\/JPM.2008.050","article-title":"Intrauterine restriction (IUGR).","volume":"36","author":"Mandruzzato","year":"2008","journal-title":"J. Perinat. Med."},{"key":"B57","doi-asserted-by":"publisher","DOI":"10.1016\/j.xagr.2021.100049","article-title":"Systematic review and meta-analysis of COVID maternal and neonatal clinical features and pregnancy outcomes to June 3rd 2021.","volume":"2","author":"Marchand","year":"2022","journal-title":"AJOG Glob. Rep."},{"key":"B58","doi-asserted-by":"publisher","first-page":"634","DOI":"10.1152\/physiolgenomics.00082.2015","article-title":"Intrauterine growth restriction perturbs nucleosome depletion at a growth hormone-responsive element in the mouse IGF-1 gene.","volume":"47","author":"McKnight","year":"2015","journal-title":"Physiol. Genomics"},{"key":"B59","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1530\/rep.0.1220195","article-title":"Fetal growth restriction: adaptations and consequences.","volume":"122","author":"McMillen","year":"2001","journal-title":"Reproduction"},{"key":"B60","doi-asserted-by":"publisher","first-page":"180","DOI":"10.1016\/j.neubiorev.2014.12.001","article-title":"Sensitive and critical periods during neurotypical and aberrant neurodevelopment: a framework for neurodevelopmental disorders.","volume":"50","author":"Meredith","year":"2015","journal-title":"Neurosci. Biobehav. Rev."},{"key":"B61","doi-asserted-by":"publisher","first-page":"807","DOI":"10.1113\/JP271402","article-title":"The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome.","volume":"594","author":"Miller","year":"2016","journal-title":"J. Physiol."},{"key":"B62","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1111\/jpi.12121","article-title":"Antenatal antioxidant treatment with melatonin to decrease newborn neurodevelopmental deficits and brain injury caused by fetal growth restriction.","volume":"56","author":"Miller","year":"2014","journal-title":"J. Pineal Res."},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.1098\/rsob.210042","article-title":"Development of the mammalian cortical hem and its derivatives: the choroid plexus, Cajal-Retzius cells and hippocampus.","volume":"11","author":"Moore","year":"2021","journal-title":"Open Biol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"e874","DOI":"10.1542\/peds.2010-1821","article-title":"Cognitive function after intrauterine growth restriction and very preterm birth.","volume":"127","author":"Morsing","year":"2011","journal-title":"Pediatrics"},{"key":"B65","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1515\/JPM.2008.042","article-title":"Head circumference and long-term outcome in small-for-gestational age infants.","volume":"36","author":"Ochiai","year":"2008","journal-title":"J. Perinat. Med."},{"key":"B66","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1016\/j.nbd.2007.01.001","article-title":"Moderate growth restriction: deleterious and protective effects on white matter damage.","volume":"26","author":"Olivier","year":"2007","journal-title":"Neurobiol. Dis."},{"key":"B67","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.brainres.2013.12.007","article-title":"Differential vulnerability of gray matter and white matter to intrauterine growth restriction in preterm infants at 12 months corrected age.","volume":"1545","author":"Padilla","year":"2014","journal-title":"Brain Res."},{"key":"B68","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1111\/j.1469-8749.1981.tb08445.x","article-title":"School achievement and behaviour of children who were small-for-dates at birth.","volume":"23","author":"Parkinson","year":"1981","journal-title":"Dev. Med. Child Neurol."},{"key":"B69","doi-asserted-by":"publisher","first-page":"R151","DOI":"10.1152\/ajpregu.00036.2014","article-title":"Impact of chronic hypoxemia on blood flow to the brain, heart, and adrenal gland in the late-gestation IUGR sheep fetus.","volume":"308","author":"Poudel","year":"2015","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"B70","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.neulet.2004.02.002","article-title":"Brain development during fetal life: influences of the intra-uterine environment.","volume":"361","author":"Rees","year":"2004","journal-title":"Neurosci. Lett."},{"key":"B71","first-page":"211","article-title":"Structure of the fetal sheep brain in experimental growth retardation.","volume":"10","author":"Rees","year":"1988","journal-title":"J. Dev. Physiol."},{"key":"B72","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1016\/j.dcn.2016.02.002","article-title":"Hippocampal functional connectivity and episodic memory in early childhood.","volume":"19","author":"Riggins","year":"2016","journal-title":"Dev. Cogn. Neurosci."},{"key":"B73","article-title":"Animal models of cognitive impairment","author":"Rodriguiz","year":"2006","journal-title":"Assessments of cognitive deficits in mutant mice"},{"key":"B74","doi-asserted-by":"publisher","first-page":"R279","DOI":"10.1016\/S0960-9822(00)00407-3","article-title":"Hippocampus formation: an intriguing collaboration.","volume":"10","author":"Roelink","year":"2000","journal-title":"Curr. Biol."},{"key":"B75","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1101\/gad.5.3.381","article-title":"Expression of two members of the Wnt family during mouse development\u2013restricted temporal and spatial patterns in the developing neural tube.","volume":"5","author":"Roelink","year":"1991","journal-title":"Genes Dev."},{"key":"B76","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1016\/j.ajog.2021.03.001","article-title":"Coronavirus disease 2019 infection and hypertensive disorders of pregnancy.","volume":"224","author":"Rosenbloom","year":"2021","journal-title":"Am. J. Obstet. Gynecol."},{"key":"B77","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1002\/uog.9597","article-title":"Evaluation of fetal cerebral blood flow perfusion using power Doppler ultrasound angiography (3D-PDA) in growth-restricted fetuses.","volume":"3","author":"Rossi","year":"2011","journal-title":"Facts Views Vis. Obgyn."},{"key":"B78","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1146\/annurev.psych.49.1.289","article-title":"The cognitive neuroscience of constructive memory.","volume":"49","author":"Schacter","year":"1998","journal-title":"Annu. Rev. Psychol."},{"key":"B79","doi-asserted-by":"publisher","first-page":"F108","DOI":"10.1136\/fn.86.2.F108","article-title":"Outcome at school age following antenatal detection of absent or reversed end diastolic flow velocity in the umbilical artery.","volume":"86","author":"Schreuder","year":"2002","journal-title":"Arch. Dis. Child. Fetal Neonatal Ed."},{"key":"B80","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1002\/cne.23460","article-title":"Distinctive population of Gfap-expressing neural progenitors arising around the dentate notch migrate and form the granule cell layer in the developing hippocampus.","volume":"522","author":"Seki","year":"2014","journal-title":"J. Comp. Neurol."},{"key":"B81","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1016\/j.bcp.2015.04.012","article-title":"Bioactive factors in uteroplacental and systemic circulation link placental ischemia to generalized vascular dysfunction in hypertensive pregnancy and preeclampsia.","volume":"95","author":"Shah","year":"2015","journal-title":"Biochem. Pharmacol."},{"key":"B82","doi-asserted-by":"publisher","first-page":"2083","DOI":"10.1242\/dev.020099","article-title":"Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth.","volume":"135","author":"Simmons","year":"2008","journal-title":"Development"},{"key":"B83","doi-asserted-by":"publisher","first-page":"B2","DOI":"10.1016\/j.ajog.2020.05.010","article-title":"Society for maternal-fetal medicine consult series #52: diagnosis and management of fetal growth restriction: (replaces clinical guideline number 3, April 2012).","volume":"223","author":"Martins","year":"2020","journal-title":"Am. J. Obstet. Gynecol."},{"key":"B84","doi-asserted-by":"publisher","first-page":"214","DOI":"10.1159\/000521611","article-title":"Intrauterine growth restriction disrupts the postnatal critical period of synaptic plasticity in the mouse dorsal hippocampus in a model of hypertensive disease of pregnancy.","volume":"44","author":"St Pierre","year":"2022","journal-title":"Dev. Neurosci."},{"key":"B85","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1001\/jama.283.5.625","article-title":"Adult functional outcome of those born small for gestational age: twenty-six-year follow-up of the 1970 British Birth Cohort.","volume":"283","author":"Strauss","year":"2000","journal-title":"JAMA"},{"key":"B86","doi-asserted-by":"publisher","first-page":"765","DOI":"10.1016\/j.earlhumdev.2012.04.004","article-title":"Birth weight- and fetal weight-growth restriction: impact on neurodevelopment.","volume":"88","author":"Streimish","year":"2012","journal-title":"Early Hum. Dev."},{"key":"B87","doi-asserted-by":"publisher","first-page":"823","DOI":"10.1001\/jamapsychiatry.2020.0306","article-title":"Association of preeclampsia in term births with neurodevelopmental disorders in offspring.","volume":"77","author":"Sun","year":"2020","journal-title":"JAMA Psychiatry"},{"key":"B88","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1016\/j.nlm.2016.08.005","article-title":"Developmental changes in plasticity, synaptic, glia and connectivity protein levels in rat dorsal hippocampus.","volume":"135","author":"Travaglia","year":"","journal-title":"Neurobiol. Learn. Mem."},{"key":"B89","doi-asserted-by":"publisher","first-page":"1225","DOI":"10.1038\/nn.4348","article-title":"Infantile amnesia reflects a developmental critical period for hippocampal learning.","volume":"19","author":"Travaglia","year":"","journal-title":"Nat. Neurosci."},{"key":"B90","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0046970","article-title":"Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals.","volume":"7","author":"Uematsu","year":"2012","journal-title":"PLoS One"},{"key":"B91","doi-asserted-by":"publisher","first-page":"e131","DOI":"10.1016\/j.ajog.2012.11.014","article-title":"Perinatal complications and long-term neurodevelopmental outcome of infants with intrauterine growth restriction.","volume":"208","author":"von Beckerath","year":"2013","journal-title":"Am. J. Obstet. Gynecol."},{"key":"B92","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1159\/000100545","article-title":"Animal models for small for gestational age and fetal programming of adult disease.","volume":"68","author":"Vuguin","year":"2007","journal-title":"Horm. Res."},{"key":"B93","doi-asserted-by":"publisher","first-page":"1003","DOI":"10.1152\/jn.1963.26.6.1003","article-title":"Single-cell responses in striate cortex of kittens deprived of vision in one eye.","volume":"26","author":"Wiesel","year":"1963","journal-title":"J Neurophysiol"},{"key":"B94","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.23798","article-title":"NPTX2 and cognitive dysfunction in Alzheimer\u2019s disease.","volume":"6","author":"Xiao","year":"2017","journal-title":"Elife"},{"key":"B95","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1016\/j.siny.2004.03.005","article-title":"Paediatric consequences of fetal growth restriction.","volume":"9","author":"Yanney","year":"2004","journal-title":"Semin. Fetal Neonatal Med."},{"key":"B96","doi-asserted-by":"publisher","first-page":"1119","DOI":"10.1016\/j.neuroscience.2006.07.007","article-title":"Neuronal production and precursor proliferation defects in the neocortex of mice with loss of function in the canonical Wnt signaling pathway.","volume":"142","author":"Zhou","year":"2006","journal-title":"Neuroscience"}],"container-title":["Frontiers in Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2023.1092357\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,17]],"date-time":"2023-03-17T14:35:07Z","timestamp":1679063707000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2023.1092357\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,16]]},"references-count":96,"alternative-id":["10.3389\/fnins.2023.1092357"],"URL":"https:\/\/doi.org\/10.3389\/fnins.2023.1092357","relation":{},"ISSN":["1662-453X"],"issn-type":[{"value":"1662-453X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,16]]},"article-number":"1092357"}}