{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,24]],"date-time":"2026-03-24T09:23:38Z","timestamp":1774344218256,"version":"3.50.1"},"reference-count":87,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2020,12,28]],"date-time":"2020-12-28T00:00:00Z","timestamp":1609113600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Encephalopathy of Prematurity (EoP) is a major cause of morbidity in (extreme) preterm neonates. Though the majority of EoP research has focused on failure of oligodendrocyte maturation as an underlying pathophysiological mechanism, recent pioneer work has identified developmental disturbances in inhibitory interneurons to contribute to EoP. Here we investigated interneuron abnormalities in two experimental models of EoP and explored the potential of two promising treatment strategies, namely intranasal mesenchymal stem cells (MSCs) or insulin-like growth factor I (IGF1), to restore interneuron development. In rats, fetal inflammation and postnatal hypoxia led to a transient increase in total cortical interneuron numbers, with a layer-specific deficit in parvalbumin (PV)+ interneurons. Additionally, a transient excess of total cortical cell density was observed, including excitatory neuron numbers. In the hippocampal cornu ammonis (CA) 1 region, long-term deficits in total interneuron numbers and PV+ subtype were observed. In mice subjected to postnatal hypoxia\/ischemia and systemic inflammation, total numbers of cortical interneurons remained unaffected; however, subtype analysis revealed a global, transient reduction in PV+ cells and a long-lasting layer-specific increase in vasoactive intestinal polypeptide (VIP)+ cells. In the dentate gyrus, a long-lasting deficit of somatostatin (SST)+ cells was observed. Both intranasal MSC and IGF1 therapy restored the majority of interneuron abnormalities in EoP mice. In line with the histological findings, EoP mice displayed impaired social behavior, which was partly restored by the therapies. In conclusion, induction of experimental EoP is associated with model-specific disturbances in interneuron development. In addition, intranasal MSCs and IGF1 are promising therapeutic strategies to aid interneuron development after EoP.<\/jats:p>","DOI":"10.3390\/ijms22010211","type":"journal-article","created":{"date-parts":[[2020,12,28]],"date-time":"2020-12-28T10:33:56Z","timestamp":1609151636000},"page":"211","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Regenerative Therapies to Restore Interneuron Disturbances in Experimental Models of Encephalopathy of Prematurity"],"prefix":"10.3390","volume":"22","author":[{"given":"Josine E. G.","family":"Vaes","sequence":"first","affiliation":[{"name":"Department for Developmental Origins of Disease, University Medical Center Utrecht Brain Center and Wilhelmina Children\u2019s Hospital, Utrecht University, 3584 Utrecht, The Netherlands"},{"name":"Department of Neonatology, University Medical Center Utrecht Brain Center and Wilhelmina Children\u2019s Hospital, Utrecht University, 3584 Utrecht, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9847-5490","authenticated-orcid":false,"given":"Chantal M.","family":"Kosmeijer","sequence":"additional","affiliation":[{"name":"Department for Developmental Origins of Disease, University Medical Center Utrecht Brain Center and Wilhelmina Children\u2019s Hospital, Utrecht University, 3584 Utrecht, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marthe","family":"Kaal","sequence":"additional","affiliation":[{"name":"Department for Developmental Origins of Disease, University Medical Center Utrecht Brain Center and Wilhelmina Children\u2019s Hospital, Utrecht University, 3584 Utrecht, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rik","family":"van Vliet","sequence":"additional","affiliation":[{"name":"Department for Developmental Origins of Disease, University Medical Center Utrecht Brain Center and Wilhelmina Children\u2019s Hospital, Utrecht University, 3584 Utrecht, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Myrna J. V.","family":"Brandt","sequence":"additional","affiliation":[{"name":"Department for Developmental Origins of Disease, University Medical Center Utrecht Brain Center and Wilhelmina Children\u2019s Hospital, Utrecht University, 3584 Utrecht, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Manon J. N. L.","family":"Benders","sequence":"additional","affiliation":[{"name":"Department of Neonatology, University Medical Center Utrecht Brain Center and Wilhelmina Children\u2019s Hospital, Utrecht University, 3584 Utrecht, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cora H.","family":"Nijboer","sequence":"additional","affiliation":[{"name":"Department for Developmental Origins of Disease, University Medical Center Utrecht Brain Center and Wilhelmina Children\u2019s Hospital, Utrecht University, 3584 Utrecht, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,12,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1038\/nrneurol.2010.53","article-title":"Neurobiology of injury to the developing brain","volume":"6","author":"Deng","year":"2010","journal-title":"Nat. Rev. Neurol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1016\/S0140-6736(08)60380-3","article-title":"Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): A longitudinal cohort study","volume":"371","author":"Larroque","year":"2008","journal-title":"Lancet"},{"key":"ref_3","doi-asserted-by":"crossref","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":"New Engl. J. Med."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1136\/archdischild-2017-313414","article-title":"Cognitive trajectories from infancy to early adulthood following birth before 26 weeks of gestation: A prospective, population-based cohort study","volume":"103","author":"Linsell","year":"2018","journal-title":"Arch. Dis. Child."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1002\/ana.24132","article-title":"Brain injury in premature neonates: A primary cerebral dysmaturation disorder?","volume":"75","author":"Back","year":"2014","journal-title":"Ann. Neurol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.pneurobio.2015.11.002","article-title":"Impaired oligodendrocyte maturation in preterm infants: Potential therapeutic targets","volume":"136","author":"Heijnen","year":"2016","journal-title":"Prog. Neurobiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1016\/S1474-4422(08)70294-1","article-title":"Brain injury in premature infants: A complex amalgam of destructive and developmental disturbances","volume":"8","author":"Volpe","year":"2009","journal-title":"Lancet Neurol."},{"key":"ref_8","doi-asserted-by":"crossref","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":"ref_9","doi-asserted-by":"crossref","first-page":"F153","DOI":"10.1136\/adc.2006.108837","article-title":"Pathogenesis of cerebral white matter injury of prematurity","volume":"93","author":"Khwaja","year":"2008","journal-title":"Arch. Dis. Child. Fetal Neonatal Ed."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1007\/s00234-013-1233-y","article-title":"Imaging the premature brain: Ultrasound or MRI?","volume":"55","author":"Benders","year":"2013","journal-title":"Neuroradiology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1042","DOI":"10.1016\/S1474-4422(09)70257-1","article-title":"Imaging biomarkers of outcome in the developing preterm brain","volume":"8","author":"Ment","year":"2009","journal-title":"Lancet Neurol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1302","DOI":"10.1523\/JNEUROSCI.21-04-01302.2001","article-title":"Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury","volume":"21","author":"Back","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1523\/JNEUROSCI.4445-12.2013","article-title":"Neurogenesis continues in the third trimester of pregnancy and is suppressed by premature birth","volume":"33","author":"Malik","year":"2013","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"575","DOI":"10.3389\/fneur.2020.00575","article-title":"Cortical Gray Matter Injury in Encephalopathy of Prematurity: Link to Neurodevelopmental Disorders","volume":"11","author":"Fleiss","year":"2020","journal-title":"Front. Neurol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2242","DOI":"10.1093\/cercor\/bhv074","article-title":"Extended Production of Cortical Interneurons into the Third Trimester of Human Gestation","volume":"26","author":"Arshad","year":"2016","journal-title":"Cereb. Cortex"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1016\/j.neuron.2018.10.009","article-title":"Development and Functional Diversification of Cortical Interneurons","volume":"100","author":"Lim","year":"2018","journal-title":"Neuron"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1038\/nrn3155","article-title":"Interneuron dysfunction in psychiatric disorders","volume":"13","year":"2012","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1038\/nm.4225","article-title":"Developmental timing and critical windows for the treatment of psychiatric disorders","volume":"22","year":"2016","journal-title":"Nat. Med."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"955","DOI":"10.3389\/fphys.2019.00955","article-title":"Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and Human","volume":"10","author":"Stolp","year":"2019","journal-title":"Front. Physiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"7378","DOI":"10.1523\/JNEUROSCI.0478-18.2018","article-title":"Estrogen Treatment Reverses Prematurity-Induced Disruption in Cortical Interneuron Population","volume":"38","author":"Panda","year":"2018","journal-title":"J. Neurosci."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Lacaille, H., Vacher, C.M., Bakalar, D., O\u2019Reilly, J.J., Salzbank, J., and Penn, A.A. (2019). Impaired Interneuron Development in a Novel Model of Neonatal Brain Injury. eNeuro, 6.","DOI":"10.1523\/ENEURO.0300-18.2019"},{"key":"ref_22","first-page":"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":"ref_23","doi-asserted-by":"crossref","first-page":"563","DOI":"10.3389\/fphys.2019.00563","article-title":"Dysmaturation of Somatostatin Interneurons Following Umbilical Cord Occlusion in Preterm Fetal Sheep","volume":"10","author":"Ardalan","year":"2019","journal-title":"Front. Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1100","DOI":"10.1523\/JNEUROSCI.1875-17.2017","article-title":"Disruption of Interneuron Neurogenesis in Premature Newborns and Reversal with Estrogen Treatment","volume":"38","author":"Tibrewal","year":"2018","journal-title":"J. Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"112621","DOI":"10.1016\/j.psychres.2019.112621","article-title":"Reduced cortical somatostatin gene expression in a rat model of maternal immune activation","volume":"282","author":"Duchatel","year":"2019","journal-title":"Psychiatry Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"956","DOI":"10.1038\/mp.2015.222","article-title":"Maternal immune activation leads to selective functional deficits in offspring parvalbumin interneurons","volume":"21","author":"Canetta","year":"2016","journal-title":"Mol. Psychiatry"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"13375","DOI":"10.1523\/JNEUROSCI.5286-12.2013","article-title":"Hypoxia-induced developmental delays of inhibitory interneurons are reversed by environmental enrichment in the postnatal mouse forebrain","volume":"33","author":"Komitova","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"540","DOI":"10.3389\/fphys.2019.00540","article-title":"The Potential of Stem Cell Therapy to Repair White Matter Injury in Preterm Infants: Lessons Learned From Experimental Models","volume":"10","author":"Vaes","year":"2019","journal-title":"Front. Physiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1038\/pr.2011.64","article-title":"Mesenchymal stem cells as a treatment for neonatal ischemic brain damage","volume":"71","author":"Kavelaars","year":"2012","journal-title":"Pediatr. Res."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Ophelders, D., Gussenhoven, R., Klein, L., Jellema, R.K., Westerlaken, R.J.J., H\u00fctten, M.C., Vermeulen, J., Wassink, G., Gunn, A.J., and Wolfs, T. (2020). Preterm Brain Injury, Antenatal Triggers, and Therapeutics: Timing Is Key. Cells, 9.","DOI":"10.3390\/cells9081871"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1111\/dmcn.13528","article-title":"Repair of neonatal brain injury: Bringing stem cell-based therapy into clinical practice","volume":"59","author":"Wagenaar","year":"2017","journal-title":"Dev. Med. Child. Neurol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Vaes, J.E.G., van Kammen, C.M., Trayford, C., van der Toorn, A., Ruhwedel, T., Benders, M.J.N.L., Dijkhuizen, R.M., M\u00f6bius, W., van Rijt, S.H., and Nijboer, C.H. (2020). Intranasal mesenchymal stem cell therapy to boost myelination after encephalopathy of prematurity. Glia.","DOI":"10.1002\/glia.23919"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/j.bbi.2009.10.017","article-title":"Mesenchymal stem cell treatment after neonatal hypoxic-ischemic brain injury improves behavioral outcome and induces neuronal and oligodendrocyte regeneration","volume":"24","author":"Kavelaars","year":"2010","journal-title":"Brain Behav. Immunity"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1089\/scd.2016.0108","article-title":"Wharton\u2019s Jelly Mesenchymal Stem Cells Protect the Immature Brain in Rats and Modulate Cell Fate","volume":"26","author":"Mueller","year":"2017","journal-title":"Stem Cells Dev."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1038\/s41390-019-0366-z","article-title":"Umbilical cord blood versus mesenchymal stem cells for inflammation-induced preterm brain injury in fetal sheep","volume":"86","author":"Paton","year":"2019","journal-title":"Pediatr. Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1111\/apa.13350","article-title":"Insulin-like growth factor 1 has multisystem effects on foetal and preterm infant development","volume":"105","author":"Hellstrom","year":"2016","journal-title":"Acta Paediatr."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1038\/pr.2013.135","article-title":"Circulatory insulin-like growth factor-I and brain volumes in relation to neurodevelopmental outcome in very preterm infants","volume":"74","author":"Hovel","year":"2013","journal-title":"Pediatr. Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/0896-6273(95)90216-3","article-title":"Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons","volume":"14","author":"Beck","year":"1995","journal-title":"Neuron"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.1210\/jc.2010-2440","article-title":"Postnatal decrease in circulating insulin-like growth factor-I and low brain volumes in very preterm infants","volume":"96","author":"Hovel","year":"2011","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_40","first-page":"52","article-title":"IGF-I: A Key Growth Factor that Regulates Neurogenesis and Synaptogenesis from Embryonic to Adult Stages of the Brain","volume":"10","author":"Defterali","year":"2016","journal-title":"Front. Neurosci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1067","DOI":"10.1055\/s-0036-1586109","article-title":"Role of Insulinlike Growth Factor 1 in Fetal Development and in the Early Postnatal Life of Premature Infants","volume":"33","author":"Ley","year":"2016","journal-title":"Am. J. Perinatol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/j.neuroscience.2011.08.003","article-title":"Intranasal administration of insulin-like growth factor-1 protects against lipopolysaccharide-induced injury in the developing rat brain","volume":"194","author":"Cai","year":"2011","journal-title":"Neuroscience"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/j.expneurol.2009.03.021","article-title":"Intranasal administration of IGF-1 attenuates hypoxic-ischemic brain injury in neonatal rats","volume":"217","author":"Lin","year":"2009","journal-title":"Exp. Neurol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1097\/00004647-200105000-00003","article-title":"Insulin-like growth factor-1 reduces postischemic white matter injury in fetal sheep","volume":"21","author":"Guan","year":"2001","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1097\/01.WCB.0000067720.12805.6F","article-title":"Insulin-like growth factor (IGF)-1 suppresses oligodendrocyte caspase-3 activation and increases glial proliferation after ischemia in near-term fetal sheep","volume":"23","author":"Cao","year":"2003","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1097\/nen.0b013e3180301c06","article-title":"Layer-specific markers as probes for neuron type identity in human neocortex and malformations of cortical development","volume":"66","author":"Hevner","year":"2007","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1002\/cne.22229","article-title":"Immunochemical characterization of inhibitory mouse cortical neurons: Three chemically distinct classes of inhibitory cells","volume":"518","author":"Xu","year":"2010","journal-title":"J. Comp. Neurol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.neuron.2016.06.033","article-title":"GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits","volume":"91","author":"Tremblay","year":"2016","journal-title":"Neuron"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1002\/dneu.20853","article-title":"Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons","volume":"71","author":"Rudy","year":"2011","journal-title":"Dev. Neurobiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1002\/glia.23216","article-title":"Combined fetal inflammation and postnatal hypoxia causes myelin deficits and autism-like behavior in a rat model of diffuse white matter injury","volume":"66","author":"Achterberg","year":"2018","journal-title":"Glia"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1619","DOI":"10.1152\/physrev.00007.2017","article-title":"Hippocampal GABAergic Inhibitory Interneurons","volume":"97","author":"Pelkey","year":"2017","journal-title":"Physiol. Rev."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1111\/j.1601-1848.2004.00076.x","article-title":"Sociability and preference for social novelty in five inbred strains: An approach to assess autistic-like behavior in mice","volume":"3","author":"Moy","year":"2004","journal-title":"Genes Brain Behav."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1038\/nrn2851","article-title":"Behavioural phenotyping assays for mouse models of autism","volume":"11","author":"Silverman","year":"2010","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_54","first-page":"1931","article-title":"The Number of Parvalbumin-Expressing Interneurons Is Decreased in the Prefrontal Cortex in Autism","volume":"27","author":"Hashemi","year":"2017","journal-title":"Cereb. Cortex"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1038\/s41390-018-0214-6","article-title":"Cortical interneuron function in autism spectrum condition","volume":"85","author":"Lunden","year":"2019","journal-title":"Pediatr. Res."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"18060","DOI":"10.1073\/pnas.1908126116","article-title":"Inhibitory interneurons mediate autism-associated behaviors via 4E-BP2","volume":"116","author":"Wiebe","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1016\/j.biopsych.2016.05.011","article-title":"Excitation\/Inhibition Imbalance in Animal Models of Autism Spectrum Disorders","volume":"81","author":"Lee","year":"2017","journal-title":"Biol. Psychiatry"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1203\/PDR.0b013e318212faa0","article-title":"Preterm Birth and Childhood Psychiatric Disorders","volume":"69","author":"Johnson","year":"2011","journal-title":"Pediatr. Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"3867","DOI":"10.1242\/dev.132852","article-title":"Cortical interneuron development: A tale of time and space","volume":"144","author":"Hu","year":"2017","journal-title":"Development"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1248","DOI":"10.1038\/s41380-019-0426-0","article-title":"Excitation-inhibition balance as a framework for investigating mechanisms in neuropsychiatric disorders","volume":"24","author":"Sohal","year":"2019","journal-title":"Mol. Psychiatry"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1038\/nature12983","article-title":"Interneuron cell types are fit to function","volume":"505","author":"Kepecs","year":"2014","journal-title":"Nature"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"2313","DOI":"10.1038\/s41380-019-0539-5","article-title":"Maternal inflammation has a profound effect on cortical interneuron development in a stage and subtype-specific manner","volume":"25","author":"Vasistha","year":"2020","journal-title":"Mol. Psychiatry"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.pediatrneurol.2019.02.016","article-title":"Dysmaturation of Premature Brain: Importance, Cellular Mechanisms, and Potential Interventions","volume":"95","author":"Volpe","year":"2019","journal-title":"Pediatr. Neurol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.semcdb.2017.09.017","article-title":"Conserved rules in embryonic development of cortical interneurons","volume":"76","author":"Laclef","year":"2018","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1038\/nrn.2017.30","article-title":"Genetic and activity-dependent mechanisms underlying interneuron diversity","volume":"18","author":"Wamsley","year":"2017","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"845","DOI":"10.1093\/cercor\/bhq155","article-title":"GABAergic interneuron lineages selectively sort into specific cortical layers during early postnatal development","volume":"21","author":"Miyoshi","year":"2011","journal-title":"Cereb. Cortex"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1710","DOI":"10.1016\/j.celrep.2018.01.064","article-title":"Modulation of Apoptosis Controls Inhibitory Interneuron Number in the Cortex","volume":"22","author":"Denaxa","year":"2018","journal-title":"Cell Rep."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"3078","DOI":"10.1523\/JNEUROSCI.3055-06.2007","article-title":"Lhx6 Activity Is Required for the Normal Migration and Specification of Cortical Interneuron Subtypes","volume":"27","author":"Liodis","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.conb.2013.12.012","article-title":"Genetic programs controlling cortical interneuron fate","volume":"26","author":"Kessaris","year":"2014","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_70","first-page":"3","article-title":"Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining","volume":"1","author":"Gonchar","year":"2007","journal-title":"Front. Neuroanat."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1016\/j.celrep.2019.06.086","article-title":"Biphasic Impact of Prenatal Inflammation and Macrophage Depletion on the Wiring of Neocortical Inhibitory Circuits","volume":"28","author":"Thion","year":"2019","journal-title":"Cell Rep."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1007\/s10856-015-5558-4","article-title":"The overwhelming use of rat models in nerve regeneration research may compromise designs of nerve guidance conduits for humans","volume":"26","author":"Kaplan","year":"2015","journal-title":"J. Mater. Sci. Mater. Med."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/j.conb.2017.03.011","article-title":"A role for GABAergic interneuron diversity in circuit development and plasticity of the neonatal cerebral cortex","volume":"43","author":"Butt","year":"2017","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"395","DOI":"10.3389\/fnhum.2017.00395","article-title":"Reduced Gray Matter Volume in the Social Brain Network in Adults with Autism Spectrum Disorder","volume":"11","author":"Sato","year":"2017","journal-title":"Front. Hum. Neurosci."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.pneurobio.2013.04.001","article-title":"Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species","volume":"106\u2013107","author":"Semple","year":"2013","journal-title":"Prog. Neurobiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.expneurol.2009.10.011","article-title":"Hepatocyte growth factor (HGF) modulates GABAergic inhibition and seizure susceptibility","volume":"221","author":"Bae","year":"2010","journal-title":"Exp. Neurol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/S0896-6273(01)00264-1","article-title":"Hepatocyte Growth Factor\/Scatter Factor Is a Motogen for Interneurons Migrating from the Ventral to Dorsal Telencephalon","volume":"30","author":"Powell","year":"2001","journal-title":"Neuron"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1016\/j.neuron.2005.01.043","article-title":"GDNF and GFR\u03b11 Promote Differentiation and Tangential Migration of Cortical GABAergic Neurons","volume":"45","author":"Pozas","year":"2005","journal-title":"Neuron"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"10695","DOI":"10.1523\/JNEUROSCI.2658-09.2009","article-title":"Regionalized Loss of Parvalbumin Interneurons in the Cerebral Cortex of Mice with Deficits in GFR\u03b11 Signaling","volume":"29","author":"Canty","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.neuron.2014.06.007","article-title":"Neuregulin-ERBB signaling in the nervous system and neuropsychiatric diseases","volume":"83","author":"Mei","year":"2014","journal-title":"Neuron"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"742","DOI":"10.1111\/j.1460-9568.2009.06870.x","article-title":"IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone","volume":"30","author":"Bulfone","year":"2009","journal-title":"Eur. J. Neurosci."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"2633","DOI":"10.1242\/dev.034439","article-title":"Differential effects of BMP signaling on parvalbumin and somatostatin interneuron differentiation","volume":"136","author":"Mukhopadhyay","year":"2009","journal-title":"Development"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"134615","DOI":"10.1016\/j.neulet.2019.134615","article-title":"The cerebral cortex is a substrate of multiple interactions between GABAergic interneurons and oligodendrocyte lineage cells","volume":"715","author":"Benamer","year":"2020","journal-title":"Neurosci. Lett."},{"key":"ref_84","doi-asserted-by":"crossref","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":"ref_85","first-page":"1951","article-title":"Mouse Models of Periventricular Leukomalacia","volume":"39","author":"Shen","year":"2010","journal-title":"J. Vis. Exp."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/j.ejcb.2009.02.001","article-title":"Intranasal delivery of cells to the brain","volume":"88","author":"Danielyan","year":"2009","journal-title":"Eur. J. Cell Biol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1111\/j.1601-183X.2004.00071.x","article-title":"Automated apparatus for quantitation of social approach behaviors in mice","volume":"3","author":"Nadler","year":"2004","journal-title":"Genes Brain Behav."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/1\/211\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:46:54Z","timestamp":1760179614000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/1\/211"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,12,28]]},"references-count":87,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,1]]}},"alternative-id":["ijms22010211"],"URL":"https:\/\/doi.org\/10.3390\/ijms22010211","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,12,28]]}}}