{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,15]],"date-time":"2026-05-15T05:56:39Z","timestamp":1778824599574,"version":"3.51.4"},"reference-count":52,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2021,7,1]],"date-time":"2021-07-01T00:00:00Z","timestamp":1625097600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2021,7,1]],"date-time":"2021-07-01T00:00:00Z","timestamp":1625097600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2021,5,20]],"date-time":"2021-05-20T00:00:00Z","timestamp":1621468800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Journal of Neuroscience Methods"],"published-print":{"date-parts":[[2021,7]]},"DOI":"10.1016\/j.jneumeth.2021.109223","type":"journal-article","created":{"date-parts":[[2021,5,15]],"date-time":"2021-05-15T11:01:30Z","timestamp":1621076490000},"page":"109223","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":10,"special_numbering":"C","title":["Simultaneous flow cytometric characterization of multiple cell types and metabolic states in the rat brain after repeated mild traumatic brain injury"],"prefix":"10.1016","volume":"359","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0618-3173","authenticated-orcid":false,"given":"Chidozie C.","family":"Anyaegbu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yilin","family":"Mao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Terry","family":"McGonigle","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2210-0593","authenticated-orcid":false,"given":"Sushmitha","family":"Raja","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5975-2018","authenticated-orcid":false,"given":"Thomas","family":"Clarke","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7762-9809","authenticated-orcid":false,"given":"Tanya","family":"Solomon","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna M.B.","family":"Black","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3462-7501","authenticated-orcid":false,"given":"Kathy","family":"Fuller","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4823-8179","authenticated-orcid":false,"given":"Melinda","family":"Fitzgerald","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"78","reference":[{"key":"10.1016\/j.jneumeth.2021.109223_bib0005","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1126\/science.aat0473","article-title":"Glia as architects of central nervous system formation and function","volume":"362","author":"Allen","year":"2018","journal-title":"Science"},{"key":"10.1016\/j.jneumeth.2021.109223_bib0010","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.jneumeth.2016.01.025","article-title":"A flow cytometric approach to analyzing mature and progenitor endothelial cells following traumatic brain injury","volume":"263","author":"Assis-Nascimento","year":"2016","journal-title":"J. Neurosci. Methods"},{"issue":"10","key":"10.1016\/j.jneumeth.2021.109223_bib0015","doi-asserted-by":"crossref","first-page":"2892","DOI":"10.1007\/s11064-017-2310-0","article-title":"Flow cytometric characterization of t cell subsets and microglia after repetitive mild traumatic brain injury in rats","volume":"42","author":"Bai","year":"2017","journal-title":"Neurochem. Res."},{"issue":"1","key":"10.1016\/j.jneumeth.2021.109223_bib0020","doi-asserted-by":"crossref","first-page":"e0142520","DOI":"10.1371\/journal.pone.0142520","article-title":"A single 9-colour flow cytometric method to characterise major leukocyte populations in the rat: validation in a model of LPS-induced pulmonary inflammation","volume":"11","author":"Barnett-Vanes","year":"2016","journal-title":"PLoS One"},{"issue":"1\u20132","key":"10.1016\/j.jneumeth.2021.109223_bib0025","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/S0022-1759(00)00229-5","article-title":"A practical approach to multicolor flow cytometry for immunophenotyping","volume":"243","author":"Baumgarth","year":"2000","journal-title":"J. Immunol. Methods"},{"issue":"2","key":"10.1016\/j.jneumeth.2021.109223_bib0030","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1017\/S1355617709991287","article-title":"Neuropsychological performance following a history of multiple self-reported concussions: a meta-analysis","volume":"16","author":"Belanger","year":"2010","journal-title":"J. Int. Neuropsychol. Soc."},{"key":"10.1016\/j.jneumeth.2021.109223_bib0035","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/j.it.2012.02.010","article-title":"A deep profiler\u2019s guide to cytometry","volume":"33","author":"Bendall","year":"2012","journal-title":"Trends Immunol."},{"key":"10.1016\/j.jneumeth.2021.109223_bib0040","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.jneumeth.2018.04.005","article-title":"Flow cytometry for receptor analysis from ex-vivo brain tissue in adult rat","volume":"304","author":"Benoit","year":"2018","journal-title":"J. Neurosci. Methods"},{"issue":"2","key":"10.1016\/j.jneumeth.2021.109223_bib0045","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1111\/jnc.13745","article-title":"The oligodendrocyte-specific antibody \u2018CC1\u2019 binds quaking 7","volume":"139","author":"Bin","year":"2016","journal-title":"J. Neurochem."},{"key":"10.1016\/j.jneumeth.2021.109223_bib0050","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.ibror.2019.12.004","article-title":"Dissociation of neonatal and adult mice brain for simultaneous analysis of microglia, astrocytes and infiltrating lymphocytes by flow cytometry","volume":"8","author":"Calvo","year":"2020","journal-title":"IBRO Rep."},{"issue":"2","key":"10.1016\/j.jneumeth.2021.109223_bib0055","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1161\/hs0202.103399","article-title":"Flow cytometric analysis of inflammatory cells in ischemic rat brain","volume":"33","author":"Campanella","year":"2002","journal-title":"Stroke"},{"key":"10.1016\/j.jneumeth.2021.109223_bib0060","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1007\/s11481-009-9164-4","article-title":"Heterogeneity of microglial activation in the innate immune response in the brain","volume":"4","author":"Colton","year":"2009","journal-title":"J. Neuroimmune Pharmacol."},{"issue":"2","key":"10.1016\/j.jneumeth.2021.109223_bib0065","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1038\/84701","article-title":"11-color, 13-parameter flow cytometry: Identification of human naive T cells by phenotype, function, and T-cell receptor diversity","volume":"7","author":"De Rosa","year":"2001","journal-title":"Nat. Med."},{"issue":"4","key":"10.1016\/j.jneumeth.2021.109223_bib0070","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1111\/j.1471-4159.2006.04162.x","article-title":"Macrophages are comprised of resident brain microglia not infiltrating peripheral monocytes acutely after neonatal stroke","volume":"100","author":"Denker","year":"2007","journal-title":"J. Neurochem."},{"issue":"7","key":"10.1016\/j.jneumeth.2021.109223_bib0075","doi-asserted-by":"crossref","first-page":"1040","DOI":"10.1089\/neu.2018.6019","article-title":"Sex differences in acute neuroinflammation after experimental traumatic brain injury are mediated by infiltrating myeloid cells","volume":"36","author":"Doran","year":"2019","journal-title":"J. Neurotrauma"},{"issue":"1","key":"10.1016\/j.jneumeth.2021.109223_bib0080","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1186\/s12974-020-01860-y","article-title":"Evaluation of M2-like macrophage enrichment after diffuse traumatic brain injury through transient interleukin-4 expression from engineered mesenchymal stromal cells","volume":"17","author":"Enam","year":"2020","journal-title":"J. Neuroinflammation"},{"key":"10.1016\/j.jneumeth.2021.109223_bib0085","doi-asserted-by":"crossref","first-page":"84","DOI":"10.3389\/fninf.2018.00084","article-title":"A cell atlas for the mouse brain","volume":"12","author":"Er\u00f6","year":"2018","journal-title":"Front. Neuroinform."},{"issue":"38","key":"10.1016\/j.jneumeth.2021.109223_bib0090","doi-asserted-by":"crossref","first-page":"9962","DOI":"10.1523\/JNEUROSCI.1898-15.2016","article-title":"Interfering with the chronic immune response rescues chronic degeneration after traumatic brain injury","volume":"36","author":"Ert\u00fcrk","year":"2016","journal-title":"J. Neurosci."},{"issue":"153","key":"10.1016\/j.jneumeth.2021.109223_bib0095","article-title":"Simultaneous flow cytometric characterization of multiple cell types retrieved from mouse brain\/spinal cord through different homogenization methods","volume":"2019","author":"Estevez","year":"2019","journal-title":"J. Vis. Exp."},{"issue":"7","key":"10.1016\/j.jneumeth.2021.109223_bib0100","doi-asserted-by":"crossref","first-page":"1131","DOI":"10.1177\/0963689717714092","article-title":"Repeated mild traumatic brain injury: potential mechanisms of damage","volume":"26","author":"Fehily","year":"2017","journal-title":"Cell Transplant."},{"issue":"5","key":"10.1016\/j.jneumeth.2021.109223_bib0105","doi-asserted-by":"crossref","first-page":"660","DOI":"10.1111\/jnc.14673","article-title":"Differential responses to increasing numbers of mild traumatic brain injury in a rodent closed-head injury model","volume":"149","author":"Fehily","year":"2019","journal-title":"J. Neurochem."},{"key":"10.1016\/j.jneumeth.2021.109223_bib0110","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1089\/neu.2009.1112","article-title":"Early events of secondary degeneration after partial optic nerve transection: an immunohistochemical study","volume":"27","author":"Fitzgerald","year":"2010","journal-title":"J. Neurotrauma"},{"issue":"2","key":"10.1016\/j.jneumeth.2021.109223_bib0115","doi-asserted-by":"crossref","first-page":"42","DOI":"10.32607\/20758251-2015-7-2-42-47","article-title":"NeuN as a neuronal nuclear antigen and neuron differentiation marker","volume":"7","author":"Gusel\u2019nikova","year":"2015","journal-title":"Acta Naturae"},{"issue":"1","key":"10.1016\/j.jneumeth.2021.109223_bib0120","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.neuro.2012.10.015","article-title":"Disrupted cytoskeletal homeostasis, astrogliosis and apoptotic cell death in the cerebellum of preweaning rats injected with diphenyl ditelluride","volume":"34","author":"Heimfarth","year":"2013","journal-title":"NeuroToxicology"},{"key":"10.1016\/j.jneumeth.2021.109223_bib0125","first-page":"206","volume":"2","author":"Iannaccone","year":"2009"},{"key":"10.1016\/j.jneumeth.2021.109223_bib0130","series-title":"Maternal Immune Activation Evoked by Polyinosinic: Polycytidylic Acid Does Not Evoke Microglial Cell Activation in the Embryo","author":"Kato","year":"2015"},{"issue":"8","key":"10.1016\/j.jneumeth.2021.109223_bib0135","doi-asserted-by":"crossref","DOI":"10.15252\/embr.201846182","article-title":"Infection with the dengue RNA virus activates TLR9 signaling in human dendritic cells","volume":"19","author":"Lai","year":"2018","journal-title":"EMBO Rep."},{"issue":"1","key":"10.1016\/j.jneumeth.2021.109223_bib0140","first-page":"1","article-title":"Summary for policymakers","volume":"10","author":"Launer","year":"2015","journal-title":"Clim. Change 2013 \u2013 Phys. Sci. Basis"},{"key":"10.1016\/j.jneumeth.2021.109223_bib0145","doi-asserted-by":"crossref","first-page":"2909","DOI":"10.1093\/cercor\/bhn051","article-title":"Members of the NuRD chromatin remodeling complex interact with AUF1 in developing cortical neurons","volume":"18","author":"Lee","year":"2008","journal-title":"Cerebral Cortex December"},{"key":"10.1016\/j.jneumeth.2021.109223_bib0150","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.jneumeth.2015.03.021","article-title":"An optimized method to process mouse CNS to simultaneously analyze neural cells and leukocytes by flow cytometry","volume":"247","author":"Legroux","year":"2015","journal-title":"J. Neurosci. Methods"},{"issue":"5","key":"10.1016\/j.jneumeth.2021.109223_bib0155","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1002\/glia.22953","article-title":"Traumatically injured astrocytes release a proteomic signature modulated by STAT3-dependent cell survival","volume":"64","author":"Levine","year":"2016","journal-title":"GLIA"},{"issue":"9","key":"10.1016\/j.jneumeth.2021.109223_bib0160","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1002\/cyto.a.20333","article-title":"Flow cytometry controls, instrument setup, and the determination of positivity","volume":"69","author":"Maecker","year":"2006","journal-title":"Cytom. Part A"},{"issue":"6","key":"10.1016\/j.jneumeth.2021.109223_bib0165","doi-asserted-by":"crossref","DOI":"10.1523\/ENEURO.0212-17.2017","article-title":"Cross-laboratory analysis of brain cell type transcriptomes with applications to interpretation of bulk tissue data","volume":"4","author":"Mancarci","year":"2017","journal-title":"ENeuro"},{"issue":"11","key":"10.1016\/j.jneumeth.2021.109223_bib0170","doi-asserted-by":"crossref","first-page":"3408","DOI":"10.3390\/ijms19113408","article-title":"The effects of a combination of ion channel inhibitors in female rats following repeated mild traumatic brain injury","volume":"19","author":"Mao","year":"2018","journal-title":"Int. J. Mol. Sci."},{"issue":"2","key":"10.1016\/j.jneumeth.2021.109223_bib0175","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1021\/acschemneuro.6b00374","article-title":"Neurocytometry: flow cytometric sorting of specific neuronal populations from human and rodent brain","volume":"8","author":"Martin","year":"2017","journal-title":"ACS Chem. Neurosci."},{"key":"10.1016\/j.jneumeth.2021.109223_bib0180","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.ijpsycho.2017.09.019","article-title":"Long-term effects of sport concussion on cognitive and motor performance: a review","volume":"132","author":"Martini","year":"2018","journal-title":"Int. J. Psychophysiol."},{"issue":"4","key":"10.1016\/j.jneumeth.2021.109223_bib0185","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1001\/jama.2017.8334","article-title":"Clinicopathological evaluation of chronic traumatic encephalopathy in players of American football","volume":"318","author":"Mez","year":"2017","journal-title":"JAMA \u2013 J. Am. Med. Assoc."},{"issue":"1","key":"10.1016\/j.jneumeth.2021.109223_bib0190","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1186\/2040-7378-4-20","article-title":"Isolation of inflammatory cells from rat brain tissue after stroke","volume":"4","author":"M\u00f6ller","year":"2012","journal-title":"Exp. Transl. Stroke Med."},{"key":"10.1016\/j.jneumeth.2021.109223_bib0195","series-title":"Children and Infants-acute Management of Head Injury Summary Basic Clinical Practice Guidelines for the Acute Treatment of Infants and Children with Head Injury. North Sydney","author":"NSW Dept. of Health","year":"2011"},{"key":"10.1016\/j.jneumeth.2021.109223_bib0200","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.expneurol.2014.06.007","article-title":"Reactive species and oxidative stress in optic nerve vulnerable to secondary degeneration","volume":"261","author":"O\u2019Hare Doig","year":"2014","journal-title":"Exp. Neurol."},{"key":"10.1016\/j.jneumeth.2021.109223_bib0205","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1038\/nri1416","article-title":"Seventeen-colour flow cytometry: Unravelling the immune system","volume":"4","author":"Perfetto","year":"2004","journal-title":"Nat. Rev. Immunol."},{"issue":"8","key":"10.1016\/j.jneumeth.2021.109223_bib0210","doi-asserted-by":"crossref","first-page":"1158","DOI":"10.1212\/WNL.55.8.1158","article-title":"Documented head injury in early adulthood and risk of Alzheimer\u2019s disease and other dementias","volume":"55","author":"Plassman","year":"2000","journal-title":"Neurology"},{"issue":"108","key":"10.1016\/j.jneumeth.2021.109223_bib0215","first-page":"53658","article-title":"Isolation and flow cytometric analysis of immune cells from the ischemic mouse brain","volume":"2016","author":"P\u00f6sel","year":"2016","journal-title":"J. Vis. Exp."},{"issue":"9","key":"10.1016\/j.jneumeth.2021.109223_bib0220","doi-asserted-by":"crossref","first-page":"e107649","DOI":"10.1371\/journal.pone.0107649","article-title":"Characterization of oligodendroglial populations in mouse demyelinating disease using flow cytometry: clues for MS pathogenesis","volume":"9","author":"Robinson","year":"2014","journal-title":"PLoS One"},{"issue":"1","key":"10.1016\/j.jneumeth.2021.109223_bib0225","first-page":"1.14.1","article-title":"Compensation in flow cytometry","volume":"22","author":"Roederer","year":"2002","journal-title":"Curr. Protoc. Cytom."},{"issue":"9","key":"10.1016\/j.jneumeth.2021.109223_bib0230","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1080\/00207450590934570","article-title":"Distribution of GFAP+ astrocytes in adult and neonatal rat brain","volume":"115","author":"Taft","year":"2005","journal-title":"Int. J. Neurosci."},{"issue":"1","key":"10.1016\/j.jneumeth.2021.109223_bib0235","doi-asserted-by":"crossref","first-page":"11991","DOI":"10.1038\/s41598-020-68770-0","article-title":"High-resolution and differential analysis of rat microglial markers in traumatic brain injury: conventional flow cytometric and bioinformatics analysis","volume":"10","author":"Toledano Furman","year":"2020","journal-title":"Sci. Rep."},{"issue":"3","key":"10.1016\/j.jneumeth.2021.109223_bib0240","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1097\/SHK.0000000000000291","article-title":"Differential activation of infiltrating monocyte-derived cells after mild and severe traumatic brain injury","volume":"43","author":"Trahanas","year":"2015","journal-title":"Shock"},{"issue":"3","key":"10.1016\/j.jneumeth.2021.109223_bib0245","doi-asserted-by":"crossref","first-page":"2199","DOI":"10.3892\/ol.2016.4209","article-title":"Development of a standardized flow cytometric method to conduct longitudinal analyses of intracellular CD3\u03b6 expression in patients with head and neck cancer","volume":"11","author":"Upreti","year":"2016","journal-title":"Oncol. Lett."},{"issue":"3","key":"10.1016\/j.jneumeth.2021.109223_bib0250","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/S0304-3940(98)00813-1","article-title":"Immunocytochemical evidence for a distinct GFAP-negative subpopulation of astrocytes in the adult rat hippocampus","volume":"257","author":"Walz","year":"1998","journal-title":"Neurosci. Lett."},{"issue":"5","key":"10.1016\/j.jneumeth.2021.109223_bib0255","doi-asserted-by":"crossref","first-page":"e0178013","DOI":"10.1371\/journal.pone.0178013","article-title":"Therapeutic benefits of phosphodiesterase 4B inhibition after traumatic brain injury","volume":"12","author":"Wilson","year":"2017","journal-title":"PLoS One"},{"issue":"7","key":"10.1016\/j.jneumeth.2021.109223_bib0260","doi-asserted-by":"crossref","first-page":"2133","DOI":"10.1007\/s00221-017-4958-8","article-title":"Repeated mild traumatic brain injury in female rats increases lipid peroxidation in neurons","volume":"235","author":"Yates","year":"2017","journal-title":"Exp. Brain Res."}],"container-title":["Journal of Neuroscience Methods"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0165027021001588?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0165027021001588?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,28]],"date-time":"2025-09-28T00:57:48Z","timestamp":1759021068000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0165027021001588"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7]]},"references-count":52,"alternative-id":["S0165027021001588"],"URL":"https:\/\/doi.org\/10.1016\/j.jneumeth.2021.109223","relation":{},"ISSN":["0165-0270"],"issn-type":[{"value":"0165-0270","type":"print"}],"subject":[],"published":{"date-parts":[[2021,7]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Simultaneous flow cytometric characterization of multiple cell types and metabolic states in the rat brain after repeated mild traumatic brain injury","name":"articletitle","label":"Article Title"},{"value":"Journal of Neuroscience Methods","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.jneumeth.2021.109223","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2021 The Authors. Published by Elsevier B.V.","name":"copyright","label":"Copyright"}],"article-number":"109223"}}