{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,27]],"date-time":"2026-10-27T22:47:06Z","timestamp":1793141226138,"version":"4.5.0"},"reference-count":57,"publisher":"Springer Science and Business Media LLC","issue":"7","license":[{"start":{"date-parts":[[2025,7,25]],"date-time":"2025-07-25T00:00:00Z","timestamp":1753401600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,7,25]],"date-time":"2025-07-25T00:00:00Z","timestamp":1753401600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["2022\/45\/N\/NZ4\/03028"],"award-info":[{"award-number":["2022\/45\/N\/NZ4\/03028"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["2022\/45\/N\/NZ4\/03028"],"award-info":[{"award-number":["2022\/45\/N\/NZ4\/03028"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["2022\/45\/N\/NZ4\/03028"],"award-info":[{"award-number":["2022\/45\/N\/NZ4\/03028"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["2022\/45\/N\/NZ4\/03028"],"award-info":[{"award-number":["2022\/45\/N\/NZ4\/03028"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Brain Struct Funct"],"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:p>Traumatic brain injury (TBI) is one of the most common causes of disability worldwide and a risk factor for the development of post-traumatic epilepsy and mood disorders. Sexual differences in the tissue response to the injury may contribute to the varied pathophysiology of TBI, making it particularly challenging to develop a satisfactory therapy. The aim of this study was to investigate the sexual difference in astrogliosis, microgliosis, and neuronal loss after TBI. Penetrating cortical brain injury was performed in male and female rats that were sacrificed 2, 8, 16, or 30\u00a0days after injury. Glial scar development and neuronal loss were analysed, as well as the morphology of astrocytes and microglia in perilesional cerebral cortex. Increased astrogliosis was observed in females compared to males, including more complex and hypertrophied morphology of astrocytes 2 and 8\u00a0days after TBI, an earlier onset of contralateral astrocytic reaction, and a greater GFAP\u2009+\u2009(glial fibrillary acidic protein) area fraction in perilesional cortex in females 30\u00a0days post-injury. Sex differences in microglia morphology were also observed, such as more complex and ramified microglia in females 2 and 30\u00a0days after TBI. Moreover, an increased loss of parvalbumin- and neuropeptide Y-expressing neurons in perilesional and contralateral cortex was noticed in females compared to males, along with a higher number of cells expressing neuronal nitric oxide synthase. These results suggest a sexual differences in the cellular response to traumatic brain injury, which may contribute to the different outcomes and development of post-traumatic pathologies in males and females.<\/jats:p>","DOI":"10.1007\/s00429-025-02986-6","type":"journal-article","created":{"date-parts":[[2025,7,25]],"date-time":"2025-07-25T05:04:31Z","timestamp":1753419871000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Sex differences in neuropathological response to traumatic brain injury: increased neuronal loss and astrogliosis in females"],"prefix":"10.1007","volume":"230","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6576-0666","authenticated-orcid":false,"given":"Zuzanna","family":"Rauk","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joanna","family":"J\u0119drusik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zofia","family":"Walczak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zuzanna","family":"Setkowicz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,7,25]]},"reference":[{"key":"2986_CR1","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2022.114222","volume":"358","author":"PM Abdul-Muneer","year":"2022","unstructured":"Abdul-Muneer PM, Saikia BB, Bhowmick S (2022) Synergistic effect of mild traumatic brain injury and alcohol aggravates neuroinflammation, amyloidogenesis, tau pathology, neurodegeneration, and blood-brain barrier alterations: Impact on psychological stress. Exp Neurol 358:114222. https:\/\/doi.org\/10.1016\/j.expneurol.2022.114222","journal-title":"Exp Neurol"},{"key":"2986_CR2","doi-asserted-by":"publisher","first-page":"1966","DOI":"10.1002\/glia.22867","volume":"63","author":"E Acaz-Fonseca","year":"2015","unstructured":"Acaz-Fonseca E, Duran JC, Carrero P et al (2015) Sex differences in glia reactivity after cortical brain injury. Glia 63:1966\u20131981. https:\/\/doi.org\/10.1002\/glia.22867","journal-title":"Glia"},{"key":"2986_CR3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fnagi.2014.00132","volume":"6","author":"GE Barreto","year":"2014","unstructured":"Barreto GE, Santos-Galindo M, Garcia-Segura LM (2014) Selective estrogen receptor modulators regulate reactive microglia after penetrating brain injury. Front Aging Neurosci 6:1\u20137. https:\/\/doi.org\/10.3389\/fnagi.2014.00132","journal-title":"Front Aging Neurosci"},{"key":"2986_CR4","doi-asserted-by":"publisher","first-page":"2596","DOI":"10.1210\/en.2018-00220","volume":"159","author":"MR Bell","year":"2018","unstructured":"Bell MR (2018) Comparing postnatal development of gonadal hormones and associated social behaviors in rats, mice, and humans. Endocrinology 159:2596\u20132613. https:\/\/doi.org\/10.1210\/en.2018-00220","journal-title":"Endocrinology"},{"key":"2986_CR5","doi-asserted-by":"publisher","unstructured":"Bhowmick S, Malat A, Caruso D, et al (2021) Intercellular adhesion molecule-1-induced posttraumatic brain injury neuropathology in the prefrontal cortex and hippocampus leads to sensorimotor function deficits and psychological stress. eNeuro 8:1\u201321. https:\/\/doi.org\/10.1523\/ENEURO.0242-21.2021","DOI":"10.1523\/ENEURO.0242-21.2021"},{"key":"2986_CR6","doi-asserted-by":"publisher","first-page":"2306","DOI":"10.1093\/cercor\/bhu041","volume":"25","author":"D Cantu","year":"2015","unstructured":"Cantu D, Walker K, Andresen L et al (2015) Traumatic Brain Injury Increases Cortical Glutamate Network Activity by Compromising GABAergic Control. Cereb Cortex 25:2306\u20132320. https:\/\/doi.org\/10.1093\/cercor\/bhu041","journal-title":"Cereb Cortex"},{"key":"2986_CR7","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1016\/j.neuroscience.2018.07.020","volume":"388","author":"SF Carron","year":"2018","unstructured":"Carron SF, Yan EB, Allitt BJ, Rajan R (2018) Immediate and Medium-term Changes in Cortical and Hippocampal Inhibitory Neuronal Populations after Diffuse TBI. Neuroscience 388:152\u2013170. https:\/\/doi.org\/10.1016\/j.neuroscience.2018.07.020","journal-title":"Neuroscience"},{"key":"2986_CR8","doi-asserted-by":"publisher","DOI":"10.1016\/j.mad.2021.111473","volume":"196","author":"JA Chowen","year":"2021","unstructured":"Chowen JA, Garcia-Segura LM (2021) Role of glial cells in the generation of sex differences in neurodegenerative diseases and brain aging. Mech Ageing Dev 196:111473. https:\/\/doi.org\/10.1016\/j.mad.2021.111473","journal-title":"Mech Ageing Dev"},{"key":"2986_CR9","doi-asserted-by":"publisher","unstructured":"Cieri MB, Villarreal A, Gomez-Cuautle DD, et al (2023) Progression of reactive gliosis and astroglial phenotypic changes following stab wound-induced traumatic brain injury in mice. J Neurochem 167:183\u2013203. https:\/\/doi.org\/10.1111\/jnc.15941","DOI":"10.1111\/jnc.15941"},{"key":"2986_CR10","doi-asserted-by":"publisher","first-page":"528","DOI":"10.1002\/glia.23736","volume":"68","author":"T Cl\u00e9ment","year":"2020","unstructured":"Cl\u00e9ment T, Lee JB, Ichkova A et al (2020) Juvenile mild traumatic brain injury elicits distinct spatiotemporal astrocyte responses. Glia 68:528\u2013542. https:\/\/doi.org\/10.1002\/glia.23736","journal-title":"Glia"},{"key":"2986_CR11","doi-asserted-by":"publisher","unstructured":"Qui\u00f1ones S, Wang JC, Kim E, et al (2024) Cortical inhibitory parvalbumin interneurons exhibit metabolic specializations coordinated by PGC-1\u03b1 that are lost in rodents and humans after traumatic brain injury. bioRxiv 2024.06.19.599637. https:\/\/doi.org\/10.1101\/2024.06.19.599637","DOI":"10.1101\/2024.06.19.599637"},{"key":"2986_CR12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12974-020-1719-6","volume":"17","author":"A Crespo-Castrillo","year":"2020","unstructured":"Crespo-Castrillo A, Garcia-Segura LM, Arevalo MA (2020) The synthetic steroid tibolone exerts sex-specific regulation of astrocyte phagocytosis under basal conditions and after an inflammatory challenge. J Neuroinflammation 17:1\u201314. https:\/\/doi.org\/10.1186\/s12974-020-1719-6","journal-title":"J Neuroinflammation"},{"key":"2986_CR13","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s40659-024-00532-y","volume":"57","author":"LM Delgado-Garc\u00eda","year":"2024","unstructured":"Delgado-Garc\u00eda LM, Ojalvo-Sanz AC, Nakamura TKE et al (2024) Dissecting reactive astrocyte responses: lineage tracing and morphology-based clustering. Biol Res 57:1\u201316. https:\/\/doi.org\/10.1186\/s40659-024-00532-y","journal-title":"Biol Res"},{"key":"2986_CR14","doi-asserted-by":"publisher","first-page":"1080","DOI":"10.3171\/2017.10.JNS17352","volume":"130","author":"MC Dewan","year":"2019","unstructured":"Dewan MC, Rattani A, Gupta S et al (2019) Estimating the global incidence of traumatic brain injury. J Neurosurg 130:1080\u20131097. https:\/\/doi.org\/10.3171\/2017.10.JNS17352","journal-title":"J Neurosurg"},{"key":"2986_CR15","doi-asserted-by":"publisher","first-page":"1040","DOI":"10.1089\/neu.2018.6019","volume":"36","author":"SJ Doran","year":"2019","unstructured":"Doran SJ, Ritzel RM, Glaser EP et al (2019) Sex differences in acute neuroinflammation after experimental traumatic brain injury are mediated by infiltrating myeloid cells. J Neurotrauma 36:1040\u20131053. https:\/\/doi.org\/10.1089\/neu.2018.6019","journal-title":"J Neurotrauma"},{"key":"2986_CR16","doi-asserted-by":"publisher","unstructured":"Fern\u00e1ndez-Arjona M del M, Grondona JM, Granados-Dur\u00e1n P, et al (2017) Microglia morphological categorization in a rat model of neuroinflammation by hierarchical cluster and principal components analysis. Front Cell Neurosci 11:1\u201322. https:\/\/doi.org\/10.3389\/fncel.2017.00235","DOI":"10.3389\/fncel.2017.00235"},{"key":"2986_CR17","doi-asserted-by":"publisher","unstructured":"Koenig JB, Cantu D, Low C, et al (2019) Glycolytic inhibitor 2-deoxyglucose prevents cortical hyperexcitability after traumatic brain injury. https:\/\/doi.org\/10.1101\/479782","DOI":"10.1101\/479782"},{"key":"2986_CR18","doi-asserted-by":"publisher","first-page":"3063","DOI":"10.1089\/neu.2018.6171","volume":"36","author":"R Gupte","year":"2019","unstructured":"Gupte R, Brooks W, Vukas R et al (2019) Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know. J Neurotrauma 36:3063\u20133091. https:\/\/doi.org\/10.1089\/neu.2018.6171","journal-title":"J Neurotrauma"},{"key":"2986_CR19","doi-asserted-by":"publisher","unstructured":"Hall ED, Wang JA, Miller DM (2012) Relationship of nitric oxide synthase induction to peroxynitrite-mediated oxidative damage during the first week after experimental traumatic brain injury. Exp Neurol 238:176\u2013182. https:\/\/doi.org\/10.1016\/j.expneurol.2012.08.024","DOI":"10.1016\/j.expneurol.2012.08.024"},{"key":"2986_CR20","doi-asserted-by":"publisher","first-page":"4070","DOI":"10.1093\/cercor\/bhac327","volume":"33","author":"MQ Hameed","year":"2023","unstructured":"Hameed MQ, Hodgson N, Lee HHC et al (2023) N-acetylcysteine treatment mitigates loss of cortical parvalbumin-positive interneuron and perineuronal net integrity resulting from persistent oxidative stress in a rat TBI model. Cereb Cortex 33:4070\u20134084. https:\/\/doi.org\/10.1093\/cercor\/bhac327","journal-title":"Cereb Cortex"},{"key":"2986_CR21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-021-02849-0","volume":"11","author":"M Har-Even","year":"2021","unstructured":"Har-Even M, Rubovitch V, Ratliff WA et al (2021) Ketogenic Diet as a potential treatment for traumatic brain injury in mice. Sci Rep 11:1\u201312. https:\/\/doi.org\/10.1038\/s41598-021-02849-0","journal-title":"Sci Rep"},{"key":"2986_CR22","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1016\/0006-8993(89)90566-0","volume":"485","author":"K Janeczko","year":"1989","unstructured":"Janeczko K (1989) Spatiotemporal patterns of the astroglial proliferation in rat brain injured at the postmitotic stage of postnatal development: a combined immunocytochemical and autoradiographic study. Brain Res 485:236\u2013243. https:\/\/doi.org\/10.1016\/0006-8993(89)90566-0","journal-title":"Brain Res"},{"key":"2986_CR23","doi-asserted-by":"publisher","first-page":"1646","DOI":"10.1089\/neu.2017.5547","volume":"35","author":"A Jullienne","year":"2018","unstructured":"Jullienne A, Salehi A, Affeldt B et al (2018) Male and Female Mice Exhibit Divergent Responses of the Cortical Vasculature to Traumatic Brain Injury. J Neurotrauma 35:1646\u20131658. https:\/\/doi.org\/10.1089\/neu.2017.5547","journal-title":"J Neurotrauma"},{"key":"2986_CR57","doi-asserted-by":"publisher","unstructured":"Karperien AL, Jelinek HF, Milosevic NT (2011) Reviewing Lacunarity analysis and classification of microglia in neuroscience. Proceedings of the 8th European Conference on Mathematical and Theoretical Biology MS88. https:\/\/doi.org\/10.13140\/2.1.3576.6082","DOI":"10.13140\/2.1.3576.6082"},{"key":"2986_CR24","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fncel.2013.00003","volume":"7","author":"A Karperien","year":"2013","unstructured":"Karperien A, Ahammer H, Jelinek HF (2013) Quantitating the subtleties of microglial morphology with fractal analysis. Front Cell Neurosci 7:1\u201334. https:\/\/doi.org\/10.3389\/fncel.2013.00003","journal-title":"Front Cell Neurosci"},{"key":"2986_CR25","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1007\/s00441-012-1336-5","volume":"349","author":"H Kawano","year":"2012","unstructured":"Kawano H, Kimura-Kuroda J, Komuta Y et al (2012) Role of the lesion scar in the response to damage and repair of the central nervous system. Cell Tissue Res 349:169\u2013180. https:\/\/doi.org\/10.1007\/s00441-012-1336-5","journal-title":"Cell Tissue Res"},{"key":"2986_CR26","doi-asserted-by":"publisher","DOI":"10.1016\/j.saa.2021.120214","volume":"263","author":"K Kawon","year":"2021","unstructured":"Kawon K, Setkowicz Z, Drozdz A et al (2021) The methods of vibrational microspectroscopy reveals long-term biochemical anomalies within the region of mechanical injury within the rat brain. Spectrochim Acta A Mol Biomol Spectrosc 263:120214. https:\/\/doi.org\/10.1016\/j.saa.2021.120214","journal-title":"Spectrochim Acta A Mol Biomol Spectrosc"},{"key":"2986_CR27","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1016\/j.brainres.2010.10.090","volume":"1368","author":"A Keser","year":"2011","unstructured":"Keser A, Balkan B, Gozen O et al (2011) Hippocampal neuronal nitric oxide synthase (nNOS) is regulated by nicotine and stress in female but not in male rats. Brain Res 1368:134\u2013142. https:\/\/doi.org\/10.1016\/j.brainres.2010.10.090","journal-title":"Brain Res"},{"key":"2986_CR28","doi-asserted-by":"publisher","unstructured":"Koh P-O (2014) Estradiol ameliorates the reduction in parvalbumin expression induced by ischemic brain injury. Neurosci Lett 574:36\u201340. https:\/\/doi.org\/10.1016\/j.neulet.2014.05.006","DOI":"10.1016\/j.neulet.2014.05.006"},{"key":"2986_CR29","doi-asserted-by":"publisher","first-page":"2627","DOI":"10.1016\/j.bbadis.2016.12.020","volume":"1863","author":"AV Kozlov","year":"2017","unstructured":"Kozlov AV, Bahrami S, Redl H, Szabo C (2017) Alterations in nitric oxide homeostasis during traumatic brain injury. Biochim Biophys Acta Mol Basis Dis 1863:2627\u20132632. https:\/\/doi.org\/10.1016\/j.bbadis.2016.12.020","journal-title":"Biochim Biophys Acta Mol Basis Dis"},{"key":"2986_CR30","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1038\/sj.jcbfm.9600331","volume":"27","author":"M Liu","year":"2007","unstructured":"Liu M, Hurn PD, Roselli CE, Alkayed NJ (2007) Role of P450 aromatase in sex-specific astrocytic cell death. J Cereb Blood Flow Metab 27:135\u2013141. https:\/\/doi.org\/10.1038\/sj.jcbfm.9600331","journal-title":"J Cereb Blood Flow Metab"},{"key":"2986_CR31","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1016\/j.brainres.2009.09.077","volume":"1314","author":"JC Morales-Medina","year":"2010","unstructured":"Morales-Medina JC, Dumont Y, Quirion R (2010) A possible role of neuropeptide Y in depression and stress. Brain Res 1314:194\u2013205. https:\/\/doi.org\/10.1016\/j.brainres.2009.09.077","journal-title":"Brain Res"},{"key":"2986_CR32","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1016\/j.bbr.2015.03.010","volume":"286","author":"R Mychasiuk","year":"2015","unstructured":"Mychasiuk R, Hehar H, Esser MJ (2015) A mild traumatic brain injury (mTBI) induces secondary attention-deficit hyperactivity disorder-like symptomology in young rats. Behav Brain Res 286:285\u2013292. https:\/\/doi.org\/10.1016\/j.bbr.2015.03.010","journal-title":"Behav Brain Res"},{"key":"2986_CR33","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1016\/j.bbr.2013.10.048","volume":"259","author":"R Mychasiuk","year":"2014","unstructured":"Mychasiuk R, Hehar H, Farran A, Esser MJ (2014) Mean girls: Sex differences in the effects of mild traumatic brain injury on the social dynamics of juvenile rat play behaviour. Behav Brain Res 259:284\u2013291. https:\/\/doi.org\/10.1016\/j.bbr.2013.10.048","journal-title":"Behav Brain Res"},{"key":"2986_CR34","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12974-023-02916-5","volume":"20","author":"KJ Neale","year":"2023","unstructured":"Neale KJ, Reid HMO, Sousa B et al (2023) Repeated mild traumatic brain injury causes sex-specific increases in cell proliferation and inflammation in juvenile rats. J Neuroinflammation 20:1\u201320. https:\/\/doi.org\/10.1186\/s12974-023-02916-5","journal-title":"J Neuroinflammation"},{"key":"2986_CR35","doi-asserted-by":"publisher","first-page":"1277","DOI":"10.1113\/JP275393","volume":"596","author":"J Nichols","year":"2018","unstructured":"Nichols J, Bjorklund GR, Newbern J, Anderson T (2018) Parvalbumin fast-spiking interneurons are selectively altered by paediatric traumatic brain injury. J Physiol 596:1277\u20131293. https:\/\/doi.org\/10.1113\/JP275393","journal-title":"J Physiol"},{"key":"2986_CR36","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1055\/s-0035-1565241","volume":"49","author":"S Ozsoy","year":"2016","unstructured":"Ozsoy S, Olguner Eker O, Abdulrezzak U (2016) The Effects of Antidepressants on Neuropeptide y in Patients with Depression and Anxiety. Pharmacopsychiatry 49:26\u201331. https:\/\/doi.org\/10.1055\/s-0035-1565241","journal-title":"Pharmacopsychiatry"},{"key":"2986_CR37","doi-asserted-by":"publisher","first-page":"987","DOI":"10.1016\/j.neuroscience.2005.07.052","volume":"138","author":"GC Panzica","year":"2006","unstructured":"Panzica GC, Viglietti-Panzica C, Sica M et al (2006) Effects of gonadal hormones on central nitric oxide producing systems. Neuroscience 138:987\u2013995. https:\/\/doi.org\/10.1016\/j.neuroscience.2005.07.052","journal-title":"Neuroscience"},{"key":"2986_CR38","volume-title":"The Rat Brain in Stereotaxic Coordinates","author":"G Paxinos","year":"2007","unstructured":"Paxinos G, Watson C (2007) The Rat Brain in Stereotaxic Coordinates. Elsevier"},{"key":"2986_CR39","doi-asserted-by":"publisher","first-page":"865","DOI":"10.1089\/neu.1999.16.865","volume":"16","author":"VL Raghavendra Rao","year":"1999","unstructured":"Raghavendra Rao VL, Dogan A, Bowen KK, Dempsey RJ (1999) Traumatic injury to rat brain upregulates neuronal nitric oxide synthase expression and l-[3H]nitroarginine binding. J Neurotrauma 16:865\u2013877. https:\/\/doi.org\/10.1089\/neu.1999.16.865","journal-title":"J Neurotrauma"},{"key":"2986_CR40","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1186\/2042-6410-2-7","volume":"2","author":"M Santos-Galindo","year":"2011","unstructured":"Santos-Galindo M, Acaz-Fonseca E, Bellini MJ, Garcia-Segura LM (2011) Sex differences in the inflammatory response of primary astrocytes to lipopolysaccharide. Biol Sex Differ 2:7. https:\/\/doi.org\/10.1186\/2042-6410-2-7","journal-title":"Biol Sex Differ"},{"key":"2986_CR41","doi-asserted-by":"publisher","unstructured":"Schwarz JM, Sholar PW, Bilbo SD (2012) Sex differences in microglial colonization of the developing rat brain. J Neurochem 120:948\u2013963. https:\/\/doi.org\/10.1111\/j.1471-4159.2011.07630.x","DOI":"10.1111\/j.1471-4159.2011.07630.x"},{"key":"2986_CR42","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1111\/j.1399-6576.2009.02125.x","volume":"54","author":"E Semenas","year":"2010","unstructured":"Semenas E, Nozari A, Sharma HS et al (2010) Sex differences in cerebral injury after severe haemorrhage and ventricular fibrillation in pigs. Acta Anaesthesiol Scand 54:343\u2013353. https:\/\/doi.org\/10.1111\/j.1399-6576.2009.02125.x","journal-title":"Acta Anaesthesiol Scand"},{"key":"2986_CR43","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1016\/S0920-1211(03)00029-9","volume":"53","author":"Z Setkowicz","year":"2003","unstructured":"Setkowicz Z, Janeczko K (2003) Long-term changes in susceptibility to pilocarpine-induced status epilepticus following neocortical injuries in the rat at different developmental stages. Epilepsy Res 53:216\u2013224. https:\/\/doi.org\/10.1016\/S0920-1211(03)00029-9","journal-title":"Epilepsy Res"},{"key":"2986_CR44","doi-asserted-by":"publisher","unstructured":"Setkowicz Z, Kosonowska E, Kaczy\u0144ska M, et al (2016) Physical training decreases susceptibility to pilocarpine-induced seizures in the injured rat brain. Brain Res 1642:20\u201332. https:\/\/doi.org\/10.1016\/j.brainres.2016.03.008","DOI":"10.1016\/j.brainres.2016.03.008"},{"key":"2986_CR45","doi-asserted-by":"crossref","unstructured":"Tucker LB, Winston BS, Liu J, et al (2019) Sex differences in cued fear responses and parvalbumin cell density in the hippocampus following repetitive concussive brain injuries in C57BL\/6J mice","DOI":"10.1371\/journal.pone.0222153"},{"key":"2986_CR46","doi-asserted-by":"publisher","unstructured":"Sharma HS, Wiklund L, Badgaiyan RD, et al (2006) Intracerebral administration of neuronal nitric oxide synthase antiserum attenuates traumatic brain injury-induced blood-brain barrier permeability, brain edema formation, and sensory motor disturbances in the rat. Acta Neurochir Suppl (Wien) 288\u2013294. https:\/\/doi.org\/10.1007\/3-211-30714-1_62","DOI":"10.1007\/3-211-30714-1_62"},{"key":"2986_CR47","doi-asserted-by":"publisher","first-page":"3672","DOI":"10.1073\/pnas.97.7.3672","volume":"97","author":"R Singh","year":"2000","unstructured":"Singh R, Pervin S, Shryne J et al (2000) Castration increases and androgens decrease nitric oxide synthase activity in the brain: Physiologic implications. Proc Natl Acad Sci U S A 97:3672\u20133677. https:\/\/doi.org\/10.1073\/pnas.97.7.3672","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2986_CR48","doi-asserted-by":"publisher","first-page":"638","DOI":"10.1016\/j.tins.2009.08.002","volume":"32","author":"MV Sofroniew","year":"2009","unstructured":"Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638\u2013647. https:\/\/doi.org\/10.1016\/j.tins.2009.08.002","journal-title":"Trends Neurosci"},{"key":"2986_CR49","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1002\/1097-4547(20010101)63:1<90::AID-JNR11>3.0.CO;2-9","volume":"63","author":"Z Soltys","year":"2001","unstructured":"Soltys Z, Ziaja M, Pawlinski R et al (2001) Morphology of reactive microglia in the injured cerebral cortex. J Neurosci Res 63:90\u201397","journal-title":"J Neurosci Res"},{"key":"2986_CR50","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1016\/j.yebeh.2018.08.002","volume":"87","author":"Z Sun","year":"2018","unstructured":"Sun Z, Liu S, Kharlamov EA et al (2018) Hippocampal neuropeptide Y protein expression following controlled cortical impact and posttraumatic epilepsy. Epilepsy Behav 87:188\u2013194. https:\/\/doi.org\/10.1016\/j.yebeh.2018.08.002","journal-title":"Epilepsy Behav"},{"key":"2986_CR51","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fimmu.2022.997786","volume":"13","author":"A Vidal-Itriago","year":"2022","unstructured":"Vidal-Itriago A, Radford RAW, Aramideh JA et al (2022) Microglia morphophysiological diversity and its implications for the CNS. Front Immunol 13:1\u201316. https:\/\/doi.org\/10.3389\/fimmu.2022.997786","journal-title":"Front Immunol"},{"key":"2986_CR52","doi-asserted-by":"publisher","unstructured":"Villapol S, Loane DJ, Burns MP (2017) Sexual dimorphism in the inflammatory response to traumatic brain injury. Glia 65:1423\u20131438. https:\/\/doi.org\/10.1002\/glia.23171","DOI":"10.1002\/glia.23171"},{"key":"2986_CR53","doi-asserted-by":"publisher","first-page":"807","DOI":"10.3171\/jns.1998.89.5.0807","volume":"89","author":"K Wada","year":"1998","unstructured":"Wada K, Chatzipanteli K, Busto R, Dietrich WD (1998) Role of nitric oxide in traumatic brain injury in the rat. J Neurosurg 89:807\u2013818. https:\/\/doi.org\/10.3171\/jns.1998.89.5.0807","journal-title":"J Neurosurg"},{"key":"2986_CR54","doi-asserted-by":"publisher","first-page":"640","DOI":"10.1002\/acn3.441","volume":"4","author":"DK Wright","year":"2017","unstructured":"Wright DK, O\u2019Brien TJ, Shultz SR, Mychasiuk R (2017) Sex matters: repetitive mild traumatic brain injury in adolescent rats. Ann Clin Transl Neurol 4:640\u2013654. https:\/\/doi.org\/10.1002\/acn3.441","journal-title":"Ann Clin Transl Neurol"},{"key":"2986_CR55","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fneur.2019.01149","volume":"10","author":"S Xu","year":"2019","unstructured":"Xu S, Sun Q, Fan J et al (2019) Role of Astrocytes in Post-traumatic Epilepsy. Front Neurol 10:1\u201310. https:\/\/doi.org\/10.3389\/fneur.2019.01149","journal-title":"Front Neurol"},{"key":"2986_CR56","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12964-020-00549-2","volume":"18","author":"Y Zhou","year":"2020","unstructured":"Zhou Y, Shao A, Yao Y et al (2020) Dual roles of astrocytes in plasticity and reconstruction after traumatic brain injury. Cell Communication and Signaling 18:1\u201316. https:\/\/doi.org\/10.1186\/s12964-020-00549-2","journal-title":"Cell Communication and Signaling"}],"container-title":["Brain Structure and Function"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00429-025-02986-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00429-025-02986-6\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00429-025-02986-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,9,29]],"date-time":"2025-09-29T14:17:16Z","timestamp":1759155436000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00429-025-02986-6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,7,25]]},"references-count":57,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2025,9]]}},"alternative-id":["2986"],"URL":"https:\/\/doi.org\/10.1007\/s00429-025-02986-6","relation":{},"ISSN":["1863-2661"],"issn-type":[{"value":"1863-2661","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,7,25]]},"assertion":[{"value":"13 May 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 July 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 July 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"All procedures using experimental animals were approved by the Second Local Ethical Committee in Cracow (agreement no. 316\/2020) and were in accordance with the international standards.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}}],"article-number":"122"}}