{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T08:43:34Z","timestamp":1790844214596,"version":"4.1.0"},"reference-count":140,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,2,4]],"date-time":"2021-02-04T00:00:00Z","timestamp":1612396800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Pediatr."],"abstract":"<jats:p>Preterm birth is associated with poor long-term neurodevelopmental and behavioral outcomes, even in the absence of obvious brain injury at the time of birth. In particular, behavioral disorders characterized by inattention, social difficulties and anxiety are common among children and adolescents who were born moderately to late preterm (32\u201337 weeks' gestation). Diffuse deficits in white matter microstructure are thought to play a role in these poor outcomes with evidence suggesting that a failure of oligodendrocytes to mature and myelinate axons is responsible. However, there remains a major knowledge gap over the mechanisms by which preterm birth interrupts normal oligodendrocyte development. <jats:italic>In utero<\/jats:italic> neurodevelopment occurs in an inhibitory-dominant environment due to the action of placentally derived neurosteroids on the GABA<jats:sub>A<\/jats:sub> receptor, thus promoting GABAergic inhibitory activity and maintaining the fetal behavioral state. Following preterm birth, and the subsequent premature exposure to the <jats:italic>ex utero<\/jats:italic> environment, this action of neurosteroids on GABA<jats:sub>A<\/jats:sub> receptors is greatly reduced. Coinciding with a reduction in GABAergic inhibition, the preterm neonatal brain is also exposed to <jats:italic>ex utero<\/jats:italic> environmental insults such as periods of hypoxia and excessive glucocorticoid concentrations. Together, these insults may increase levels of the excitatory neurotransmitter glutamate in the developing brain and result in a shift in the balance of inhibitory: excitatory activity toward excitatory. This review will outline the normal development of oligodendrocytes, how it is disrupted under excitation-dominated conditions and highlight how shifting the balance back toward an inhibitory-dominated environment may improve outcomes.<\/jats:p>","DOI":"10.3389\/fped.2021.618052","type":"journal-article","created":{"date-parts":[[2021,2,4]],"date-time":"2021-02-04T05:09:21Z","timestamp":1612415361000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":25,"title":["Impaired Oligodendrocyte Development Following Preterm Birth: Promoting GABAergic Action to Improve Outcomes"],"prefix":"10.3389","volume":"9","author":[{"given":"Julia C.","family":"Shaw","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabrielle K.","family":"Crombie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hannah K.","family":"Palliser","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan J.","family":"Hirst","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,2,4]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"741","DOI":"10.1542\/peds.2013-1131","article-title":"Late preterm infants: near term but still in a critical developmental time period","volume":"132","author":"Kugelman","year":"2013","journal-title":"Pediatrics."},{"key":"B2","doi-asserted-by":"publisher","first-page":"570743","DOI":"10.1155\/2013\/570743","article-title":"Mental health outcomes in us children and adolescents born prematurely or with low birthweight","volume":"2013","author":"Singh","year":"2013","journal-title":"Depress Res Treat."},{"key":"B3","doi-asserted-by":"publisher","first-page":"784","DOI":"10.1111\/j.1440-1754.2012.02536.x","article-title":"Increasing rates of prematurity and epidemiology of late preterm birth","volume":"48","author":"Cheong","year":"2012","journal-title":"J Paediatr Child Health."},{"key":"B4","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1016\/j.jpeds.2008.01.027","article-title":"School outcomes of late preterm infants: Special needs and challenges for infants born at 32 to 36 weeks gestation","volume":"153","author":"Chyi","year":"2008","journal-title":"J Pediatr."},{"key":"B5","doi-asserted-by":"publisher","first-page":"262","DOI":"10.1056\/NEJMoa0706475","article-title":"Long-term medical and social consequences of preterm birth","volume":"359","author":"Moster","year":"2008","journal-title":"N Engl J Med."},{"key":"B6","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/j.earlhumdev.2011.01.023","article-title":"Behavior problems of 9-16 year old preterm children: biological, sociodemographic, and intellectual contributions","volume":"87","author":"Loe","year":"2011","journal-title":"Early Hum Dev."},{"key":"B7","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1136\/adc.2011.300131","article-title":"Higher rates of behavioural and emotional problems at preschool age in children born moderately preterm","volume":"97","author":"Potijk","year":"2012","journal-title":"Arch Dis Child."},{"key":"B8","doi-asserted-by":"publisher","first-page":"438","DOI":"10.1007\/s11065-012-9210-5","article-title":"Late preterm birth: a review of medical and neuropsychological childhood outcomes","volume":"22","author":"Baron","year":"2012","journal-title":"Neuropsychol Rev."},{"key":"B9","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1016\/j.jpeds.2008.08.020","article-title":"Increased risk of adverse neurological development for late preterm infants","volume":"154","author":"Petrini","year":"2009","journal-title":"J Pediatrics."},{"key":"B10","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1007\/s11910-018-0862-2","article-title":"Neurologic consequences of preterm birth","volume":"18","author":"Ream","year":"2018","journal-title":"Curr Neurol Neurosci Rep."},{"key":"B11","doi-asserted-by":"publisher","first-page":"31","DOI":"10.2471\/BLT.08.062554","article-title":"The worldwide incidence of preterm birth: a systematic review of maternal mortality and morbidity","volume":"88","author":"Beck","year":"2010","journal-title":"Bull World Health Organ."},{"key":"B12","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.earlhumdev.2016.02.006","article-title":"Neurobehaviour and neurological development in the first month after birth for infants born between 32-42 weeks' gestation","volume":"96","author":"Spittle","year":"2016","journal-title":"Early Hum Dev."},{"key":"B13","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1038\/pr.2016.82","article-title":"Altered brain function, structure, and developmental trajectory in children born late preterm","volume":"80","author":"Brumbaugh","year":"2016","journal-title":"Pediatr Res."},{"key":"B14","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1016\/j.jsbmb.2013.04.002","article-title":"Neuroactive steroids in pregnancy: key regulatory and protective roles in the foetal brain","volume":"139","author":"Hirst","year":"2014","journal-title":"J Steroid Biochem Mol Biol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/S0733-8619(18)30060-4","article-title":"Oligodendrocytes and myelin","volume":"13","author":"McLaurin","year":"1995","journal-title":"Neurol Clin."},{"key":"B16","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1002\/glia.23256","article-title":"Origin and dynamics of oligodendrocytes in the developing brain: implications for perinatal white matter injury","volume":"66","author":"van Tilborg","year":"2018","journal-title":"Glia."},{"key":"B17","doi-asserted-by":"publisher","first-page":"779","DOI":"10.1126\/science.1190927","article-title":"Regulation of oligodendrocyte differentiation and myelination","volume":"330","author":"Emery","year":"2010","journal-title":"Science"},{"key":"B18","doi-asserted-by":"publisher","first-page":"4355","DOI":"10.1007\/s00018-013-1365-6","article-title":"Regulation of oligodendrocyte precursor migration during development, in adulthood and in pathology","volume":"70","author":"de Castro","year":"2013","journal-title":"Cell Mol Life Sci."},{"key":"B19","doi-asserted-by":"publisher","first-page":"869","DOI":"10.1016\/S0896-6273(00)80469-9","article-title":"Oligodendrocyte population dynamics and the role of PDGF in vivo","volume":"20","author":"Calver","year":"1998","journal-title":"Neuron"},{"key":"B20","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1016\/j.neuron.2010.01.027","article-title":"Dicer1 and miR-219 are required for normal oligodendrocyte differentiation and myelination","volume":"65","author":"Dugas","year":"2010","journal-title":"Neuron."},{"key":"B21","doi-asserted-by":"publisher","first-page":"612","DOI":"10.1016\/j.neuron.2010.02.018","article-title":"MicroRNA-mediated control of oligodendrocyte differentiation","volume":"65","author":"Zhao","year":"2010","journal-title":"Neuron."},{"key":"B22","doi-asserted-by":"publisher","first-page":"e1001625","DOI":"10.1371\/journal.pbio.1001625","article-title":"MYRF is a membrane-associated transcription factor that autoproteolytically cleaves to directly activate myelin genes","volume":"11","author":"Bujalka","year":"2013","journal-title":"PLoS Biol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1016\/j.conb.2017.09.016","article-title":"Oligodendroglia-lineage cells in brain plasticity, homeostasis and psychiatric disorders","volume":"47","author":"Birey","year":"2017","journal-title":"Curr Opin Neurobiol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1369\/0022155413517700","article-title":"Distribution of corticosteroid receptors in mature oligodendrocytes and oligodendrocyte progenitors of the adult mouse brain","volume":"62","author":"Matsusue","year":"2014","journal-title":"J Histochem Cytochem."},{"key":"B25","doi-asserted-by":"publisher","first-page":"256","DOI":"10.3389\/fncel.2020.00256","article-title":"Expression and function of GABA receptors in myelinating cells","volume":"14","author":"Serrano-Regal","year":"2020","journal-title":"Front Cell Neurosci."},{"key":"B26","doi-asserted-by":"publisher","first-page":"674","DOI":"10.1038\/nn.3990","article-title":"GABAergic regulation of cerebellar NG2 cell development is altered in perinatal white matter injury","volume":"18","author":"Zonouzi","year":"2015","journal-title":"Nat Neurosci."},{"key":"B27","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1016\/j.neuroscience.2019.07.014","article-title":"Oligodendrocyte differentiation and myelination is potentiated via GABAB receptor activation","volume":"439","author":"Serrano-Regal","year":"","journal-title":"Neuroscience."},{"key":"B28","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1016\/j.devcel.2015.05.013","article-title":"Actin filament turnover drives leading edge growth during myelin sheath formation in the central nervous system","volume":"34","author":"Nawaz","year":"2015","journal-title":"Dev Cell."},{"key":"B29","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/j.pneurobio.2017.03.009","article-title":"Blocked, delayed, or obstructed: what causes poor white matter development in intrauterine growth restricted infants?","volume":"154","author":"Tolcos","year":"2017","journal-title":"Prog Neurobiol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.expneurol.2011.08.002","article-title":"Intrauterine growth restriction affects the maturation of myelin","volume":"232","author":"Tolcos","year":"2011","journal-title":"Exp Neurol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"350","DOI":"10.1017\/S2040174415001075","article-title":"Effect of postnatal progesterone therapy following preterm birth on neurosteroid concentrations and cerebellar myelination in guinea pigs","volume":"6","author":"Palliser","year":"2015","journal-title":"J Dev Orig Health Dis."},{"key":"B32","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1677\/JOE-10-0248","article-title":"Sex-dependent effect of a low neurosteroid environment and intrauterine growth restriction on foetal guinea pig brain development","volume":"208","author":"Kelleher","year":"2011","journal-title":"J Endocrinol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"1365","DOI":"10.1177\/1933719113485295","article-title":"Changes in neuroactive steroid concentrations after preterm delivery in the Guinea pig","volume":"20","author":"Kelleher","year":"2013","journal-title":"Reprod Sci."},{"key":"B34","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1038\/pr.2016.63","article-title":"Long-term effects of preterm birth on behavior and neurosteroid sensitivity in the guinea pig","volume":"80","author":"Shaw","year":"2016","journal-title":"Pediatr Res."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1088","DOI":"10.1038\/nn1319","article-title":"Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination","volume":"7","author":"Antony","year":"2004","journal-title":"Nat Neurosci."},{"key":"B36","doi-asserted-by":"crossref","DOI":"10.1016\/B978-008045046-9.00125-X","article-title":"Astrocytes and oligodendrocytes during normal brain ageing","volume-title":"Encyclopedia of Neuroscience","author":"Blasko","year":"2009"},{"key":"B37","doi-asserted-by":"publisher","first-page":"753","DOI":"10.1016\/j.earlhumdev.2005.07.004","article-title":"Fetal and neonatal origins of altered brain development","volume":"81","author":"Rees","year":"2005","journal-title":"Early Hum Dev."},{"key":"B38","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1111\/apa.12445","article-title":"White matter microstructure is influenced by extremely preterm birth and neonatal respiratory factors","volume":"103","author":"Alexandrou","year":"2014","journal-title":"Acta Paediatr."},{"key":"B39","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1007\/s00401-017-1718-6","article-title":"White matter injury in the preterm infant: pathology and mechanisms","volume":"134","author":"Back","year":"2017","journal-title":"Acta Neuropathol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1111\/j.1750-3639.2007.00107.x","article-title":"Myelin abnormalities without oligodendrocyte loss in periventricular leukomalacia","volume":"18","author":"Billiards","year":"2008","journal-title":"Brain Pathol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1016\/j.neuroimage.2017.02.026","article-title":"White matter alterations to cingulum and fornix following very preterm birth and their relationship with cognitive functions","volume":"150","author":"Caldinelli","year":"2017","journal-title":"Neuroimage."},{"key":"B42","doi-asserted-by":"publisher","first-page":"505","DOI":"10.1007\/s00234-010-0700-y","article-title":"Magnetic resonance imaging of white matter diseases of prematurity","volume":"52","author":"Rutherford","year":"2010","journal-title":"Neuroradiology."},{"key":"B43","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1542\/peds.112.1.176","article-title":"Cerebral white matter injury of the premature infant-more common than you think","volume":"112","author":"Volpe","year":"2003","journal-title":"Pediatrics."},{"key":"B44","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1002\/ana.22627","article-title":"Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants","volume":"71","author":"Buser","year":"2012","journal-title":"Ann Neurol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"396","DOI":"10.3171\/ped.2006.104.6.396","article-title":"Neonatal loss of gamma-aminobutyric acid pathway expression after human perinatal brain injury","volume":"104","author":"Robinson","year":"2006","journal-title":"J Neurosurg."},{"key":"B46","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1016\/j.ijdevneu.2011.02.012","article-title":"The developing oligodendrocyte: key cellular target in brain injury in the premature infant","volume":"29","author":"Volpe","year":"2011","journal-title":"Int J Dev Neurosci."},{"key":"B47","doi-asserted-by":"publisher","first-page":"520","DOI":"10.1002\/ana.21359","article-title":"Arrested oligodendrocyte lineage maturation in chronic perinatal white matter injury","volume":"63","author":"Segovia","year":"2008","journal-title":"Ann Neurol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"1802","DOI":"10.3389\/fphys.2018.01802","article-title":"Birth and neonatal transition in the guinea pig: experimental approaches to prevent preterm birth and protect the premature fetus","volume":"9","author":"Hirst","year":"2018","journal-title":"Front Physiol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/S0304-3940(01)01861-4","article-title":"Effect of finasteride on behavioural arousal and somatosensory evoked potentials in fetal sheep","volume":"306","author":"Nicol","year":"2001","journal-title":"Neurosci Lett."},{"key":"B50","doi-asserted-by":"publisher","first-page":"821","DOI":"10.1016\/j.neuroscience.2005.07.021","article-title":"Neuroactive steroids and inhibitory neurotransmission: mechanisms of action and physiological relevance","volume":"138","author":"Belelli","year":"2006","journal-title":"Neuroscience."},{"key":"B51","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1038\/nrn1703","article-title":"Neurosteroids: endogenous regulators of the GABA(A) receptor","volume":"6","author":"Belelli","year":"2005","journal-title":"Nat Rev Neurosci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1016\/j.pneurobio.2013.08.005","article-title":"Allopregnanolone in the brain: protecting pregnancy and birth outcomes","volume":"113","author":"Brunton","year":"2014","journal-title":"Prog Neurobiol."},{"key":"B53","doi-asserted-by":"publisher","first-page":"602","DOI":"10.1016\/j.neuint.2007.07.018","article-title":"Neurosteroids in the fetus and neonate: potential protective role in compromised pregnancies","volume":"52","author":"Hirst","year":"2008","journal-title":"Neurochem Int."},{"key":"B54","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1080\/09513590500361747","article-title":"3alpha-reduced neuroactive steroids and their precursors during pregnancy and the postpartum period","volume":"21","author":"Gilbert Evans","year":"2005","journal-title":"Gynecol Endocrinol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1038\/s41390-018-0185-7","article-title":"Neurosteroid replacement therapy using the allopregnanolone-analogue ganaxolone following preterm birth in male guinea pigs","volume":"85","author":"Shaw","year":"2019","journal-title":"Pediatr Res."},{"key":"B56","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1016\/S0092-8674(01)00341-5","article-title":"GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition","volume":"105","author":"Ganguly","year":"2001","journal-title":"Cell."},{"key":"B57","article-title":"The GABAA excitatory-to-inhibitory switch in the hippocampus of perinatal guinea-pigs","author":"Coleman","year":"2013","journal-title":"The 40th Annual Meeting Fetal and Neonatal Physiological Society"},{"key":"B58","doi-asserted-by":"publisher","first-page":"4574","DOI":"10.1093\/cercor\/bhv218","article-title":"Developmental expression patterns of KCC2 and functionally associated molecules in the human brain","volume":"26","author":"Sedmak","year":"2016","journal-title":"Cereb Cortex."},{"key":"B59","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.nbd.2018.03.005","article-title":"Developmental excitatory-to-inhibitory GABA polarity switch is delayed in Ts65Dn mice, a genetic model of down syndrome","volume":"115","author":"Lysenko","year":"2018","journal-title":"Neurobiol Dis."},{"key":"B60","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1016\/j.biopsych.2019.08.023","article-title":"Cannabinoid exposure via lactation in rats disrupts perinatal programming of the gamma-aminobutyric acid trajectory and select early-life behaviors","volume":"87","author":"Scheyer","year":"2020","journal-title":"Biol Psychiatry."},{"key":"B61","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1038\/16697","article-title":"The K+\/Cl\u2013 co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation","volume":"397","author":"Rivera","year":"1999","journal-title":"Nature."},{"key":"B62","doi-asserted-by":"publisher","first-page":"29777","DOI":"10.1074\/jbc.M705053200","article-title":"Direct protein kinase C-dependent phosphorylation regulates the cell surface stability and activity of the potassium chloride cotransporter KCC2","volume":"282","author":"Lee","year":"2007","journal-title":"J Biol Chem."},{"key":"B63","doi-asserted-by":"publisher","first-page":"S48","DOI":"10.1016\/j.psyneuen.2009.08.009","article-title":"Neurosteroids: endogenous allosteric modulators of GABA(A) receptors","volume":"34","author":"Lambert","year":"2009","journal-title":"Psychoneuroendocrinology."},{"key":"B64","doi-asserted-by":"publisher","first-page":"7728","DOI":"10.1038\/s41598-019-44050-4","article-title":"Enhanced remyelination during late pregnancy: involvement of the GABAergic system","volume":"9","author":"Kalakh","year":"2019","journal-title":"Sci Rep."},{"key":"B65","doi-asserted-by":"publisher","first-page":"2092","DOI":"10.1002\/glia.23618","article-title":"Glutamate versus GABA in neuron-oligodendroglia communication","volume":"67","author":"Habermacher","year":"2019","journal-title":"Glia."},{"key":"B66","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1111\/cns.13195","article-title":"Ganaxolone enhances microglial clearance activity and promotes remyelination in focal demyelination in the corpus callosum of ovariectomized rats","volume":"26","author":"Mouihate","year":"2020","journal-title":"CNS Neurosci Ther."},{"key":"B67","doi-asserted-by":"publisher","first-page":"49","DOI":"10.3389\/fncel.2017.00049","article-title":"Androstenediol reduces demyelination-induced axonopathy in the rat corpus callosum: impact on microglial polarization","volume":"11","author":"Kalakh","year":"2017","journal-title":"Front Cell Neurosci."},{"key":"B68","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1016\/j.clp.2018.05.003","article-title":"Behavioral and socioemotional development in preterm children","volume":"45","author":"Peralta-Carcelen","year":"2018","journal-title":"Clin Perinatol"},{"key":"B69","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1038\/s41390-019-0385-9","article-title":"Behavioural and cognitive outcomes following an early stress-reduction intervention for very preterm and extremely preterm infants","volume":"86","author":"Milgrom","year":"2019","journal-title":"Pediatr Res."},{"key":"B70","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/j.neuroscience.2019.05.050","article-title":"Glucocorticoid-Induced reductions of myelination and connexin 43 in mixed central nervous system cell cultures are prevented by mifepristone","volume":"411","author":"Miguel-Hidalgo","year":"2019","journal-title":"Neuroscience."},{"key":"B71","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1016\/j.jsgi.2005.02.003","article-title":"Effect of pro-inflammatory cytokines on expression and activity of 11beta-hydroxysteroid dehydrogenase type 2 in cultured human term placental trophoblast and human choriocarcinoma JEG-3 cells","volume":"12","author":"Chisaka","year":"2005","journal-title":"J Soc Gynecol Investig."},{"key":"B72","doi-asserted-by":"publisher","first-page":"892","DOI":"10.1203\/00006450-200212000-00014","article-title":"Endotoxin increases sleep and brain allopregnanolone concentrations in newborn lambs","volume":"52","author":"Billiards","year":"2002","journal-title":"Pediatr Res."},{"key":"B73","doi-asserted-by":"publisher","first-page":"416","DOI":"10.1159\/000354176","article-title":"Effects of prenatal stress on fetal neurodevelopment and responses to maternal neurosteroid treatment in Guinea pigs","volume":"35","author":"Bennett","year":"2013","journal-title":"Dev Neurosci."},{"key":"B74","doi-asserted-by":"publisher","first-page":"580","DOI":"10.1080\/10253890.2017.1378637","article-title":"Maternal stress in pregnancy affects myelination and neurosteroid regulatory pathways in the guinea pig cerebellum","volume":"20","author":"Bennett","year":"2017","journal-title":"Stress."},{"key":"B75","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1159\/000437302","article-title":"Prenatal stress alters hippocampal neuroglia and increases anxiety in childhood","volume":"37","author":"Bennett","year":"2015","journal-title":"Dev Neurosci."},{"key":"B76","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/j.psyneuen.2016.04.011","article-title":"Severity and timing: How prenatal stress exposure affects glial developmental, emotional behavioural and plasma neurosteroid responses in guinea pig offspring","volume":"70","author":"Bennett","year":"2016","journal-title":"Psychoneuroendocrinology."},{"key":"B77","doi-asserted-by":"publisher","first-page":"250","DOI":"10.1017\/S2040174415000069","article-title":"Preterm birth affects GABAA receptor subunit mRNA levels during the foetal-to-neonatal transition in guinea pigs","volume":"6","author":"Shaw","year":"2015","journal-title":"J Dev Orig Health Dis."},{"key":"B78","doi-asserted-by":"publisher","first-page":"584","DOI":"10.1017\/S2040174417000307","article-title":"Effects of combined IUGR and prenatal stress on the development of the hippocampus in a fetal guinea pig model","volume":"8","author":"Cumberland","year":"2017","journal-title":"J Dev Orig Health Dis"},{"key":"B79","doi-asserted-by":"publisher","first-page":"306","DOI":"10.1007\/s12311-016-0802-0","article-title":"Cerebellar changes in guinea pig offspring following suppression of neurosteroid synthesis during late gestation","volume":"16","author":"Cumberland","year":"2017","journal-title":"Cerebellum."},{"key":"B80","doi-asserted-by":"publisher","first-page":"2863","DOI":"10.1210\/en.2015-1149","article-title":"5alpha-Reductase type 2 regulates glucocorticoid action and metabolic phenotype in human hepatocytes","volume":"156","author":"Nasiri","year":"2015","journal-title":"Endocrinology."},{"key":"B81","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1523\/JNEUROSCI.5104-13.2015","article-title":"5alpha-Reduced neurosteroids sex-dependently reverse central prenatal programming of neuroendocrine stress responses in rats","volume":"35","author":"Brunton","year":"2015","journal-title":"J Neurosci."},{"key":"B82","doi-asserted-by":"publisher","first-page":"166","DOI":"10.1111\/j.1365-2826.2009.01949.x","article-title":"The effect of betamethasone treatment on neuroactive steroid synthesis in a foetal guinea pig model of growth restriction","volume":"22","author":"McKendry","year":"2010","journal-title":"J Neuroendocrinol."},{"key":"B83","doi-asserted-by":"publisher","first-page":"599","DOI":"10.1071\/RD08224","article-title":"Changes in human placental 5alpha-reductase isoenzyme expression with advancing gestation: effects of fetal sex and glucocorticoid exposure","volume":"21","author":"Vu","year":"2009","journal-title":"Reprod Fertil Dev."},{"key":"B84","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.neuroscience.2014.04.009","article-title":"Prenatal betamethasone does not affect glutamatergic or GABAergic neurogenesis in preterm newborns","volume":"270","author":"Vose","year":"2014","journal-title":"Neuroscience."},{"key":"B85","doi-asserted-by":"publisher","first-page":"1924","DOI":"10.1001\/jama.2020.3937","article-title":"Associations between maternal antenatal corticosteroid treatment and mental and behavioral disorders in children","volume":"323","author":"Raikkonen","year":"2020","journal-title":"JAMA."},{"key":"B86","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1016\/j.neuropharm.2012.04.013","article-title":"Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice","volume":"68","author":"Matrisciano","year":"2013","journal-title":"Neuropharmacology."},{"key":"B87","doi-asserted-by":"publisher","first-page":"e711","DOI":"10.1038\/tp.2015.191","article-title":"Behavioral and molecular neuroepigenetic alterations in prenatally stressed mice: relevance for the study of chromatin remodeling properties of antipsychotic drugs","volume":"6","author":"Dong","year":"2016","journal-title":"Transl Psychiatry."},{"key":"B88","doi-asserted-by":"publisher","first-page":"4170","DOI":"10.1210\/en.2013-1484","article-title":"Effects of antenatal synthetic glucocorticoid on glucocorticoid receptor binding, DNA methylation, and genome-wide mRNA levels in the fetal male hippocampus","volume":"154","author":"Crudo","year":"2013","journal-title":"Endocrinology."},{"key":"B89","doi-asserted-by":"publisher","first-page":"1168","DOI":"10.1210\/en.2012-1980","article-title":"Glucocorticoid programming of the fetal male hippocampal epigenome","volume":"154","author":"Crudo","year":"2013","journal-title":"Endocrinology."},{"key":"B90","doi-asserted-by":"publisher","first-page":"E729","DOI":"10.1152\/ajpendo.2001.280.5.E729","article-title":"Maternal glucocorticoid treatment programs HPA regulation in adult offspring: sex-specific effects","volume":"280","author":"Liu","year":"2001","journal-title":"Am J Physiol Endocrinol Metab."},{"key":"B91","doi-asserted-by":"publisher","first-page":"586","DOI":"10.1016\/j.brainresrev.2007.06.013","article-title":"Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids","volume":"57","author":"Kapoor","year":"2008","journal-title":"Brain Res Rev."},{"key":"B92","doi-asserted-by":"publisher","first-page":"5571","DOI":"10.1113\/JP274949","article-title":"The fetus at the tipping point: modifying the outcome of fetal asphyxia","volume":"596","author":"Dhillon","year":"2018","journal-title":"J Physiol."},{"key":"B93","doi-asserted-by":"publisher","first-page":"3045","DOI":"10.1523\/JNEUROSCI.5200-05.2006","article-title":"Spatial heterogeneity in oligodendrocyte lineage maturation and not cerebral blood flow predicts fetal ovine periventricular white matter injury","volume":"26","author":"Riddle","year":"2006","journal-title":"J Neurosci."},{"key":"B94","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1523\/JNEUROSCI.22-02-00455.2002","article-title":"Selective vulnerability of late oligodendrocyte progenitors to hypoxia\u2013ischemia","volume":"22","author":"Back","year":"2002","journal-title":"J Neurosci."},{"key":"B95","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1002\/glia.20267","article-title":"Differential oxidative stress in oligodendrocytes and neurons after excitotoxic insults and protection by natural polyphenols","volume":"53","author":"Ibarretxe","year":"2006","journal-title":"Glia."},{"key":"B96","doi-asserted-by":"publisher","first-page":"9519","DOI":"10.1523\/JNEUROSCI.23-29-09519.2003","article-title":"Caspase-dependent and caspase-independent oligodendrocyte death mediated by AMPA and kainate receptors","volume":"23","author":"Sanchez-Gomez","year":"2003","journal-title":"J Neurosci."},{"key":"B97","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1002\/(SICI)1097-4547(19961115)46:4<427::AID-JNR4>3.0.CO;2-I","article-title":"Pathophysiology of oligodendroglial excitotoxicity","volume":"46","author":"Yoshioka","year":"1996","journal-title":"J Neurosci Res."},{"key":"B98","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1006\/nbdi.2001.0457","article-title":"Ca(2+) influx through AMPA or kainate receptors alone is sufficient to initiate excitotoxicity in cultured oligodendrocytes","volume":"9","author":"Alberdi","year":"2002","journal-title":"Neurobiol Dis."},{"key":"B99","doi-asserted-by":"publisher","first-page":"810","DOI":"10.1002\/glia.22965","article-title":"Movement and structure of mitochondria in oligodendrocytes and their myelin sheaths","volume":"64","author":"Rinholm","year":"2016","journal-title":"Glia."},{"key":"B100","doi-asserted-by":"publisher","first-page":"RC16","DOI":"10.1523\/JNEUROSCI.19-14-j0002.1999","article-title":"Novel injury mechanism in anoxia and trauma of spinal cord white matter: glutamate release via reverse Na+-dependent glutamate transport","volume":"19","author":"Li","year":"1999","journal-title":"J Neurosci."},{"key":"B101","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1038\/nm0398-291","article-title":"Oligodendrocytes from forebrain are highly vulnerable to AMPA\/kainate receptor-mediated excitotoxicity","volume":"4","author":"McDonald","year":"1998","journal-title":"Nat Med."},{"key":"B102","doi-asserted-by":"publisher","first-page":"1167","DOI":"10.1038\/nature04301","article-title":"NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury","volume":"438","author":"Salter","year":"2005","journal-title":"Nature."},{"key":"B103","doi-asserted-by":"publisher","first-page":"e6705","DOI":"10.1371\/journal.pone.0006705","article-title":"Glutamate excitotoxicity inflicts paranodal myelin splitting and retraction","volume":"4","author":"Fu","year":"2009","journal-title":"PLoS ONE."},{"key":"B104","doi-asserted-by":"publisher","first-page":"1162","DOI":"10.1038\/nature04302","article-title":"NMDA receptors are expressed in oligodendrocytes and activated in ischaemia","volume":"438","author":"Karadottir","year":"2005","journal-title":"Nature."},{"key":"B105","doi-asserted-by":"publisher","first-page":"705","DOI":"10.1016\/S0306-4522(02)00756-X","article-title":"Extracellular glutamate levels and neuropathology in cerebral white matter following repeated umbilical cord occlusion in the near term fetal sheep","volume":"116","author":"Loeliger","year":"2003","journal-title":"Neuroscience."},{"key":"B106","doi-asserted-by":"publisher","first-page":"838","DOI":"10.1016\/j.neuroscience.2009.07.009","article-title":"Role of neurosteroids in regulating cell death and proliferation in the late gestation fetal brain","volume":"163","author":"Yawno","year":"2009","journal-title":"Neuroscience."},{"key":"B107","doi-asserted-by":"publisher","first-page":"1726","DOI":"10.1016\/j.neuroscience.2007.03.023","article-title":"Inhibition of neurosteroid synthesis increases asphyxia-induced brain injury in the late gestation fetal sheep","volume":"146","author":"Yawno","year":"2007","journal-title":"Neuroscience."},{"key":"B108","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1113\/jphysiol.2004.069336","article-title":"Increased allopregnanolone levels in the fetal sheep brain following umbilical cord occlusion","volume":"560","author":"Nguyen","year":"2004","journal-title":"J Physiol."},{"key":"B109","doi-asserted-by":"publisher","first-page":"13","DOI":"10.3109\/10253890.2010.504789","article-title":"Neuroactive steroids induce changes in fetal sheep behavior during normoxic and asphyxic states","volume":"14","author":"Yawno","year":"2011","journal-title":"Stress."},{"key":"B110","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1007\/s00401-009-0601-5","article-title":"Oligodendrocytes: biology and pathology","volume":"119","author":"Bradl","year":"2010","journal-title":"Acta Neuropathol."},{"key":"B111","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1159\/000242818","article-title":"Brain development in the fetus, neonate and infant","volume":"54","author":"Herschkowitz","year":"1988","journal-title":"Neonatology."},{"key":"B112","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1016\/j.earlhumdev.2005.10.013","article-title":"Ontogeny of the human central nervous system: what is happening when?","volume":"82","author":"de Graaf-Peters","year":"2006","journal-title":"Early Hum Dev."},{"key":"B113","doi-asserted-by":"publisher","first-page":"898","DOI":"10.1002\/glia.23750","article-title":"Differential effects of glucose deprivation on the survival of fetal versus adult neural stem cells-derived oligodendrocyte precursor cells","volume":"68","author":"Baldassarro","year":"2020","journal-title":"Glia."},{"key":"B114","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1097\/01.wnr.0000192733.00535.b6","article-title":"Hypoglycemia influences oligodendrocyte development and myelin formation","volume":"17","author":"Yan","year":"2006","journal-title":"Neuroreport."},{"key":"B115","doi-asserted-by":"publisher","first-page":"538","DOI":"10.1523\/JNEUROSCI.3516-10.2011","article-title":"Regulation of oligodendrocyte development and myelination by glucose and lactate","volume":"31","author":"Rinholm","year":"2011","journal-title":"J Neurosci."},{"key":"B116","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1111\/cns.12782","article-title":"Monocarboxylate transporter 1 and the vulnerability of oligodendrocyte lineage cells to metabolic stresses","volume":"24","author":"Zhou","year":"2018","journal-title":"CNS Neurosci Ther."},{"key":"B117","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.metabol.2017.11.017","article-title":"Circadian regulation of glucose, lipid, energy metabolism in humans","volume":"84","author":"Poggiogalle","year":"2018","journal-title":"Metabolism."},{"key":"B118","doi-asserted-by":"publisher","first-page":"549","DOI":"10.1038\/nrn2683","article-title":"The genetic and molecular regulation of sleep: from fruit flies to humans","volume":"10","author":"Cirelli","year":"2009","journal-title":"Nat Rev Neurosci."},{"key":"B119","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/S0896-6273(03)00814-6","article-title":"Extensive and divergent effects of sleep and wakefulness on brain gene expression","volume":"41","author":"Cirelli","year":"2004","journal-title":"Neuron."},{"key":"B120","doi-asserted-by":"publisher","first-page":"1147","DOI":"10.1093\/sleep\/33.9.1147","article-title":"Separating the contribution of glucocorticoids and wakefulness to the molecular and electrophysiological correlates of sleep homeostasis","volume":"33","author":"Mongrain","year":"2010","journal-title":"Sleep."},{"key":"B121","doi-asserted-by":"publisher","first-page":"14288","DOI":"10.1523\/JNEUROSCI.5102-12.2013","article-title":"Effects of sleep and wake on oligodendrocytes and their precursors","volume":"33","author":"Bellesi","year":"2013","journal-title":"J Neurosci."},{"key":"B122","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1016\/S0896-6273(00)80155-5","article-title":"GGF\/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors","volume":"17","author":"Canoll","year":"1996","journal-title":"Neuron."},{"key":"B123","doi-asserted-by":"publisher","first-page":"620","DOI":"10.1523\/JNEUROSCI.5486-08.2009","article-title":"Long-term homeostasis of extracellular glutamate in the rat cerebral cortex across sleep and waking states","volume":"29","author":"Dash","year":"2009","journal-title":"J Neurosci."},{"key":"B124","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1677\/joe.0.1520379","article-title":"Effect of alteration of maternal plasma progesterone concentrations on fetal behavioural state during late gestation","volume":"152","author":"Nicol","year":"1997","journal-title":"J Endocrinol."},{"key":"B125","doi-asserted-by":"publisher","first-page":"767","DOI":"10.1071\/R97074","article-title":"Suppression of arousal by progesterone in fetal sheep","volume":"9","author":"Crossley","year":"1997","journal-title":"Reprod Fertil Dev."},{"key":"B126","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/j.biocel.2016.05.018","article-title":"Activity-dependent calcium signalling in oligodendrocyte generation","volume":"77","author":"Pitman","year":"2016","journal-title":"Int J Biochem Cell Biol."},{"key":"B127","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/j.brainres.2019.05.027","article-title":"Neuroprotective effects of a protein tyrosine phosphatase inhibitor against hippocampal excitotoxic injury","volume":"1719","author":"Kim","year":"2019","journal-title":"Brain Res."},{"key":"B128","doi-asserted-by":"publisher","first-page":"34","DOI":"10.3389\/fnmol.2012.00034","article-title":"The essential role of AMPA receptor GluR2 subunit RNA editing in the normal and diseased brain","volume":"5","author":"Wright","year":"2012","journal-title":"Front Mol Neurosci."},{"key":"B129","doi-asserted-by":"publisher","first-page":"10499","DOI":"10.1073\/pnas.89.21.10499","article-title":"Switch in glutamate receptor subunit gene expression in CA1 subfield of hippocampus following global ischemia in rats","volume":"89","author":"Pellegrini-Giampietro","year":"1992","journal-title":"Proc Natl Acad Sci U.S.A."},{"key":"B130","doi-asserted-by":"publisher","first-page":"2112","DOI":"10.1523\/JNEUROSCI.23-06-02112.2003","article-title":"Ischemic insults derepress the gene silencer REST in neurons destined to die","volume":"23","author":"Calderone","year":"2003","journal-title":"J Neurosci."},{"key":"B131","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1002\/cne.20978","article-title":"Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic\/ischemic injury. II. Human cerebral white matter and cortex","volume":"497","author":"Talos","year":"2006","journal-title":"J Comp Neurol."},{"key":"B132","doi-asserted-by":"publisher","first-page":"4412","DOI":"10.1523\/JNEUROSCI.0477-04.2004","article-title":"Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate","volume":"24","author":"Follett","year":"2004","journal-title":"J Neurosci."},{"key":"B133","doi-asserted-by":"publisher","first-page":"990","DOI":"10.1093\/jnen\/63.9.990","article-title":"Developmental lag in superoxide dismutases relative to other antioxidant enzymes in premyelinated human telencephalic white matter","volume":"63","author":"Folkerth","year":"2004","journal-title":"J Neuropathol Exp Neurol."},{"key":"B134","doi-asserted-by":"publisher","first-page":"101110","DOI":"10.1016\/j.siny.2020.101110","article-title":"Mechanisms of brain injury in newborn infants associated with the fetal inflammatory response syndrome","volume":"25","author":"Yap","year":"2020","journal-title":"Semin Fetal Neonatal Med"},{"key":"B135","doi-asserted-by":"publisher","first-page":"1034","DOI":"10.1016\/j.neuroscience.2008.02.065","article-title":"Glutamate-induced losses of oligodendrocytes and neurons and activation of caspase-3 in the rat spinal cord","volume":"153","author":"Xu","year":"2008","journal-title":"Neuroscience."},{"key":"B136","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1159\/000362433","article-title":"GABA, resting-state connectivity and the developing brain","volume":"106","author":"Kwon","year":"2014","journal-title":"Neonatology."},{"key":"B137","doi-asserted-by":"publisher","first-page":"10549","DOI":"10.1038\/s41598-020-67188-y","article-title":"Age and sex influences gamma-aminobutyric acid concentrations in the developing brain of very premature infants","volume":"10","author":"Basu","year":"2020","journal-title":"Sci Rep."},{"key":"B138","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/j.neuroscience.2005.05.023","article-title":"Progesterone increases oligodendroglial cell proliferation in rat cerebellar slice cultures","volume":"135","author":"Ghoumari","year":"2005","journal-title":"Neuroscience."},{"key":"B139","doi-asserted-by":"publisher","first-page":"848","DOI":"10.1046\/j.1471-4159.2003.01881.x","article-title":"Progesterone and its metabolites increase myelin basic protein expression in organotypic slice cultures of rat cerebellum","volume":"86","author":"Ghoumari","year":"2003","journal-title":"J Neurochem."},{"key":"B140","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1111\/jpc.13882_31","article-title":"Behavioural deficits induced by chronic perinatal stress is ameliorated by Xbd173 administration in male guinea pig offspring","volume":"54","author":"Crombie","year":"2018","journal-title":"J Paediatr Child Health."}],"container-title":["Frontiers in Pediatrics"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fped.2021.618052\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,4]],"date-time":"2021-02-04T05:09:26Z","timestamp":1612415366000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fped.2021.618052\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,4]]},"references-count":140,"alternative-id":["10.3389\/fped.2021.618052"],"URL":"https:\/\/doi.org\/10.3389\/fped.2021.618052","relation":{},"ISSN":["2296-2360"],"issn-type":[{"value":"2296-2360","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,2,4]]},"article-number":"618052"}}