Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-05T00:46:32.237Z Has data issue: false hasContentIssue false

Chapter 1 - Neurobiological Aspects of Post-traumatic Epilepsy: Lessons from Animal Models

Published online by Cambridge University Press:  10 August 2021

By
Patricia G. Saletti ,
Anna Maria Katsarou ,
Mariana Molero  and
Aristea S. Galanopoulou
Edited by
Marco Mula
Marco Mula
Affiliation:
St George's Hospital Medical School, University of London
Get access

Summary

Traumatic brain injury (TBI) is a leading type of epilepsy with significant repercussions for the quality of life of patients, due to the associated injury, consequent epilepsy and cognitive, behavioral or neuropsychiatric sequelae. There have been intense efforts to generate better strategies and methods to treat these patients better. This chapter reviews the advances in animal models of posttraumatic epilepsy (PTE), focusing on rodents, presenting an update on models, their phenotype, findings on neurobiology of TBI and PTE and future directions. The value of models, like the fluid percussion injury, controlled cortical impact, blast, penetrating TBI, weight drop TBI, in this process in being discussed as well as efforts to accelerate progress in the field through the use of collaborative research and infrastructure.

Keywords

rodentmodel of traumatic brain injurymodel of posttraumatic epilepsyfluid percussion injurycontrolled cortical impactpenetrating injuryblast injurytauinflammationhemorrhagetreatmentcomorbidities
Type
Chapter
Information
Post-traumatic Epilepsy , pp. 1 - 28
Publisher: Cambridge University Press
Print publication year: 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Centers for Disease Control and Prevention. Traumatic Brain Injury & Concussion 2019. Available from: www.cdc.gov/traumaticbraininjury/index.html.Google Scholar
Ali, I., Silva, J.C., Liu, S., et al. Targeting neurodegeneration to prevent post-traumatic epilepsy. Neurobiol Dis 2019;123:100–9.Google Scholar
Hunt, R.F., Boychuk, J.A., Smith, B.N.. Neural circuit mechanisms of post-traumatic epilepsy. Front Cell Neurosci 2013;7:89.Google Scholar
Xiong, Y., Mahmood, A., Chopp, M.. Animal models of traumatic brain injury. Nat Rev Neurosci 2013;14(2):128–42.CrossRefGoogle ScholarPubMed
Giza, C.C., Mink, R.B., Madikians, A.. Pediatric traumatic brain injury: not just little adults. Curr Op Crit Care 2007;13(2):143–52.Google Scholar
Saletti, P.G., Ali, I., Casillas-Espinosa, P.M., et al. In search of antiepileptogenic treatments for post-traumatic epilepsy. Neurobiol Dis 2019;123:86–99.CrossRefGoogle ScholarPubMed
Christensen, J.. Traumatic brain injury: risks of epilepsy and implications for medicolegal assessment. Epilepsia 2012;53 Suppl 4:43–7.Google Scholar
Christensen, J., Pedersen, M.G., Pedersen, C.B., Sidenius, P., Olsen, J., Vestergaard, M.. Long-term risk of epilepsy after traumatic brain injury in children and young adults: a population-based cohort study. Lancet 2009;373(9669):1105–10.CrossRefGoogle Scholar
Fisher, R.S., Acevedo, C., Arzimanoglou, A., et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia 2014;55(4):475–82.Google Scholar
Scheffer, I.E., French, J., Hirsch, E., et al. Classification of the epilepsies: New concepts for discussion and debate-Special report of the ILAE Classification Task Force of the Commission for Classification and Terminology. Epilepsia Open 2016;1(1–2):37–44.CrossRefGoogle ScholarPubMed
Ding, K., Gupta, P.K., Diaz-Arrastia, R.. Epilepsy after traumatic brain injury. In: Laskowitz, D, Grant, G, eds. Translational Research in Traumatic Brain Injury. Frontiers in Neuroscience. Boca Raton (FL): CRC Press/Taylor and Francis Group;2016.Google Scholar
Englander, J., Bushnik, T., Wright, J.M., Jamison, L., Duong, T.T.. Mortality in late post-traumatic seizures. J Neurotrauma 2009;26(9):1471–7.CrossRefGoogle ScholarPubMed
Agrawal, A., Timothy, J., Pandit, L., Manju, M.. Post-traumatic epilepsy: an overview. Clin Neurol Neurosurg 2006;108(5):433–9.CrossRefGoogle ScholarPubMed
D’Ambrosio, R., Perucca, E.. Epilepsy after head injury. Curr Opin Neurol 2004;17(6):731–5.Google Scholar
Xu, T., Yu, X., Ou, S., et al. Risk factors for posttraumatic epilepsy: A systematic review and meta-analysis. Epilepsy Behav 2017;67:1–6.CrossRefGoogle ScholarPubMed
Tubi, M.A., Lutkenhoff, E., Blanco, M.B., et al. Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study. Neurobiol Dis 2019;123:115–21.Google Scholar
Brady, R.D., Casillas-Espinosa, P.M., Agoston, D.V., et al. Modelling traumatic brain injury and posttraumatic epilepsy in rodents. Neurobiol Dis 2019;123:8–19.Google Scholar
Johnstone, V.P., Wright, D.K., Wong, K., O’Brien, T.J., Rajan, R., Shultz, S.R.. Experimental traumatic brain injury results in long-term recovery of functional responsiveness in sensory cortex but persisting structural changes and sensorimotor, cognitive, and emotional deficits. J Neurotrauma 2015;32(17):1333–46.Google Scholar
Jones, N.C., Cardamone, L., Williams, J.P., Salzberg, M.R., Myers, D., O’Brien, T.J.. Experimental traumatic brain injury induces a pervasive hyperanxious phenotype in rats. J Neurotrauma 2008;25(11):1367–74.CrossRefGoogle ScholarPubMed
Rodgers, K.M., Deming, Y.K., Bercum, F.M., et al. Reversal of established traumatic brain injury-induced, anxiety-like behavior in rats after delayed, post-injury neuroimmune suppression. J Neurotrauma 2014;31(5):487–97.Google Scholar
Shultz, S.R., Wright, D.K., Zheng, P., et al. Sodium selenate reduces hyperphosphorylated tau and improves outcomes after traumatic brain injury. Brain 2015;138(5):1297–313.Google Scholar
Beauchamp, M.H., Anderson, V.. Cognitive and psychopathological sequelae of pediatric traumatic brain injury. In: Dulac, O., Lassonde, M., Sarnat, H.B., eds. Handbook of Clinical Neurology. Philadelphia, PA: Elsevier, 2013; 112:913–20.Google Scholar
Anderson, V.A., Spencer-Smith, M.M., Coleman, L., et al. Predicting neurocognitive and behavioural outcome after early brain insult. Developmental Medicine and Child Neurology 2014;56(4):329–36.Google Scholar
Luo, J., Nguyen, A., Villeda, S., et al. Long-term cognitive impairments and pathological alterations in a mouse model of repetitive mild traumatic brain injury. Front Neurol 2014;5:12.Google Scholar
Muccigrosso, M.M., Ford, J., Benner, B., et al. Cognitive deficits develop 1 month after diffuse brain injury and are exaggerated by microglia-associated reactivity to peripheral immune challenge. Brain Behav Immun 2016;54:95–109.CrossRefGoogle ScholarPubMed
Ogier, M., Belmeguenai, A., Lieutaud, T., et al. Cognitive deficits and inflammatory response resulting from mild-to-moderate traumatic brain injury in rats are exacerbated by repeated pre-exposure to an innate stress stimulus. J Neurotrauma 2017;34(8):1645–57.Google Scholar
Castriotta, R.J., Wilde, M.C., Lai, J.M., Atanasov, S., Masel, B.E., Kuna, S.T.. Prevalence and consequences of sleep disorders in traumatic brain injury. J Clin Sleep Med 2007;3(4):349–56.Google Scholar
Vos, B.C., Nieuwenhuijsen, K., Sluiter, J.K.. Consequences of traumatic brain injury in professional american football players: A systematic review of the literature. Clin J Sport Med 2018;28(2):91–9.Google Scholar
Semple, B.D., Zamani, A., Rayner, G., Shultz, S.R., Jones, N.C.. Affective, neurocognitive and psychosocial disorders associated with traumatic brain injury and post-traumatic epilepsy. Neurobiol Dis 2019;123:27–41.CrossRefGoogle ScholarPubMed
Dudek, F.E., Staley, K.J.. The time course of acquired epilepsy: implications for therapeutic intervention to suppress epileptogenesis. Neurosci Lett 2011;497(3):240–6.Google Scholar
Klein, P., Dingledine, R., Aronica, E., et al. Commonalities in epileptogenic processes from different acute brain insults: Do they translate? Epilepsia 2018;59(1):37–66.Google Scholar
Akman, O., Moshe, S.L., Galanopoulou, A.S.. Sex-specific consequences of early life seizures. Neurobiol Dis 2014;72 Pt B:153–66.CrossRefGoogle ScholarPubMed
Galanopoulou, A.S., Moshe, S.L.. In search of epilepsy biomarkers in the immature brain: goals, challenges and strategies. Biomark Med 2011;5(5):615–28.CrossRefGoogle ScholarPubMed
Katsarou, A.M., Moshe, S.L., Galanopoulou, A.S.. Interneuronopathies and their role in early life epilepsies and neurodevelopmental disorders. Epilepsia Open 2017;2(3):284–306.Google Scholar
Katsarou, A.M., Galanopoulou, A.S., Moshe, S.L.. Epileptogenesis in neonatal brain. Semin Fetal Neonatal Med 2018;23(3):159–67.Google Scholar
Gottlieb, A., Keydar, I., Epstein, H.T.. Rodent brain growth stages: an analytical review. Biol Neonate 1977;32(3–4):166–76.Google Scholar
Dobbing, J., Sands, J.. Comparative aspects of the brain growth spurt. Early Human Development 1979;3:79–83.CrossRefGoogle ScholarPubMed
Avishai-Eliner, S., Brunson, K.L., Sandman, C.A., Baram, T.Z.. Stressed-out, or in (utero)? Trends in Neurosciences 2002;25(10):518–24.Google Scholar
Romijn, H.J., Hofman, M.A., Gramsbergen, A.. At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Human Development 1991;26(1):61–7.Google Scholar
Semple, B.D., Blomgren, K., Gimlin, K., Ferriero, D.M., Noble-Haeusslein, L.J.. Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species. Progress in Neurobiology 2013;106(7):1–16.Google Scholar
Prins, M.L., Hovda, D.A.. Developing experimental models to address traumatic brain injury in children. J Neurotrauma 2003;20(2):123–37.Google Scholar
McIntosh, T.K., Vink, R., Noble, L., et al. Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 1989;28(1):233–44.Google Scholar
Prins, M.L., Lee, S.M., Cheng, C.L., Becker, D.P., Hovda, D.A.. Fluid percussion brain injury in the developing and adult rat: a comparative study of mortality, morphology, intracranial pressure and mean arterial blood pressure. Brain Res Developmental Brain Res 1996;95(2):272–82.Google Scholar
Armstead, W.M., Kurth, C.D.. Different cerebral hemodynamic responses following fluid percussion brain injury in the newborn and juvenile pig. J Neurotrauma 1994;11(5):487–97.Google Scholar
Aungst, S.L., Kabadi, S.V., Thompson, S.M., Stoica, B.A., Faden, A.I.. Repeated mild traumatic brain injury causes chronic neuroinflammation, changes in hippocampal synaptic plasticity, and associated cognitive deficits. J Cereb Blood Flow Metab 2014;34(7):1223–32.Google Scholar
Bao, F., Shultz, S.R., Hepburn, J.D., et al. A CD11d monoclonal antibody treatment reduces tissue injury and improves neurological outcome after fluid percussion brain injury in rats. J Neurotrauma 2012;29(14):2375–92.CrossRefGoogle ScholarPubMed
DeRoss, A.L., Adams, J.E., Vane, D.W., Russell, S.J., Terella, A.M., Wald, S.L.. Multiple head injuries in rats: effects on behavior. J Trauma 2002;52(4):708–14.Google Scholar
Gurkoff, G.G., Giza, C.C., Hovda, D.A.. Lateral fluid percussion injury in the developing rat causes an acute, mild behavioral dysfunction in the absence of significant cell death. Brain Res 2006;1077(1):24–36.Google Scholar
Hayward, N.M., Immonen, R., Tuunanen, P.I., Ndode-Ekane, X.E., Grohn, O., Pitkanen, A.. Association of chronic vascular changes with functional outcome after traumatic brain injury in rats. J Neurotrauma 2010;27(12):2203–19.Google Scholar
Shultz, S.R., Bao, F., Omana, V., Chiu, C., Brown, A., Cain, D.P.. Repeated mild lateral fluid percussion brain injury in the rat causes cumulative long-term behavioral impairments, neuroinflammation, and cortical loss in an animal model of repeated concussion. J Neurotrauma 2012;29(2):281–94.Google Scholar
Shultz, S.R., Cardamone, L., Liu, Y.R., et al. Can structural or functional changes following traumatic brain injury in the rat predict epileptic outcome? Epilepsia 2013;54(7):1240–50.Google Scholar
Shultz, S.R., MacFabe, D.F., Foley, K.A., Taylor, R., Cain, D.P.. A single mild fluid percussion injury induces short-term behavioral and neuropathological changes in the Long-Evans rat: support for an animal model of concussion. Behav Brain Res 2011;224(2):326–35.Google Scholar
Bolkvadze, T., Pitkanen, A.. Development of post-traumatic epilepsy after controlled cortical impact and lateral fluid-percussion-induced brain injury in the mouse. J Neurotrauma 2012;29(5):789–812.CrossRefGoogle ScholarPubMed
Cole, J.T., Yarnell, A., Kean, W.S., et al. Craniotomy: true sham for traumatic brain injury, or a sham of a sham? J Neurotrauma 2011;28(3):359–69.Google Scholar
Johnstone, V.P.A., Shultz, S.R., Yan, E.B., O’Brien, T.J., Rajan, R.. The acute phase of mild traumatic brain injury is characterized by a distance-dependent neuronal hypoactivity. J Neurotraum 2014;31(22):1881–95.CrossRefGoogle ScholarPubMed
Skopin, M.D., Kabadi, S.V., Viechweg, S.S., Mong, J.A., Faden, A.I.. Chronic decrease in wakefulness and disruption of sleep-wake behavior after experimental traumatic brain injury. J Neurotrauma 2015;32(5):289–96.Google Scholar
Jones, N.C., Nguyen, T., Corcoran, N.M., et al. Targeting hyperphosphorylated tau with sodium selenate suppresses seizures in rodent models. Neurobiol Dis 2012;45(3):897–901.Google Scholar
Liu, S.J., Zheng, P., Wright, D.K., et al. Sodium selenate retards epileptogenesis in acquired epilepsy models reversing changes in protein phosphatase 2 A and hyperphosphorylated tau. Brain 2016;139(7):1919–38.Google Scholar
Kharatishvili, I., Nissinen, J.P., McIntosh, T.K., Pitkanen, A.. A model of posttraumatic epilepsy induced by lateral fluid-percussion brain injury in rats. Neuroscience 2006;140(2):685–97.CrossRefGoogle Scholar
Reid, A.Y., Bragin, A., Giza, C.C., Staba, R.J., Engel, J. Jr. The progression of electrophysiologic abnormalities during epileptogenesis after experimental traumatic brain injury. Epilepsia 2016;57(10):1558–67.Google Scholar
D’Ambrosio, R., Fender, J.S., Fairbanks, J.P., et al. Progression from frontal-parietal to mesial-temporal epilepsy after fluid percussion injury in the rat. Brain 2005;128:174–88.Google Scholar
Kadam, S.D., D’Ambrosio, R., Duveau, V., et al. Methodological standards and interpretation of video-electroencephalography in adult control rodents. A TASK1-WG1 report of the AES/ILAE Translational Task Force of the ILAE. Epilepsia 2017;58 Suppl 4:10–27.CrossRefGoogle ScholarPubMed
Kharatishvili, I., Immonen, R., Grohn, O., Pitkanen, A.. Quantitative diffusion MRI of hippocampus as a surrogate marker for post-traumatic epileptogenesis. Brain 2007;130:3155–68.Google Scholar
Rodriguez Lucci, F., Alet, M., Ameriso, S.F.. [Post-stroke epilepsy]. Medicina (B Aires). 2018;78(2):86–90.Google Scholar
Lighthall, J.W.. Controlled cortical impact: a new experimental brain injury model. J Neurotrauma 1988;5(1):1–15.Google Scholar
Osier, N.D., Dixon, C.E.. The controlled cortical impact model: applications, considerations for researchers, and future directions. Front Neurol 2016;7:134.Google Scholar
Cernak, I.. Animal models of head trauma. NeuroRx 2005;2(3):410–22.Google Scholar
Fox, G.B., Fan, L., Levasseur, R.A., Faden, A.I.. Sustained sensory/motor and cognitive deficits with neuronal apoptosis following controlled cortical impact brain injury in the mouse. J Neurotrauma 1998;15(8):599–614.Google Scholar
Guo, D., Zeng, L., Brody, D.L., Wong, M.. Rapamycin attenuates the development of posttraumatic epilepsy in a mouse model of traumatic brain injury. PLoS One 2013;8(5):e64078.Google Scholar
Hunt, R.F., Scheff, S.W., Smith, B.N.. Posttraumatic epilepsy after controlled cortical impact injury in mice. Exp Neurol 2009;215(2):243–52.Google Scholar
Kelly, K.M., Miller, E.R., Lepsveridze, E., Kharlamov, E.A., McHedlishvili, Z.. Posttraumatic seizures and epilepsy in adult rats after controlled cortical impact. Epilepsy Res 2015;117:104–16.CrossRefGoogle ScholarPubMed
Scheff, S.W., Baldwin, S.A., Brown, R.W., Kraemer, P.J.. Morris water maze deficits in rats following traumatic brain injury: lateral controlled cortical impact. J Neurotrauma 1997;14(9):615–27.Google Scholar
Osier, N.D., Korpon, J.R., Dixon, C.E.. Frontiers in neuroengineering. controlled cortical impact model. In: Kobeissy, FH, editor. Brain Neurotrauma: Molecular, Neuropsychological, and Rehabilitation Aspects. Boca Raton (FL): CRC Press, Taylor & Francis Group, LLC.; 2015.Google Scholar
Ajao, D.O., Pop, V., Kamper, J.E., et al. Traumatic brain injury in young rats leads to progressive behavioral deficits coincident with altered tissue properties in adulthood. J Neurotrauma 2012;29(11):2060–74.Google Scholar
Card, J.P., Santone, D.J. Jr., Gluhovsky, M.Y., Adelson, P.D.. Plastic reorganization of hippocampal and neocortical circuitry in experimental traumatic brain injury in the immature rat. J Neurotrauma 2005;22(9):989–1002.Google Scholar
Semple, B.D., Canchola, S.A., Noble-Haeusslein, L.J.. Deficits in social behavior emerge during development after pediatric traumatic brain injury in mice. J Neurotrauma 2012;29(17):2672–83.Google Scholar
Semple, B.D., Noble-Haeusslein, L.J., Jun Kwon, Y., et al. Sociosexual and communication deficits after traumatic injury to the developing murine brain. PLoS One 2014;9(8):e103386.Google Scholar
Tong, W., Igarashi, T., Ferriero, D.M., Noble, L.J.. Traumatic brain injury in the immature mouse brain: characterization of regional vulnerability. Exp Neurol 2002;176(1):105–16.Google Scholar
Pullela, R., Raber, J., Pfankuch, T., et al. Traumatic injury to the immature brain results in progressive neuronal loss, hyperactivity and delayed cognitive impairments. Developmental Neurosci 2006;28(4–5):396–409.CrossRefGoogle Scholar
Semple, B.D., O’Brien, T.J., Gimlin, K., et al. Interleukin-1 receptor in seizure susceptibility after traumatic injury to the pediatric brain. J Neurosci 2017;37(33):7864–77.Google Scholar
Elder, G.A., Mitsis, E.M., Ahlers, S.T., Cristian, A.. Blast-induced mild traumatic brain injury. Psychiatr Clin North Am. 2010;33(4):757–81.Google Scholar
Risling, M., Plantman, S., Angeria, M., et al. Mechanisms of blast induced brain injuries, experimental studies in rats. Neuroimage 2011;54 Suppl 1:S89–97.Google Scholar
Cernak, I.. The importance of systemic response in the pathobiology of blast-induced neurotrauma. Front Neurol 2010;1:151.Google Scholar
Kamnaksh, A., Kovesdi, E., Kwon, S.K., et al. Factors affecting blast traumatic brain injury. J Neurotrauma 2011;28(10):2145–53.Google Scholar
Agoston, D.V., Gyorgy, A., Eidelman, O., Pollard, H.B.. Proteomic biomarkers for blast neurotrauma: targeting cerebral edema, inflammation, and neuronal death cascades. J Neurotrauma 2009;26(6):901–11.Google Scholar
Elder, G.A., Dorr, N.P., De Gasperi, R., et al. Blast exposure induces post-traumatic stress disorder-related traits in a rat model of mild traumatic brain injury. J Neurotrauma 2012;29(16):2564–75.Google Scholar
Kovesdi, E., Kamnaksh, A., Wingo, D., et al. Acute minocycline treatment mitigates the symptoms of mild blast-induced traumatic brain injury. Front Neurol 2012;3:111.Google Scholar
Kwon, S.K., Kovesdi, E., Gyorgy, A.B., et al. Stress and traumatic brain injury: a behavioral, proteomics, and histological study. Front Neurol 2011;2:12.Google Scholar
Kamnaksh, A., Kwon, S.K., Kovesdi, E., et al. Neurobehavioral, cellular, and molecular consequences of single and multiple mild blast exposure. Electrophoresis 2012;33(24):3680–92.Google Scholar
Bugay, V., Bozdemir, E., Vigil, F.A., et al. A mouse model of repetitive blast traumatic brain injury reveals post-trauma seizures and increased neuronal excitability. J Neurotrauma 2020;37(2):248–61.Google Scholar
Lu, X.C., Hartings, J.A., Si, Y., Balbir, A., Cao, Y., Tortella, F.C.. Electrocortical pathology in a rat model of penetrating ballistic-like brain injury. J Neurotrauma 2011;28(1):71–83.Google Scholar
Shear, D.A., Lu, X.C., Bombard, M.C., et al. Longitudinal characterization of motor and cognitive deficits in a model of penetrating ballistic-like brain injury. J Neurotrauma 2010;27(10):1911–23.Google Scholar
Williams, A.J., Hartings, J.A., Lu, X.C., Rolli, M.L., Dave, J.R., Tortella, F.C.. Characterization of a new rat model of penetrating ballistic brain injury. J Neurotrauma 2005;22(2):313–31.Google Scholar
Kendirli, M.T., Rose, D.T., Bertram, E.H.. A model of posttraumatic epilepsy after penetrating brain injuries: effect of lesion size and metal fragments. Epilepsia 2014;55(12):1969–77.CrossRefGoogle Scholar
Feeney, D.M., Boyeson, M.G., Linn, R.T., Murray, H.M., Dail, W.G.. Responses to cortical injury: I. Methodology and local effects of contusions in the rat. Brain Res 1981;211(1):67–77.Google Scholar
Dail, W.G., Feeney, D.M., Murray, H.M., Linn, R.T., Boyeson, M.G.. Responses to cortical injury: II. Widespread depression of the activity of an enzyme in cortex remote from a focal injury. Brain Res 1981;211(1):79–89.Google Scholar
Gasparovic, C., Arfai, N., Smid, N., Feeney, D.M.. Decrease and recovery of N-acetylaspartate/creatine in rat brain remote from focal injury. J Neurotrauma 2001;18(3):241–6.Google Scholar
Marmarou, A., Foda, M.A., van den Brink, W., Campbell, J., Kita, H., Demetriadou, K.. A new model of diffuse brain injury in rats. Part I: Pathophysiology and biomechanics.J Neurosurg 1994;80(2):291–300.Google Scholar
Heath, D.L., Vink, R.. Impact acceleration-induced severe diffuse axonal injury in rats: characterization of phosphate metabolism and neurologic outcome. J Neurotrauma 1995;12(6):1027–34.CrossRefGoogle ScholarPubMed
Schmidt, R.H., Scholten, K.J., Maughan, P.H.. Cognitive impairment and synaptosomal choline uptake in rats following impact acceleration injury. J Neurotrauma 2000;17(12):1129–39.Google Scholar
Foda, M.A., Marmarou, A.. A new model of diffuse brain injury in rats. Part II: Morphological characterization. J Neurosurg 1994;80(2):301–13.Google Scholar
Flierl, M.A., Stahel, P.F., Beauchamp, K.M., Morgan, S.J., Smith, W.R., Shohami, E.. Mouse closed head injury model induced by a weight-drop device. Nat Protoc. 2009;4(9):1328–37.Google Scholar
Chen, Y., Constantini, S., Trembovler, V., Weinstock, M., Shohami, E.. An experimental model of closed head injury in mice: pathophysiology, histopathology, and cognitive deficits. J Neurotrauma 1996;13(10):557–68.Google Scholar
Albert-Weissenberger, C., Varrallyay, C., Raslan, F., Kleinschnitz, C., Siren, A.L.. An experimental protocol for mimicking pathomechanisms of traumatic brain injury in mice. Exp Transl Stroke Med 2012;4:1.Google Scholar
Adelson, P.D., Dixon, C.E., Kochanek, P.M.. Long-term dysfunction following diffuse traumatic brain injury in the immature rat. J Neurotrauma 2000;17(4):273–82.Google Scholar
Adelson, P.D., Whalen, M.J., Kochanek, P.M., Robichaud, P., Carlos, T.M.. Blood brain barrier permeability and acute inflammation in two models of traumatic brain injury in the immature rat: a preliminary report. Acta Neurochir Suppl 1998;71:104–6.Google Scholar
Huh, J.W., Widing, A.G., Raghupathi, R.. Midline brain injury in the immature rat induces sustained cognitive deficits, bihemispheric axonal injury and neurodegeneration. Exp Neurol 2008;213(1):84–92.Google Scholar
Adelson, P.D., Jenkins, L.W., Hamilton, R.L., Robichaud, P., Tran, M.P., Kochanek, P.M.. Histopathologic response of the immature rat to diffuse traumatic brain injury. J Neurotrauma 2001;18(10):967–76.Google Scholar
Adelson, P.D., Fellows-Mayle, W., Kochanek, P.M., Dixon, C.E.. Morris water maze function and histologic characterization of two age-at-injury experimental models of controlled cortical impact in the immature rat. Childs Nerv Sys 2013;29(1):43–53.Google Scholar
Kernie, S.G., Parent, J.M.. Forebrain neurogenesis after focal ischemic and traumatic brain injury. Neurobiol Dis 2010;37(2):267–74.Google Scholar
Sun, D., Colello, R.J., Daugherty, W.P., et al. Cell proliferation and neuronal differentiation in the dentate gyrus in juvenile and adult rats following traumatic brain injury. J Neurotrauma 2005;22(1):95–105.Google Scholar
Goodus, M.T., Guzman, A.M., Calderon, F., Jiang, Y., Levison, S.W.. Neural stem cells in the immature, but not the mature, subventricular zone respond robustly to traumatic brain injury. Develop Neurosci 2015;37(1):29–42.Google Scholar
Neuberger, E.J., Swietek, B., Corrubia, L., Prasanna, A., Santhakumar, V.. Enhanced dentate neurogenesis after brain injury undermines long-term neurogenic potential and promotes seizure susceptibility. Stem Cell Rep 2017;9(3):972–84.Google Scholar
Scheff, S.W., Price, D.A., Hicks, R.R., Baldwin, S.A., Robinson, S., Brackney, C.. Synaptogenesis in the hippocampal CA1 field following traumatic brain injury. J Neurotrauma 2005;22(7):719–32.Google Scholar
Casella, E.M., Thomas, T.C., Vanino, D.L., et al. Traumatic brain injury alters long-term hippocampal neuron morphology in juvenile, but not immature, rats. Childs Nerv Sys 2014;30(8):1333–42.Google Scholar
Mychasiuk, R., Farran, A., Esser, M.J.. Assessment of an experimental rodent model of pediatric mild traumatic brain injury. J Neurotrauma 2014;31(8):749–57.Google Scholar
Nichols, J., Perez, R., Wu, C., Adelson, P.D., Anderson, T.. Traumatic brain injury induces rapid enhancement of cortical excitability in juvenile rats. CNS Neurosci Ther 2015;21(2):193–203.Google Scholar
Scheff, S.W., Benardo, L.S., Cotman, C.W.. Decline in reactive fiber growth in the dentate gyrus of aged rats compared to young adult rats following entorhinal cortex removal. Brain Res 1980;199(1):21–38.Google Scholar
Li, N., Yang, Y., Glover, D.P., et al. Evidence for impaired plasticity after traumatic brain injury in the developing brain. J Neurotrauma 2014;31(4):395–403.Google Scholar
Potts, M.B., Koh, S.E., Whetstone, W.D., et al. Traumatic injury to the immature brain: inflammation, oxidative injury, and iron-mediated damage as potential therapeutic targets. NeuroRx 2006;3(2):143–53.Google Scholar
Ravizza, T., Vezzani, A.. Pharmacological targeting of brain inflammation in epilepsy: Therapeutic perspectives from experimental and clinical studies. Epilepsia Open 2018;3(Suppl 2):133–42.Google Scholar
Claus, C.P., Tsuru-Aoyagi, K., Adwanikar, H., Walker, B., Whetstone, W., Noble-Haeusslein, L.J.. Age is a determinant of leukocyte infiltration and loss of cortical volume after traumatic brain injury. Develop Neurosci 2010;32(5–6):454–65.Google Scholar
Khan, J.Y., Black, S.M.. Developmental changes in murine brain antioxidant enzymes. Pediatr Res 2003;54(1):77–82.Google Scholar
Aspberg, A., Tottmar, O.. Development of antioxidant enzymes in rat brain and in reaggregation culture of fetal brain cells. Brain Res Develop Brain Res 1992;66(1):55–8.Google Scholar
Buard, A., Clement, M., Bourre, J.M.. Developmental changes in enzymatic systems involved in protection against peroxidation in isolated rat brain microvessels. Neurosci Lett 1992;141(1):72–4.Google Scholar
Lazo, O., Singh, A.K., Singh, I.. Postnatal development and isolation of peroxisomes from brain. J Neurochem 1991;56(4):1343–53.Google Scholar
Holshouser, B.A., Ashwal, S., Luh, G.Y., et al. Proton MR spectroscopy after acute central nervous system injury: outcome prediction in neonates, infants, and children. Radiology 1997;202(2):487–96.Google Scholar
Ashwal, S., Holshouser, B.A., Shu, S.K., et al. Predictive value of proton magnetic resonance spectroscopy in pediatric closed head injury. Pediatr Neurol 2000;23(2):114–25.Google Scholar
Scafidi, S., O’Brien, J., Hopkins, I., Robertson, C., Fiskum, G., McKenna, M.. Delayed cerebral oxidative glucose metabolism after traumatic brain injury in young rats. J Neurochem 2009;109 Suppl 1:189–97.Google Scholar
Casey, P.A., McKenna, M.C., Fiskum, G., Saraswati, M., Robertson, C.L.. Early and sustained alterations in cerebral metabolism after traumatic brain injury in immature rats. J Neurotrauma 2008;25(6):603–14.Google Scholar
Robertson, C.L., Saraswati, M., Scafidi, S., Fiskum, G., Casey, P., McKenna, M.C.. Cerebral glucose metabolism in an immature rat model of pediatric traumatic brain injury. J Neurotrauma 2013;30(24):2066–72.Google Scholar
Deng-Bryant, Y., Prins, M.L., Hovda, D.A., Harris, N.G.. Ketogenic diet prevents alterations in brain metabolism in young but not adult rats after traumatic brain injury. J Neurotrauma 2011;28(9):1813–25.Google Scholar
Prins, M.L., Matsumoto, J.. Metabolic response of pediatric traumatic brain injury. J Child Neurol 2016;31(1):28–34.Google Scholar
Schwartzkroin, P.A., Wenzel, H.J., Lyeth, B.G., et al. Does ketogenic diet alter seizure sensitivity and cell loss following fluid percussion injury? Epilepsy Res 2010;92(1):74–84.Google Scholar
Galanopoulou, A.S., Gorter, J.A., Cepeda, C.. Finding a better drug for epilepsy: the mTOR pathway as an antiepileptogenic target. Epilepsia 2012;53(7):1119–30.Google Scholar
Butler, C.R., Boychuk, J.A., Smith, B.N.. Effects of rapamycin treatment on neurogenesis and synaptic reorganization in the dentate gyrus after controlled cortical impact injury in mice. Front Syst Neurosci 2015;9:163.Google Scholar
Wang, C., Hu, Z., Zou, Y., et al. The post-therapeutic effect of rapamycin in mild traumatic brain-injured rats ensuing in the upregulation of autophagy and mitophagy. Cell Biol Int 2017;41(9):1039–47.Google Scholar
Willmore, L.J., Hurd, R.W., Sypert, G.W.. Epileptiform activity initiated by pial iontophoresis of ferrous and ferric chloride on rat cerebral cortex. Brain Res 1978;152(2):406–10.Google Scholar
Ronne Engstrom, E., Hillered, L., Flink, R., et al. Extracellular amino acid levels measured with intracerebral microdialysis in the model of posttraumatic epilepsy induced by intracortical iron injection. Epilepsy Res 2001;43(2):135–44.Google Scholar
Saletti, P.G., Lisgaras, C.P., Casillas-Espinosa, P., et al. (eds.) Site and time-specific tau hyperphosphorylation patterns in the rat cerebral cortex after traumatic brain injury: An EpiBioS4Rx Project 2 study. Society for Neuroscience Annual Meeting; 2019; Chicago, IL: Society for Neuroscience.Google Scholar
Kochanek, P.M., Bramlett, H.M., Dixon, C.E., et al. Operation brain trauma therapy: 2016 update. Mil Med 2018;183(suppl_1):303–12.Google Scholar
Galanopoulou, A.S., Engel, J. Jr., Moshe, S.L.. Preface: Antiepileptogenesis following traumatic brain injury. Neurobiol Dis 2019;123:1–2.Google Scholar
Engel, J. Jr. Epileptogenesis, traumatic brain injury, and biomarkers. Neurobiol Dis 2019;123:3–7.Google Scholar
Dixon, C.E., Lyeth, B.G., Povlishock, J.T., et al. A fluid percussion model of experimental brain injury in the rat. J Neurosurg 1987;67(1):110–9.Google Scholar
D’Ambrosio, R., Hakimian, S., Stewart, T., et al. Functional definition of seizure provides new insight into post-traumatic epileptogenesis. Brain 2009;132(10):2805–21.Google ScholarPubMed
Giza, C.C., Prins, M.L., Hovda, D.A., Herschman, H.R., Feldman, J.D.. Genes preferentially induced by depolarization after concussive brain injury: effects of age and injury severity. J Neurotrauma 2002;19(4):387–402.Google Scholar
Ip, E.Y., Giza, C.C., Griesbach, G.S., Hovda, D.A.. Effects of enriched environment and fluid percussion injury on dendritic arborization within the cerebral cortex of the developing rat. J Neurotrauma 2002;19(5):573–85.Google Scholar
Griesbach, G.S., Hovda, D.A., Molteni, R., Gomez-Pinilla, F.. Alterations in BDNF and synapsin I within the occipital cortex and hippocampus after mild traumatic brain injury in the developing rat: reflections of injury-induced neuroplasticity. J Neurotrauma 2002;19(7):803–14.Google Scholar
de la Tremblaye, P.B., Bondi, C.O., Lajud, N., Cheng, J.P., Radabaugh, H.L., Kline, A.E.. Galantamine and environmental enrichment enhance cognitive recovery after experimental traumatic brain injury but do not confer additional benefits when combined. J Neurotrauma 2017;34(8):1610–22.Google Scholar
Liu, N.K., Zhang, Y.P., Zou, J., et al. A semicircular controlled cortical impact produces long-term motor and cognitive dysfunction that correlates well with damage to both the sensorimotor cortex and hippocampus. Brain Res 2014;1576:18–26.Google Scholar
Hylin, M.J., Holden, R.C., Smith, A.C., Logsdon, A.F., Qaiser, R., Lucke-Wold, B.P.. Juvenile traumatic brain injury results in cognitive deficits associated with impaired endoplasmic reticulum stress and early tauopathy. Develop Neurosci 2018;40(2):175–88.Google Scholar
Semple, B.D., Trivedi, A., Gimlin, K., Noble-Haeusslein, L.J.. Neutrophil elastase mediates acute pathogenesis and is a determinant of long-term behavioral recovery after traumatic injury to the immature brain. Neurobiol Dis 2015;74:263–80.Google Scholar
Lee, S.W., Jang, M.S., Jeong, S.H., Kim, H.. Exploratory, cognitive, and depressive-like behaviors in adult and pediatric mice exposed to controlled cortical impact. Clin Exp Emerg Med 2019;6(2):125–37.Google Scholar
Nissinen, J., Andrade, P., Natunen, T., et al. Disease-modifying effect of atipamezole in a model of post-traumatic epilepsy. Epilepsy Res 2017;136:18–34.Google Scholar
Goodrich, G.S., Kabakov, A.Y., Hameed, M.Q., Dhamne, S.C., Rosenberg, P.A., Rotenberg, A.. Ceftriaxone treatment after traumatic brain injury restores expression of the glutamate transporter, GLT-1, reduces regional gliosis, and reduces post-traumatic seizures in the rat. J Neurotrauma 2013;30(16):1434–41.Google Scholar
D’Ambrosio, R., Eastman, C.L., Darvas, F., et al. Mild passive focal cooling prevents epileptic seizures after head injury in rats. Ann Neurol 2013;73(2):199–209.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×