Regional and temporal characterization of neuronal, glial, and axonal response after traumatic brain injury in the mouse
Abstract
Fluid percussion injury (FPI) is a commonly used and clinically relevant model of traumatic brain injury (TBI) in the rat. Recently, our lab successfully adapted FPI to mice. To account for differences in response to injury between mice and rats and provide a foundation for further use of FPI in gene-targeting studies, we sought to characterize the temporal and regional response to FPI in male C57BL/6 mice. Animals were killed at 10 min, 24 h, and 4, 7, 14, and 35 days (n = 3 for each group) after a very severe parasagittal FPI (> 4.0 atm) or sham injury (n = 3). Extensive numbers of damaged neurons were consistently found in the ipsilateral cortex, thalamus, and hippocampus by 10 min. This damage was nearly identical at 24 h, but quickly declined at subsequent time points. Activated microglia were found only in regions of neuronal injury at the earliest time points. Glial fibrillary acidic protein immunoreactivity reached significantly higher levels compared with controls at 7 days (P < 0. 05) in the cortex, thalamus, and hippocampus and remained elevated for 35 days. White matter degeneration was present in all regions examined. This damage did not appear until at least day 4, but progressed up to day 35. The spatial pattern of damage we observed in mice after FPI is similar to that seen in rats. However, the temporal progression of neuronal injury in mice is comparatively abbreviated in the hippocampus and thalamus. In conclusion, these results suggest that FPI in mice may…
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Many biological pathways are disrupted by experimental TBI resulting in progressive neurodegeneration including atrophy, neuronal loss, and axonal degeneration which are often associated with neuroinflammation including macrophage reactivity.
“Many biological pathways are disrupted by experimental TBI resulting in progressive neurodegeneration including atrophy, neuronal loss, and axonal degeneration which are often associated with neuroinflammation including macrophage reactivity (82–85).”
From The Inflammatory Continuum of Traumatic Brain Injury and Alzheimer’s Disease (2018) · cites this paper as [83]
Cites
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Experimental traumatic brain injury
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“researchers concluded that the spatial pattern of damage was similar in mice and rats post-FPI, but did note one key difference: Mice exhibited a shorter period of damage, particularly within the thalamus and hippocampus.(137) In rats, enlargement of the lateral ventricles has been reported 8 weeks post-FPI.”
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Ma, M. W., Wang, J., Dhandapani, K. M., Wang, R., & Brann, D. W. (2018) · Redox Biology · doi:10.1016/j.redox.2018.03.005 · Cited by 114 · see citing works
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MethodVagal nerve stimulation decreases blood-brain barrier disruption after traumatic brain injury
Lopez, N. E., Krzyżaniak, M., Costantini, T., Putnam, J. G., Hageny, A.-M., Eliceiri, B., Coimbra, R., & Bansal, V. (2012) · Journal of Trauma and Acute Care Surgery · doi:10.1097/ta.0b013e3182569875 · Cited by 70 · see citing works
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“In addition, the hippocampal neuronal injury following a single FP has been shown to have an extremely acute pattern in the order of minutes (Carbonell and Grady 1999b; Hicks et al., 1996; Toth et al., 1997) while excitotoxic damage occurs in the order of hours (Nadler et al., 1978).”
Microglia Receptors in Animal Models of Traumatic Brain Injury
Younger, D., Murugan, M., Rao, K. V. R., Wu, L., & Chandra, N. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1428-7 · Cited by 69 · see citing works
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“Evidence for diffuse axonal injury after mild, moderate, or severe TBI is commonly observed using a variety of immunohistochemical approaches, including amyloid precursor protein or silver stains to identify patterns of axonal degeneration (Bramlett et al., 1997; Carbonell and Grady, 1999; Hall et al., 2008).”
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“…removed and direct trauma to the brain tissue, produces moderate to severe TBI (Morales et al., 2005) resulting in focal lesions, blood–brain barrier (BBB) disturbances, edema formation, andmorphologically evident brain damage (Carbonell and Grady, 1999; Graham et al., 2000; Thompson et al., 2005).”
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“Although astroglial responses can occur within minutes of injury, some reactive glia may persist for weeks and even months after an initial insult in both humans (Mandell and Van-denBerg, 1999) and in experimental animals (Carbonell and Grady, 1999; Frisen et al., 1995; Smith et al., 1997).”
Self-citationSeo, T.-B., Kim, B.-K., Ko, I., Kim, D.-H., Shin, M., Kim, C., Yoon, J.-H., & Kim, H. K. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.06.087 · Cited by 56 · see citing works
Minimal Traumatic Brain Injury Induce Apoptotic Cell Death in Mice
Tashlykov, V., Katz, Y., Volkov, A., Gazit, V., Schreiber, S., Zohar, O., & Pick, C. G. (2008) · Journal of Molecular Neuroscience · doi:10.1007/s12031-008-9094-2 · Cited by 52 · see citing works
“Apoptosis is a common result of TBI (Carbonell and Grady 1999; O’Dell et al. 2000; Rink et al. 1995; Lu et al. 2000; Clark et al. 1999) and thus may be the cause of the delay in neuronal death that we observed.”
BackgroundImpaired spatial learning in a novel rat model of mild cerebral concussion injury
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Traumatic brain injury induces adipokine gene expression in rat brain.
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Historical Review of the Fluid-Percussion TBI Model
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“In general, neurological and behavioral deficits as well as histopathological findings in mice were similar to those of the rat model, but with the temporal progression of neuronal injury proceeding more rapidly in mice (56).”
BackgroundResultBrain Injury in the Context of Tauopathies
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“Importantly, the lateral FP technique was also adapted for mice [140–142], which makes it a useful tool for studying changes in transgenic animals.”
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“Similarly, there is an extensive experimental animal literature that shows cell loss or damage in the hippocampus following TBI (Carbonell and Grady, 1999; Geddes et al., 2003; Hicks et al., 1996; Pierce et al., 1998; Sick et al., 1998; Taft et al., 1992).”
InfluentialNeuroanatomical correlation of behavioral deficits in the CCI model of TBI
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Cell-Specific Upregulation of Survivin after Experimental Traumatic Brain Injury in Rats
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“Even if unspecific, neuroinflammation and/or neuronal loss have also been induced in these models by the mechanisms of controlled cortical impact [43,44], fluid percussion injury [45,46], weightdrop impact [47], and repetitive mild trauma [40].”
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“TBI not only induces a primary, direct mechanical injury to the brain tissue, but also initiates a secondary, delayed pro‐ gressive brain damage including extensive cell death and degenera‐ tion (Carbonell & Grady, 1999; Stoica & Faden, 2010).”
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“In contrast, cortical herniation through the dura mater causes a focal contusion in the ipsilateral cortex following lateral FPI (Carbonell and Grady, 1999).”
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Two distinct types of dying back axonal degeneration in vitro
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Self-citationExperimental Models of Head Trauma
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Altered Effective Connectivity of Hippocampus-Dependent Episodic Memory Network in mTBI Survivors
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“These results suggest two possibilities concerning the origin of nestin-positive cells: (i) these cells are reactive astrocytes in the acute phase and seizure stimulation causes their proliferation; and (ii) these cells arise from precursor cells of neurons and glia and brain damage, including injury, ischemia and epi…”
ResultBrizuela, M., Blizzard, C. A., Chuckowree, J. A., Pitman, K. A., Young, K. M., & Dickson, T. C. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2017.4977 · Cited by 22 · see citing works
“58 Therefore, cell proliferation in the cortex was evaluated as the presence of newly generated EdU + cells following mild FPI.”
Modelos experimentales de traumatismo craneoencefálico
Prieto, R., Gutiérrez-González, R., Pascual, J., Roda, J., Cerdán, S., Matías-Guíu, J., & Barcia, J. (2009) · Neurocirugía · doi:10.4321/s1130-14732009000300001 · Cited by 20 · see citing works
Paclitaxel Reduces Brain Injury from Repeated Head Trauma in Mice
Cross, D., Meabon, J., Cline, M., Richards, T., Stump, A. J., Cross, C. G., Minoshima, S., Banks, W., & Cook, D. (2019) · Journal of Alzheimer's Disease · doi:10.3233/jad-180871 · Cited by 19 · see citing works
“Synaptic loss is a well-described feature of many animal models of brain injury [43], as well as in clinical TBI [21, 44-47].”
Hånell, A., Clausen, F., Djupsjö, A., Vallstedt, A., Patra, K., Israelsson, C., Larhammar, M., Björk, M., Paixão, S., Kullander, K., et al. (2012) · Journal of Neurotrauma · doi:10.1089/neu.2012.2376 · Cited by 20 · see citing works
“67 70–74 Astrocytic hypertrophy/ astrogliosis may be both beneficial and detrimental post-TBI since astrocytes may have both growth-inhibiting and growth-promoting properties, likely determined by injury model, time post-injury, and location of injury.”
Epidemiology, Risk Factors, and Biomarkers of Post-Traumatic Epilepsy: A Comprehensive Overview
Kazis, D. A., Chatzikonstantinou, S., Ciobica, A. S., Kamal, F. Z., Burlui, V., Călin, G., & Mavroudis, I. A. (2024) · Biomedicines · doi:10.3390/biomedicines12020410 · Cited by 19 · see citing works
Nestin in the Temporal Neocortex of the Intractable Epilepsy Patients
Wang, L., Wang, X.-F., Yuan, J., Xi, Z.-Q., Xue, T., Li, Y.-Q., & Xiao, Z. (2009) · Neurochemical Research · doi:10.1007/s11064-008-9824-4 · Cited by 15
“One was that these cells came from the proliferation and differentiation of ‘‘resting’’ neural precursor cells in epileptic injured regions that mentioned above [20].”
BackgroundInvestigations on Alterations of Hippocampal Circuit Function Following Mild Traumatic Brain Injury
Smith, C. J., Johnson, B. N., Elkind, J. A., See, J., Xiong, G., & Cohen, A. (2012) · Journal of Visualized Experiments · doi:10.3791/4411 · Cited by 14 · see citing works
Ou, F.-Y., Ning, Y., Yang, N., Chen, X., Peng, Y., Zhao, Y., Li, P., Zhou, Y., & Liu, Y. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.113997 · Cited by 11 · see citing works
Resuscitation from experimental traumatic brain injury by magnolol therapy.
Wang, C.-C., Lin, K.-C., Lin, B., Chio, C., & Kuo, J.-R. (2013) · Journal of Surgical Research · doi:10.1016/j.jss.2013.04.059 · Cited by 12 · see citing works
Cao, P., Liang, Y., Gao, X., Zhao, M.-G., & Liang, G.-B. (2013) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12082 · Cited by 12 · see citing works
“The two primary mechanisms for the inflammatory cascade are releasing of upstream proinflammatory cytokines [25] and activation of microglia after TBI [26], which can exacerbate other pathophysiological processes associated with injury [27].”
BackgroundRetractedSuppressive silver methods--a tool for identifying axotomy-induced neuron degeneration.
Grant, G., Holländer, H., & Aldskogius, H. (2004) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2003.10.001 · Cited by 12
Ngwenya, L. B., Mazumder, S., Porter, Z. R., Minnema, A., Oswald, D. J., & Farhadi, H. (2018) · Stem Cells International · doi:10.1155/2018/4209821 · Cited by 11 · see citing works
“Lateral FPI elicits focal and diffuse damage including cortical and subcortical (white matter) hemorrhage, blood-brain barrier breakdown, and diffuse axonal pathology; thus, it mimics human TBI [13, 47, 48].”
BackgroundTraumatic brain injury heterogeneity affects cell death and autophagy
McDonald, B. Z., Tarudji, A. W., Zhang, H., Ryu, S., Eskridge, K. M., & Kievit, F. M. (2024) · Experimental Brain Research · doi:10.1007/s00221-024-06856-1 · Cited by 9 · see citing works
“However, several of the most commonly used models produce moderate to severe injuries plagued by focal contusions, which are underrepresented in the clinical population (Carbonell and Grady 1999; Control and Prevention 2003; Osier and Dixon 2016; Wei et al. 2010).”
Muthuraju, S., Taha, S., Pati, S., Rafique, M., Jaafar, H., & Abdullah, J. (2013) · International Journal of Biomedical Science · doi:10.59566/ijbs.2013.9194 · Cited by 10
“1 atm (5) was rapidly injected into the cranial cavity.”
BackgroundMethodMadathil, S., Deng-Bryant, Y., Wilfred, B. S., Leung, L., Gilsdorf, J. S., & Shear, D. A. (2017) · Journal of Trauma and Acute Care Surgery · doi:10.1097/ta.0000000000001471 · Cited by 9 · see citing works
Janković, T., Dolenec, P., Bumber, J. R., Gržeta, N., Kriz, J., Župan, G., & Pilipović, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212211 · Cited by 8 · see citing works
“For the Western blotting analyses in the LFPI experiment, ipsilateral and contralateral parietal cortices were dissected because, in this TBI model, that is the brain region in which the most serious tissue injury is found [52].”
BackgroundMethodElsaadani, M., Ahmed, S. M., Jacovides, C. L., Lopez, A. J., Johnson, V., Kaplan, L., Smith, D. H., & Pascual, J. (2021) · Journal of Trauma and Acute Care Surgery · doi:10.1097/ta.0000000000003112 · Cited by 7
Delcy, S. A. S., Farrugia, A. M., Nieves, I. A. D., O’Brien, C. A., Bennett, F. C., & Cohen, A. S. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.106178 · Cited by 5 · see citing works
“lFPI is a well-validated model of mild to moderate TBI; it closely replicates the pathology and symptoms observed in humans after concussion (Carbonell and Grady, 1999; Thompson et al., 2005; Xiong et al., 2013; Lyeth, 2016).”
Neuroprotective effect of triptolide on neuronal inflammation in rats with mild brain injury
Fang, Z., Shen, G., Lou, C., Botchway, B. O. A., Lu, Q., Yang, Q.-N., & Amin, N. (2024) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2024.05.007 · Cited by 6 · see citing works
“…TNF-α ) was much higher in studies on neuronal injury, cerebral ischemia, and inflammation, which intensified the inflammatory response (Lisman et al., 2017; Wang et al., 2021a; Carbonell et al., 1998) and promoted the transcription of IL-1 β and NF-κ B in brain tissue (Carbonell and Grady, 1999).”
BackgroundZhao, J.-W., Wang, W., Yan, K., Zhao, H., Zhang, Z., Wang, Y., Zhu, W.-Y., & Chen, S.-W. (2023) · PeerJ · doi:10.7717/peerj.14913 · Cited by 6
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“Similar to existing literature on the difference in the location of impact and regional differences in brain pathology [77, 78], we found that non-invasive traumatic injury to the head, only at the bregma position, exhibited prominent changes in Egr1 gene expression in the TG and elevated gene…”
Strehle, J., Somnuke, P., Li, S., Wang, S., Hirnet, T., Wang, Y., & Schäfer, M. K. E. (2025) · Acta Neuropathologica Communications · doi:10.1186/s40478-025-02156-z · Cited by 6 · see citing works
“Species-specific differences may account for this observation [64].”
Research and Publishing in Neurosurgery
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“1968) investigated effects of acetylcholine in detail [8, 31].”
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Changes in the Cerebral Cortex after Dosed Craniocerebral Trauma in Rats of Different Ages
Komoltsev, I., Levshina, I., Novikova, M., Stepanichev, M., Tishkina, A., & Gulyaeva, N. V. (2016) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-016-0317-7 · Cited by 1
“Clear hemorrhage was seen in the remote damage area [4].”
BackgroundMethodAnimal Models of Traumatic Brain Injury
Clausen, F. (2016) · Neuromethods · doi:10.1007/978-1-4939-3730-1_1 · Cited by 5 · see citing works
Rodent models used in preclinical studies of deep brain stimulation to rescue memory deficits.
Faillot, M., Chaillet, A., Palfi, S., & Senova, S. (2021) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.08.012
What Happens to Concussed Animals?
Victoroff, J. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139696432.006
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Seo, T.-B., & Yoon, J.-H. (2012) · Exercise Science · doi:10.15857/ksep.2012.21.2.255
- Authors
- Carbonell, W. S., & Grady, M. S.
- Affiliations
- University of Pennsylvania (US)
- ORCID
- Carbonell, W. Shawn
- Venue
- Acta Neuropathologica
- Published
- 1999-10-08
- Volume
- 98
- Issue
- 4
- Pages
- 396-406
- ISSN
- 0001-6322 (ISSN-L)
- 1432-0533
- OpenAlex
- W2029497833
- Cited by
- 110
- References
- 0
- Citations by year
- 2025: 2 · 2024: 4 · 2023: 7 · 2022: 2 · 2021: 4 · 2020: 3 · 2019: 4 · 2018: 5 · 2017: 4 · 2016: 5 · 2015: 8 · 2014: 5 · 2013: 4 · 2012: 8
- FWCI
- 1.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Acta Neuropathologica (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5p50ns030305-05, 5r01ns033107-03)
- National Institute of Neurological Disorders and Stroke (NS-30305, NS33107)
- Topics
- Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Automotive and Human Injury Biomechanics
- Keywords
- traumatic brain injury, fluid percussion injury, mouse model, neuronal injury, microglial activation, glial fibrillary acidic protein, white matter degeneration, hippocampus, thalamus, cortex, C57BL/6 mice
- MeSH terms
- Animals, Axons, Coloring Agents, Postural Balance, Glial Fibrillary Acidic Protein, Gliosis, Immunohistochemistry, Male, Mice, Inbred C57BL, Nerve Degeneration, Nerve Tissue Proteins, Neuroglia, Neurons, Time Factors, Silver Staining, Brain Injury, Chronic, Mice
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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