{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T21:08:20Z","timestamp":1791925700154,"version":"4.3.4"},"reference-count":78,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2022,12,28]],"date-time":"2022-12-28T00:00:00Z","timestamp":1672185600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["KO8NS096115"],"award-info":[{"award-number":["KO8NS096115"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"name":"JHU-SOM Innovation","award":["KO8NS096115"],"award-info":[{"award-number":["KO8NS096115"]}]},{"name":"The Thomas Wilson Foundation","award":["KO8NS096115"],"award-info":[{"award-number":["KO8NS096115"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Neonatal hypoxic-ischemic (HI) injury leads to deficits in hippocampal parvalbumin (PV)+ interneurons (INs) and working memory. Therapeutic hypothermia (TH) does not prevent these deficits. ErbB4 supports maturation and maintenance of PV+ IN. Thus, we hypothesized that neonatal HI leads to persistent deficits in PV+ INs, working memory and synaptic plasticity associated with ErbB4 dysregulation despite TH. P10 HI-injured mice were randomized to normothermia (NT, 36 \u00b0C) or TH (31 \u00b0C) for 4 h and compared to sham. Hippocampi were studied for \u03b1-fodrin, glial fibrillary acidic protein (GFAP), and neuroregulin (Nrg) 1 levels; erb-b2 receptor tyrosine kinase 4 (ErbB4)\/ Ak strain transforming (Akt) activation; and PV, synaptotagmin (Syt) 2, vesicular-glutamate transporter (VGlut) 2, Nrg1, and ErbB4 expression in coronal sections. Extracellular field potentials and behavioral testing were performed. At P40, deficits in PV+ INs correlated with impaired memory and coincided with blunted long-term depression (LTD), heightened long-term potentiation (LTP) and increased Vglut2\/Syt2 ratio, supporting excitatory-inhibitory (E\/I) imbalance. Hippocampal Nrg1 levels were increased in the hippocampus 24 h after neonatal HI, delaying the decline documented in shams. Paradoxically ErbB4 activation decreased 24 h and again 30 days after HI. Neonatal HI leads to persistent deficits in hippocampal PV+ INs, memory, and synaptic plasticity. While acute decreased ErbB4 activation supports impaired maturation and survival after HI, late deficit reemergence may impair PV+ INs maintenance after HI.<\/jats:p>","DOI":"10.3390\/ijms24010508","type":"journal-article","created":{"date-parts":[[2022,12,28]],"date-time":"2022-12-28T08:38:19Z","timestamp":1672216699000},"page":"508","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Dysregulation of ErbB4 Signaling Pathway in the Dorsal Hippocampus after Neonatal Hypoxia-Ischemia and Late Deficits in PV+ Interneurons, Synaptic Plasticity and Working Memory"],"prefix":"10.3390","volume":"24","author":[{"given":"Harisa","family":"Spahic","sequence":"first","affiliation":[{"name":"Division of Neonatology, Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2549-699X","authenticated-orcid":false,"given":"Pritika","family":"Parmar","sequence":"additional","affiliation":[{"name":"Mind-Brain Institute, Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3470-8798","authenticated-orcid":false,"given":"Sarah","family":"Miller","sequence":"additional","affiliation":[{"name":"Division of Neonatology, Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul Casey","family":"Emerson","sequence":"additional","affiliation":[{"name":"Mind-Brain Institute, Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4695-7644","authenticated-orcid":false,"given":"Charles","family":"Lechner","sequence":"additional","affiliation":[{"name":"Division of Neonatology, Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark","family":"St. Pierre","sequence":"additional","affiliation":[{"name":"Division of Neonatology, Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neetika","family":"Rastogi","sequence":"additional","affiliation":[{"name":"Mind-Brain Institute, Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Nugent","sequence":"additional","affiliation":[{"name":"Division of Neonatology, Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3362-6021","authenticated-orcid":false,"given":"Sarah Ann","family":"Duck","sequence":"additional","affiliation":[{"name":"Department of Molecular and Cellular Biology, Johns Hopkins University, Baltimore, MD 21205, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alfredo","family":"Kirkwood","sequence":"additional","affiliation":[{"name":"Mind-Brain Institute, Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0788-8028","authenticated-orcid":false,"given":"Raul","family":"Chavez-Valdez","sequence":"additional","affiliation":[{"name":"Division of Neonatology, Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,12,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"712","DOI":"10.1016\/j.neuron.2012.12.020","article-title":"Enhanced intrinsic excitability in basket cells maintains excitatory-inhibitory balance in hippocampal circuits","volume":"77","author":"Campanac","year":"2013","journal-title":"Neuron"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"6436","DOI":"10.1007\/s12035-019-1526-1","article-title":"Perineuronal Nets Restrict the Induction of Long-Term Depression in the Mouse Hippocampal CA1 Region","volume":"56","author":"Khoo","year":"2019","journal-title":"Mol. Neurobiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"4395","DOI":"10.1038\/s41467-020-18074-8","article-title":"Interneuron-specific plasticity at parvalbumin and somatostatin inhibitory synapses onto CA1 pyramidal neurons shapes hippocampal output","volume":"11","author":"Udakis","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1023\/A:1012324231897","article-title":"Hippocampal GABAergic interneurons: A physiological perspective","volume":"26","year":"2001","journal-title":"Neurochem. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1038\/aps.2017.172","article-title":"GABAergic inhibitory neurons as therapeutic targets for cognitive impairment in schizophrenia","volume":"39","author":"Xu","year":"2018","journal-title":"Acta Pharmacol. Sin."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1002\/hipo.22965","article-title":"Delayed injury of hippocampal interneurons after neonatal hypoxia-ischemia and therapeutic hypothermia in a murine model","volume":"28","author":"Emerson","year":"2018","journal-title":"Hippocampus"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1177\/0271678X20942707","article-title":"Accumulation of PSA-NCAM marks nascent neurodegeneration in the dorsal hippocampus after neonatal hypoxic-ischemic brain injury in mice","volume":"41","author":"Lechner","year":"2021","journal-title":"J. Cereb. Blood Flow Metab. Off. J. Int. Soc. Cereb. Blood Flow Metab."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"105222","DOI":"10.1016\/j.nbd.2020.105222","article-title":"Sex specific correlation between GABAergic disruption in the dorsal hippocampus and flurothyl seizure susceptibility after neonatal hypoxic-ischemic brain injury","volume":"148","author":"Lechner","year":"2021","journal-title":"Neurobiol. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Burnsed, J.C., Chavez-Valdez, R., Hossain, M.S., Kesavan, K., Martin, L.J., Zhang, J., and Northington, F.J. (2015). Hypoxia-ischemia and therapeutic hypothermia in the neonatal mouse brain\u2014A longitudinal study. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0118889"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1159\/000454949","article-title":"Therapeutic Hypothermia Provides Variable Protection against Behavioral Deficits after Neonatal Hypoxia-Ischemia: A Potential Role for Brain-Derived Neurotrophic Factor","volume":"39","author":"Diaz","year":"2017","journal-title":"Dev. Neurosci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1159\/000497056","article-title":"Calbindin-1 Expression in the Hippocampus following Neonatal Hypoxia-Ischemia and Therapeutic Hypothermia and Deficits in Spatial Memory","volume":"40","author":"Sanabria","year":"2018","journal-title":"Dev. Neurosci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1056\/NEJMoa1315788","article-title":"Effects of Hypothermia for Perinatal Asphyxia on Childhood Outcomes","volume":"371","author":"Azzopardi","year":"2014","journal-title":"N. Engl. J. Med."},{"key":"ref_13","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_14","doi-asserted-by":"crossref","first-page":"7288","DOI":"10.1523\/JNEUROSCI.23-19-07288.2003","article-title":"Presynaptic and postsynaptic mechanisms of a novel form of homosynaptic potentiation at aplysia sensory-motor neuron synapses","volume":"23","author":"Jin","year":"2003","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1016\/j.neuron.2005.01.043","article-title":"GDNF and GFRalpha1 promote differentiation and tangential migration of cortical GABAergic neurons","volume":"45","author":"Pozas","year":"2005","journal-title":"Neuron"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1376","DOI":"10.1038\/nature08928","article-title":"Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling","volume":"464","author":"Fazzari","year":"2010","journal-title":"Nature"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1093\/cercor\/13.3.252","article-title":"Neural development of the neuregulin receptor ErbB4 in the cerebral cortex and the hippocampus: Preferential expression by interneurons tangentially migrating from the ganglionic eminences","volume":"13","author":"Yau","year":"2003","journal-title":"Cereb. Cortex"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/1749-8104-7-10","article-title":"Neuregulin repellent signaling via ErbB4 restricts GABAergic interneurons to migratory paths from ganglionic eminence to cortical destinations","volume":"7","author":"Li","year":"2012","journal-title":"Neural Dev."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/j.neuron.2004.09.028","article-title":"Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1","volume":"44","author":"Flames","year":"2004","journal-title":"Neuron"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1038\/nrn2392","article-title":"Neuregulin 1 in neural development, synaptic plasticity and schizophrenia","volume":"9","author":"Mei","year":"2008","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.neuroscience.2015.08.047","article-title":"Neuregulin 1 protects against ischemic brain injury via ErbB4 receptors by increasing GABAergic transmission","volume":"307","author":"Guan","year":"2015","journal-title":"Neuroscience"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"21818","DOI":"10.1073\/pnas.1010669107","article-title":"ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation","volume":"107","author":"Chen","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s12993-014-0050-8","article-title":"Neuregulin1\u03b2 improves cognitive dysfunction and up-regulates expression of p-ERK1\/2 in rats with chronic omethoate poisoning","volume":"11","author":"Rong","year":"2015","journal-title":"Behav. Brain Funct. BBF"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"12255","DOI":"10.1523\/JNEUROSCI.2454-09.2009","article-title":"Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus","volume":"29","author":"Vullhorst","year":"2009","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.cell.2006.01.042","article-title":"Tangential neuronal migration controls axon guidance: A role for neuregulin-1 in thalamocortical axon navigation","volume":"125","author":"Cautinat","year":"2006","journal-title":"Cell"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/j.neuron.2007.03.028","article-title":"The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity","volume":"54","author":"Li","year":"2007","journal-title":"Neuron"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1016\/j.neuron.2007.04.009","article-title":"Neuregulin-1 enhances depolarization-induced GABA release","volume":"54","author":"Woo","year":"2007","journal-title":"Neuron"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"32944","DOI":"10.1074\/jbc.M800073200","article-title":"ErbB4-neuregulin signaling modulates synapse development and dendritic arborization through distinct mechanisms","volume":"283","author":"Krivosheya","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1038\/mp.2011.35","article-title":"Control of interneuron dendritic growth through NRG1\/erbB4-mediated kalirin-7 disinhibition","volume":"17","author":"Cahill","year":"2012","journal-title":"Mol. Psychiatry"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2482","DOI":"10.1002\/cne.24506","article-title":"Ablation of ErbB4 in parvalbumin-positive interneurons inhibits adult hippocampal neurogenesis through down-regulating BDNF\/TrkB expression","volume":"526","author":"Zhang","year":"2018","journal-title":"J. Comp. Neurol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1002\/hipo.20675","article-title":"Selective populations of hippocampal interneurons express ErbB4 and their number and distribution is altered in ErbB4 knockout mice","volume":"20","author":"Neddens","year":"2010","journal-title":"Hippocampus"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1073\/pnas.1719523115","article-title":"Somatostatin and parvalbumin inhibitory synapses onto hippocampal pyramidal neurons are regulated by distinct mechanisms","volume":"115","author":"Horn","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"3351","DOI":"10.1007\/s00221-019-05680-2","article-title":"NRG1-ErbB4 signaling promotes functional recovery in a murine model of traumatic brain injury via regulation of GABA release","volume":"237","author":"Deng","year":"2019","journal-title":"Exp. Brain Res."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Tucker, L.B., Winston, B.S., Liu, J., Velosky, A.G., Fu, A.H., Grillakis, A.A., and McCabe, J.T. (2019). Sex differences in cued fear responses and parvalbumin cell density in the hippocampus following repetitive concussive brain injuries in C57BL\/6J mice. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0222153"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1159\/000496468","article-title":"Seizure Susceptibility Correlates with Brain Injury in Male Mice Treated with Hypothermia after Neonatal Hypoxia-Ischemia","volume":"40","author":"McNally","year":"2018","journal-title":"Dev. Neurosci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0169-328X(95)00056-X","article-title":"Developmental expression of parvalbumin mRNA in the cerebral cortex and hippocampus of the rat","volume":"32","author":"Soriano","year":"1995","journal-title":"Brain Res. Mol. Brain Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1211","DOI":"10.1073\/pnas.0910302107","article-title":"Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons","volume":"107","author":"Wen","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1523\/JNEUROSCI.2538-10.2011","article-title":"Neuregulin 1 Promotes Excitatory Synapse Development and Function in GABAergic Interneurons","volume":"31","author":"Ting","year":"2011","journal-title":"J. Neurosci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1016\/S0896-6273(00)81176-9","article-title":"Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses","volume":"26","author":"Huang","year":"2000","journal-title":"Neuron"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"37","DOI":"10.3389\/fncir.2018.00037","article-title":"PV Interneurons: Critical Regulators of E\/I Balance for Prefrontal Cortex-Dependent Behavior and Psychiatric Disorders","volume":"12","author":"Ferguson","year":"2018","journal-title":"Front. Neural Circuits"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1038\/s41467-020-20328-4","article-title":"Transcriptional and morphological profiling of parvalbumin interneuron subpopulations in the mouse hippocampus","volume":"12","author":"Que","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"4","DOI":"10.3389\/fncel.2013.00004","article-title":"ErbB1\u20134-dependent EGF\/neuregulin signals and their cross talk in the central nervous system: Pathological implications in schizophrenia and Parkinson\u2019s disease","volume":"7","author":"Iwakura","year":"2013","journal-title":"Front. Cell. Neurosci."},{"key":"ref_43","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_44","doi-asserted-by":"crossref","first-page":"F16","DOI":"10.1136\/fn.86.1.F16","article-title":"Joint association of Apgar scores and early neonatal symptoms with minor disabilities at school age","volume":"86","author":"Moster","year":"2002","journal-title":"Arch. Dis. Child. Fetal Neonatal Ed."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1038\/pr.2011.30","article-title":"Seven- to eight-year follow-up of the CoolCap trial of head cooling for neonatal encephalopathy","volume":"71","author":"Guillet","year":"2012","journal-title":"Pediatr. Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e624","DOI":"10.1542\/peds.2014-1566","article-title":"Cognitive outcomes after neonatal encephalopathy","volume":"135","author":"Pappas","year":"2015","journal-title":"Pediatrics"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2085","DOI":"10.1056\/NEJMoa1112066","article-title":"Childhood Outcomes after Hypothermia for Neonatal Encephalopathy","volume":"366","author":"Shankaran","year":"2012","journal-title":"N. Engl. J. Med."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"15039","DOI":"10.1038\/ncomms15039","article-title":"Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation","volume":"8","author":"Ognjanovski","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"e27868","DOI":"10.7554\/eLife.27868","article-title":"Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation","volume":"6","author":"Xia","year":"2017","journal-title":"eLife"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1038\/mp.2016.151","article-title":"A novel mechanism of memory loss in Alzheimer\u2019s disease mice via the degeneration of entorhinal-CA1 synapses","volume":"23","author":"Yang","year":"2018","journal-title":"Mol. Psychiatry"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1177\/0269881107067097","article-title":"Sub-chronic psychotomimetic phencyclidine induces deficits in reversal learning and alterations in parvalbumin-immunoreactive expression in the rat","volume":"21","author":"Neill","year":"2007","journal-title":"J. Psychopharmacol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e02037","DOI":"10.1016\/j.heliyon.2019.e02037","article-title":"Parvalbumin-positive GABAergic interneurons deficit in the hippocampus in Gunn rats: A possible hyperbilirubinemia-induced animal model of schizophrenia","volume":"5","author":"Hayashida","year":"2019","journal-title":"Heliyon"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2344","DOI":"10.1523\/JNEUROSCI.5419-08.2009","article-title":"A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia","volume":"29","author":"Lodge","year":"2009","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"5116","DOI":"10.1523\/JNEUROSCI.0425-20.2020","article-title":"Inhibitory Parvalbumin Basket Cell Activity is Selectively Reduced during Hippocampal Sharp Wave Ripples in a Mouse Model of Familial Alzheimer\u2019s Disease","volume":"40","author":"Caccavano","year":"2020","journal-title":"J. Neurosci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"175909142092535","DOI":"10.1177\/1759091420925356","article-title":"Loss of Hippocampal Calretinin and Parvalbumin Interneurons in the 5XFAD Mouse Model of Alzheimer\u2019s Disease","volume":"12","author":"Giesers","year":"2020","journal-title":"ASN Neuro"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"327","DOI":"10.3389\/fnagi.2016.00327","article-title":"Phenotypic Alterations in Hippocampal NPY- and PV-Expressing Interneurons in a Presymptomatic Transgenic Mouse Model of Alzheimer\u2019s Disease","volume":"8","author":"Mahar","year":"2017","journal-title":"Front. Aging Neurosci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1007\/BF00308809","article-title":"Neuropathological stageing of Alzheimer-related changes","volume":"82","author":"Braak","year":"1991","journal-title":"Acta Neuropathol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.schres.2011.06.007","article-title":"Hippocampal interneurons are abnormal in schizophrenia","volume":"131","author":"Konradi","year":"2011","journal-title":"Schizophr. Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1038\/nrn1648","article-title":"Cortical inhibitory neurons and schizophrenia","volume":"6","author":"Lewis","year":"2005","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"31","DOI":"10.3389\/fnagi.2016.00031","article-title":"Implications of GABAergic Neurotransmission in Alzheimer\u2019s Disease","volume":"8","author":"Li","year":"2016","journal-title":"Front. Aging Neurosci."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1038\/nn.2583","article-title":"Amyloid-\u03b2\u2013induced neuronal dysfunction in Alzheimer\u2019s disease: From synapses toward neural networks","volume":"13","author":"Palop","year":"2010","journal-title":"Nat. Neurosci."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"609903","DOI":"10.3389\/fnsyn.2020.609903","article-title":"Increased Excitability and Heightened Magnitude of Long-Term Potentiation at Hippocampal CA3\u2013CA1 Synapses in a Mouse Model of Neonatal Hyperoxia Exposure","volume":"12","author":"Ramani","year":"2021","journal-title":"Front. Synaptic Neurosci."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.ijdevneu.2019.03.001","article-title":"Immediate and delayed decrease of long term potentiation and memory deficits after neonatal intermittent hypoxia","volume":"74","author":"Goussakov","year":"2019","journal-title":"Int. J. Dev. Neurosci. Off. J. Int. Soc. Dev. Neurosci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1016\/j.neuron.2016.08.033","article-title":"Neuregulin-1\/ErbB4 Signaling Regulates Visual Cortical Plasticity","volume":"92","author":"Sun","year":"2016","journal-title":"Neuron"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"13105","DOI":"10.1073\/pnas.1811287115","article-title":"Genetic recovery of ErbB4 in adulthood partially restores brain functions in null mice","volume":"115","author":"Wang","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1186\/s13041-020-00686-2","article-title":"Neuregulin-1 inhibits CoCl2-induced upregulation of excitatory amino acid carrier 1 expression and oxidative stress in SH-SY5Y cells and the hippocampus of mice","volume":"13","author":"Kim","year":"2020","journal-title":"Mol. Brain"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"462","DOI":"10.5115\/acb.19.210","article-title":"Neuregulin 1\/ErbB4 signaling attenuates neuronal cell damage under oxygen-glucose deprivation in primary hippocampal neurons","volume":"52","author":"Yoo","year":"2019","journal-title":"Anat. Cell Biol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1007\/s10571-020-00827-0","article-title":"Long-Lasting Actions of Progesterone Protect the Neonatal Brain Following Hypoxia-Ischemia","volume":"40","author":"Fabres","year":"2020","journal-title":"Cell. Mol. Neurobiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1016\/0896-6273(90)90194-K","article-title":"Organization of hindbrain segments in the zebrafish embryo","volume":"4","author":"Trevarrow","year":"1990","journal-title":"Neuron"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1723","DOI":"10.1523\/JNEUROSCI.0878-15.2016","article-title":"Metabotropic Glutamate Receptors Induce a Form of LTP Controlled by Translation and Arc Signaling in the Hippocampus","volume":"36","author":"Wang","year":"2016","journal-title":"J. Neurosci."},{"key":"ref_72","unstructured":"Buccafusco, J.J. (2009). Anxiety-Related Behaviors in Mice. Methods of Behavior Analysis in Neuroscience, CRC Press\/Taylor & Francis. Frontiers in Neuroscience."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S0014-2999(03)01272-X","article-title":"The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: A review","volume":"463","author":"Prut","year":"2003","journal-title":"Eur. J. Pharmacol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.neuroscience.2011.09.040","article-title":"Hippocampal effects of neuronostatin on memory, anxiety-like behavior and food intake in rats","volume":"197","author":"Carlini","year":"2011","journal-title":"Neuroscience"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1007\/s10339-011-0430-z","article-title":"The novel object recognition memory: Neurobiology, test procedure, and its modifications","volume":"13","author":"Antunes","year":"2012","journal-title":"Cogn. Process."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.bbr.2013.07.055","article-title":"Determinants of novel object and location recognition during development","volume":"256","author":"Jablonski","year":"2013","journal-title":"Behav. Brain Res."},{"key":"ref_77","first-page":"8.31.1","article-title":"Examining object location and object recognition memory in mice","volume":"69","author":"Wood","year":"2014","journal-title":"Curr. Protoc. Neurosci."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/978-1-4939-8994-2_10","article-title":"The Y-Maze for Assessment of Spatial Working and Reference Memory in Mice","volume":"1916","author":"Kraeuter","year":"2019","journal-title":"Methods Mol. Biol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/1\/508\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:53:51Z","timestamp":1760147631000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/1\/508"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,28]]},"references-count":78,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,1]]}},"alternative-id":["ijms24010508"],"URL":"https:\/\/doi.org\/10.3390\/ijms24010508","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,28]]}}}