Abstract
Traumatic brain injury (TBI) remains a significant source of mortality and morbidity throughout the world, in part because of the complex mechanisms. The complexity arises not only from the complicated intracranial biomechanics, but because that mechanical stimulus is only the start of a series of biological responses that unfold over minutes to days after the event. In this chapter, co-authors Nevin Varghese and Barclay Morrison explore the effect on cells of the primary injury that occurs during the mechanical event and the ensuing biological mechanisms of the secondary injury process.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ (2010) Structure and function of the blood-brain barrier. Neurobiol Dis 37:13–25
Ahmed SM, Rzigalinski BA, Willoughby KA, Sitterding HA, Ellis EF (2000) Stretch-induced injury alters mitochondrial membrane potential and cellular ATP in cultured astrocytes and neurons. J Neurochem 74:1951–1960
Ahmed SM, Weber JT, Liang S, Willoughby KA, Sitterding HA, Rzigalinski BA, Ellis EF (2002) NMDA receptor activation contributes to a portion of the decreased mitochondrial membrane potential and elevated intracellular free calcium in strain-injured neurons. J Neurotrauma 19:1619–1629
Ai J, Liu E, Wang J, Chen Y, Yu J, Baker AJ (2007) Calpain inhibitor MDL-28170 reduces the functional and structural deterioration of corpus callosum following fluid percussion injury. J Neurotrauma 24:960–978
Aihara N, Hall JJ, Pitts LH, Fukuda K, Noble LJ (1995) Altered immunoexpression of microglia and macrophages after mild head injury. J Neurotrauma 12:53–63
Allan SM, Tyrrell PJ, Rothwell NJ (2005) Interleukin-1 and neuronal injury. Nat Rev Immunol 5:629–640
Alluri H, Wiggins-Dohlvik K, Davis ML, Huang JH, Tharakan B (2015) Blood-brain barrier dysfunction following traumatic brain injury. Metab Brain Dis 30:1093–1104
Alvarez-Maubecin V, Garcia-Hernandez F, Williams JT, Van Bockstaele EJ (2000) Functional coupling between neurons and glia. J Neurosci 20:4091–4098
Amini M, Ma CL, Farazifard R, Zhu G, Zhang Y, Vanderluit J, Zoltewicz JS, Hage F, Savitt JM, Lagace DC, Slack RS, Beique JC, Baudry M, Greer PA, Bergeron R, Park DS (2013) Conditional disruption of calpain in the CNS alters dendrite morphology, impairs LTP, and promotes neuronal survival following injury. J Neurosci 33:5773–5784
Anderson CM, Swanson RA (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1–14
Ansari MA, Roberts KN, Scheff SW (2008) Oxidative stress and modification of synaptic proteins in hippocampus after traumatic brain injury. Free Radic Biol Med 45:443–452
Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133–1145
Bartha K, Domotor E, Lanza F, Adam-Vizi V, Machovich R (2000) Identification of thrombin receptors in rat brain capillary endothelial cells. J Cereb Blood Flow Metab 20:175–182
Baskaya MK, Rao AM, Dogan A, Donaldson D, Dempsey RJ (1997) The biphasic opening of the blood-brain barrier in the cortex and hippocampus after traumatic brain injury in rats. Neurosci Lett 226:33–36
Bernath E, Kupina N, Liu MC, Hayes RL, Meegan C, Wang KK (2006) Elevation of cytoskeletal protein breakdown in aged Wistar rat brain. Neurobiol Aging 27:624–632
Bi RF, Bi XN, Baudry M (1998) Phosphorylation regulates calpain-mediated truncation of glutamate ionotropic receptors. Brain Res 797:154–158
Blanc EM, Bruce-Keller AJ, Mattson MP (1998) Astrocytic gap junctional communication decreases neuronal vulnerability to oxidative stress-induced disruption of Ca2+ homeostasis and cell death. J Neurochem 70:958–970
Boron WF, Boulpaep EL (2017) Medical physiology. Elsevier, Philadelphia, PA
Bowman CL, Ding JP, Sachs F, Sokabe M (1992) Mechanotransducing ion channels in astrocytes. Brain Res 584:272–286
Brailoiu E, Shipsky MM, Yan G, Abood ME, Brailoiu GC (2017) Mechanisms of modulation of brain microvascular endothelial cells function by thrombin. Brain Res 1657:167–175
Cagmat EB, Guingab-Cagmat JD, Vakulenko AV, Hayes RL, Anagli J (2015) Potential use of calpain inhibitors as brain injury therapy. In: Kobeissy FH (ed) Brain neurotrauma: molecular, neuropsychological, and rehabilitation aspects. CRC Press, Boca Raton (FL)
Cargill RS, Thibault LE (1996) Acute alterations in [Ca2+]i in NG108-15 cells subjected to high strain rate deformation and chemical hypoxia: an in vitro model for neural trauma. J Neurotrauma 13:395–407
Crocker SJ, Smith PD, Jackson-Lewis V, Lamba WR, Hayley SP, Grimm E, Callaghan SM, Slack RS, Melloni E, Przedborski S, Robertson GS, Anisman H, Merali Z, Park DS (2003) Inhibition of calpains prevents neuronal and behavioral deficits in an MPTP mouse model of parkinson’s disease. J Neurosci 23:4081–4091
Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341(Pt 2):233–249
Cullen DK, Vernekar VN, Laplaca MC (2011) Trauma-induced plasmalemma disruptions in three-dimensional neural cultures are dependent on strain modality and rate. J Neurotrauma 28:2219–2233
Daneman R, Prat A (2015) The blood-brain barrier. Cold Spring Harb Perspect Biol 7:a020412
del Cerro S, Larson J, Oliver MW, Lynch G (1990) Development of hippocampal long-term potentiation is reduced by recently introduced calpain inhibitors. Brain Res 530:91–95
Domoki F, Kis B, Gaspar T, Bari F, Busija DW (2008) Cerebromicrovascular endothelial cells are resistant to l-glutamate. Am J Physiol Regul Integr Comp Physiol 295:R1099–R1108
Dugan LL, Sensi SL, Canzoniero LM, Handran SD, Rothman SM, Lin TS, Goldberg MP, Choi DW (1995) Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-d-aspartate. J Neurosci 15:6377–6388
Engl E, Attwell D (2015) Non-signalling energy use in the brain. J Physiol 593:3417–3429
Farkas O, Lifshitz J, Povlishock JT (2006) Mechanoporation induced by diffuse traumatic brain injury: an irreversible or reversible response to injury? J Neurosci 26:3130–3140
Ferreira A, Bigio EH (2011) Calpain-mediated tau cleavage: a mechanism leading to neurodegeneration shared by multiple tauopathies. Mol Med 17:676–685
Floyd CL, Gorin FA, Lyeth BG (2005) Mechanical strain injury increases intracellular sodium and reverses Na+/Ca2+ exchange in cortical astrocytes. Glia 51:35–46
Foo K, Blumenthal L, Man HY (2012) Regulation of neuronal bioenergy homeostasis by glutamate. Neurochem Int 61:389–396
Franze K, Gerdelmann J, Weick M, Betz T, Pawlizak S, Lakadamyali M, Bayer J, Rillich K, Gogler M, Lu YB, Reichenbach A, Janmey P, Kas J (2009) Neurite branch retraction is caused by a threshold-dependent mechanical impact. Biophys J 97:1883–1890
Gafni J, Ellerby LM (2002) Calpain activation in huntington’s disease. J Neurosci 22:4842–4849
Gafni J, Hermel E, Young JE, Wellington CL, Hayden MR, Ellerby LM (2004) Inhibition of calpain cleavage of huntingtin reduces toxicity: Accumulation of calpain/caspase fragments in the nucleus. J Biol Chem 279:20211–20220
Galbraith JA, Thibault LE, Matteson DR (1993) Mechanical and electrical responses of the giant squid axon to simple elongation. J Biomech Eng 115:13–22
Ganot G, Wong BS, Binstock L, Ehrenstein G (1981) Reversal potentials corresponding to mechanical stimulation and leakage current in myxicola giant axons. Biochem Biophys Acta 649:487–491
Geddes DM, Cargill RS, Laplaca MC (2003) Mechanical stretch to neurons results in a strain rate and magnitude-dependent increase in plasma membrane permeability. J Neurotrauma 20:1039–1049
Grammer M, Kuchay S, Chishti A, Baudry M (2005) Lack of phenotype for LTP and fear conditioning learning in calpain 1 knock-out mice. Neurobiol Learn Mem 84:222–227
Hall ED, Detloff MR, Johnson K, Kupina NC (2004) Peroxynitrite-mediated protein nitration and lipid peroxidation in a mouse model of traumatic brain injury. J Neurotrauma 21:9–20
Hall ED, Vaishnav RA, Mustafa AG (2010) Antioxidant therapies for traumatic brain injury. Neurotherapeutics 7:51–61
Hall ED, Yonkers PA, Andrus PK, Cox JW, Anderson DK (1992) Biochemistry and pharmacology of lipid antioxidants in acute brain and spinal cord injury. J Neurotrauma 9:S425–S442
Hamakubo T, Kannagi R, Murachi T, Matus A (1986) Distribution of calpains I and II in rat brain. J Neurosci 6:3103–3111
Harwood SM, Yaqoob MM, Allen DA (2005) Caspase and calpain function in cell death: bridging the gap between apoptosis and necrosis. Ann Clin Biochem 42:415–431
Hayes RL, Katayama Y, Young HF, Dunbar JG (1988) Coma associated with flaccidity produced by fluid-percussion concussion in the cat. I: Is it due to depression of activity within the brainstem reticular formation? Brain Inj 2:31–49
Hicks RR, Baldwin SA, Scheff SW (1997) Serum extravasation and cytoskeletal alterations following traumatic brain injury in rats. Comparison of lateral fluid percussion and cortical impact models. Mol Chem Neuropathol 32:1–16
Hooper C, Pinteaux-Jones F, Fry VA, Sevastou IG, Baker D, Heales SJ, Pocock JM (2009) Differential effects of albumin on microglia and macrophages; implications for neurodegeneration following blood-brain barrier damage. J Neurochem 109:694–705
Hooper C, Taylor DL, Pocock JM (2005) Pure albumin is a potent trigger of calcium signalling and proliferation in microglia but not macrophages or astrocytes. J Neurochem 92:1363–1376
Hovda DA, Yoshino A, Kawamata T, Katayama Y, Becker DP (1991) Diffuse prolonged depression of cerebral oxidative metabolism following concussive brain injury in the rat: a cytochrome oxidase histochemistry study. Brain Res 567:1–10
Howarth C, Gleeson P, Attwell D (2012) Updated energy budgets for neural computation in the neocortex and cerebellum. J Cereb Blood Flow Metab 32:1222–1232
Hue CD, Cao S, Haider SF, Vo KV, Effgen GB, Vogel E III, Panzer MB, Bass CR, Meaney DF, Morrison B III (2013) Blood-brain barrier dysfunction after primary blast injury in vitro. J Neurotrauma 30:1652–1663
Hue CD, Cho FS, CaoS Nicholls RE, Vogel Iii EW, Sibindi C, Arancio O, Dale Bass CR, Meaney DF, Morrison B III (2016) Time course and size of blood-brain barrier opening in a mouse model of blast-induced traumatic brain injury. J Neurotrauma 33:1202–1211
Jeffs GJ, Meloni BP, Bakker AJ, Knuckey NW (2007) The role of the Na(+)/Ca(2+) exchanger (NCX) in neurons following ischaemia. J Clin Neurosci 14:507–514
Johnson GV, Jope RS (1992) The role of microtubule-associated protein 2 (map-2) in neuronal growth, plasticity, and degeneration. J Neurosci Res 33:505–512
Jolivet R, Magistretti PJ, Weber B (2009) Deciphering neuron-glia compartmentalization in cortical energy metabolism. Front Neuroenergetics 1:4
Julian FJ, Goldman DE (1962) The effects of mechanical stimulation on some electrical properties of axons. J Gen Physiol 46:297–313
Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305:99–103
Katayama Y, Becker DP, Tamura T, Hovda DA (1990) Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 73:889–900
Khatri N, Man HY (2013) Synaptic activity and bioenergy homeostasis: implications in brain trauma and neurodegenerative diseases. Front Neurol 4:199
Khorchid A, Ikura M (2002) How calpain is activated by calcium. Nature Struc Biol 9:239
Kilinc D, Gallo G, Barbee KA (2008) Mechanically-induced membrane poration causes axonal beading and localized cytoskeletal damage. Exp Neurol 212:422–430
Kirichok Y, Krapivinsky G, Clapham DE (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427:360–364
Kobeissy FH, Liu MC, Yang Z, Zhang Z, Zheng W, Glushakova O, Mondello S, Anagli J, Hayes RL, Wang KK (2015) Degradation of betaii-spectrin protein by calpain-2 and caspase-3 under neurotoxic and traumatic brain injury conditions. Mol Neurobiol 52:696–709
Kurbatskaya K, Phillips EC, Croft CL, Dentoni G, Hughes MM, Wade MA, Al-Sarraj S, Troakes C, O’Neill MJ, Perez-Nievas BG, Hanger DP, Noble W (2016) Upregulation of calpain activity precedes tau phosphorylation and loss of synaptic proteins in alzheimer’s disease brain. Acta Neuropathol Commun 4:34
Kuriakose M, Rama Rao KV, Younger D, Chandra N (2018) Temporal and spatial effects of blast overpressure on blood-brain barrier permeability in traumatic brain injury. Sci Rep 8:8681
Laplaca MC, Lee VMY, Thibault LE (1997) An in vitro model of traumatic neuronal injury: loading rate-dependent changes in acute cytosolic calcium and lactate dehydrogenase release. J Neurotrauma 14:355–368
Laplaca MC, Prado GR, Cullen D, Simon CM (2009) Plasma membrane damage as a marker of neuronal injury. Conf Proc IEEE Eng Med Biol Soc 2009:1113–1116
Liao Y, Liu P, Guo F, Zhang ZY, Zhang Z (2013) Oxidative burst of circulating neutrophils following traumatic brain injury in human. PLoS ONE 8:e68963
Lifshitz J, Friberg H, Neumar RW, Raghupathi R, Welsh FA, Janmey P, Saatman KE, Wieloch T, Grady MS, McIntosh TK (2003) Structural and functional damage sustained by mitochondria after traumatic brain injury in the rat: evidence for differentially sensitive populations in the cortex and hippocampus. J Cereb Blood Flow Metab 23:219–231
Liu J, Wang Y, Zhuang Q, Chen M, Wang Y, Hou L, Han F (2016) Protective effects of cyclosporine a and hypothermia on neuronal mitochondria in a rat asphyxial cardiac arrest model. Am J Emerg Med 34:1080–1085
Lusardi TA, Smith DH, Wolf JA, Meaney DF (2003) The separate roles of calcium and mechanical forces in mediating cell death in mechanically injured neurons. Biorheology 40:401–409
Lynch G, Baudry M (1987) Brain spectrin, calpain and long-term changes in synaptic efficacy. Brain Res Bull 18:809–815
Ma M, Shofer FS, Neumar RW (2012) Calpastatin overexpression protects axonal transport in an in vivo model of traumatic axonal injury. J Neurotrauma 29:2555–2563
Mazzeo AT, Beat A, Singh A, Bullock MR (2009) The role of mitochondrial transition pore, and its modulation, in traumatic brain injury and delayed neurodegeneration after tbi. Exp Neurol 218:363–370
Melloni E, Salamino F, Sparatore B (1992) The calpain-calpastatin system in mammalian cells: properties and possible functions. Biochimie 74:217–223
Moldoveanu T, Hosfield CM, Lim D, Elce JS, Jia Z, Davies PL (2002) A Ca(2+) switch aligns the active site of calpain. Cell 108:649–660
Moller T, Hanisch UK, Ransom BR (2000) Thrombin-induced activation of cultured rodent microglia. J Neurochem 75:1539–1547
Momeni HR (2011) Role of calpain in apoptosis. Cell J 13:65–72
Mustafa AG, Singh IN, Wang J, Carrico KM, Hall ED (2010) Mitochondrial protection after traumatic brain injury by scavenging lipid peroxyl radicals. J Neurochem 114:271–280
Nilsson P, Hillered L, Ponten U, Ungerstedt U (1990) Changes in cortical extracellular levels of energy-related metabolites and amino acids following concussive brain injury in rats. J Cereb Blood Flow Metab 10:631–637
Pardridge WM (1998) CNS drug design based on principles of blood-brain barrier transport. J Neurochem 70:1781–1792
Pellerin L, Magistretti PJ (2003) How to balance the brain energy budget while spending glucose differently. J Physiol 546:325
Pettigrew LC, Holtz ML, Craddock SD, Minger SL, Hall N, Geddes JW (1996) Microtubular proteolysis in focal cerebral ischemia. J Cereb Blood Flow Metab 16:1189–1202
Pettus EH, Christman CW, Giebel ML, Povlishock JT (1994) Traumatically induced altered membrane permeability: its relationship to traumatically induced reactive axonal change. J Neurotrauma 11:507–522
Prado GR, Ross JD, Deweerth SP, Laplaca MC (2005) Mechanical trauma induces immediate changes in neuronal network activity. J Neural Eng 2:148–158
Raichle ME, Gusnard DA (2002) Appraising the brain’s energy budget. Proc Natl Acad Sci USA 99:10237–10239
Rose CR, Konnerth A (2001) NMDA receptor-mediated Na+ signals in spines and dendrites. J Neurosci 21:4207–4214
Ryu J, Pyo H, Jou I, Joe E (2000) Thrombin induces NO release from cultured rat microglia via protein kinase C, mitogen-activated protein kinase, and NF-kappa B. J Biol Chem 275:2995559
Rzigalinski BA, Weber JT, Willoughby KA, Ellis EF (1998) Intracellular free calcium dynamics in stretch-injured astrocytes. J Neurochem 70:2377–2385
Saatman KE, Graham DI, McIntosh TK (1998) The neuronal cytoskeleton is at risk after mild and moderate brain injury. J Neurotrauma 15:1047–1058
Samantaray S, Ray SK, Banik NL (2008) Calpain as a potential therapeutic target in parkinson’s disease. CNS Neurol Disord Drug Targets 7:305–312
Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, Cassatella MA (2000) The neutrophil as a cellular source of chemokines. Immunol Rev 177:195–203
Sengpiel B, Preis E, Krieglstein J, Prehn JH (1998) NMDA-induced superoxide production and neurotoxicity in cultured rat hippocampal neurons: role of mitochondria. Euro J Neurosci 10:1903–1910
Shapira Y, Setton D, Artru AA, Shohami E (1993) Blood-brain barrier permeability, cerebral edema, and neurologic function after closed head injury in rats. Anesth Analg 77:141–148
Shen J, Petersen KF, Behar KL, Brown P, Nixon TW, Mason GF, Petroff OA, Shulman GI, Shulman RG, Rothman DL (1999) Determination of the rate of the glutamate/glutamine cycle in the human brain by in vivo 13C NMR. Proc Natl Acad Sci USA 96:8235–8240
Shi R, Blight AR (1996) Compression injury of mammalian spinal cord in vitro and the dynamics of action potential conduction failure. J Neurophysiol 76:1572–1580
Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, Shulman RG (1998) Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci USA 95:316–321
Singh IN, Sullivan PG, Deng Y, Mbye LH, Hall ED (2006) Time course of post-traumatic mitochondrial oxidative damage and dysfunction in a mouse model of focal traumatic brain injury: implications for neuroprotective therapy. J Cereb Blood Flow Metab 26:1407–1418
Smith SL, Andrus PK, Zhang JR, Hall ED (1994) Direct measurement of hydroxyl radicals, lipid peroxidation, and blood-brain barrier disruption following unilateral cortical impact head injury in the rat. J Neurotrauma 11:393–404
Staubli U, Larson J, Thibault O, Baudry M, Lynch G (1988) Chronic administration of a thiol-proteinase inhibitor blocks long-term potentiation of synaptic responses. Brain Res 444:153–158
Takahashi H, Manaka S, Sano K (1981) Changes in extracellular potassium concentration in cortex and brain stem during the acute phase of experimental closed head injury. J Neurosurg 55:708–717
Tanaka H, Katayama Y, Kawamata T, Tsubokawa T (1994) Excitatory amino acid release from contused brain tissue into surrounding brain areas. Acta Neurochir Suppl (Wien) 60:524–527
Tecoma ES, Monyer H, Goldberg MP, Choi DW (1989) Traumatic neuronal injury in vitro is attenuated by NMDA antagonists. Neuron 2:1541–1545
Thibault LE, Nahum AM, Melvin JW (1993) Isolated tissue and cellular biomechanics. In: Accidental injury: biomechanics and prevention. New York: Springer-Verlag
Vega-Zelaya L, Ortega GJ, Sola RG, Pastor J (2014) Plasma albumin induces cytosolic calcium oscillations and DNA synthesis in human cultured astrocytes. Biomed Res Int 2014:539140
Verweij BH, Muizelaar JP, Vinas FC, Peterson PL, Xiong Y, Lee CP (2000) Impaired cerebral mitochondrial function after traumatic brain injury in humans. J Neurosurg 93:815–820
Vinade L, Petersen JD, Do K, Dosemeci A, Reese TS (2001) Activation of calpain may alter the postsynaptic density structure and modulate anchoring of NMDA receptors. Synapse 40:302–309
Vogel EW III, Rwema SH, Meaney DF, Bass CR, Morrison B III (2017) Primary blast injury depressed hippocampal long-term potentiation through disruption of synaptic proteins. J Neurotrauma 34:1063–1073
Vosler PS, Brennan CS, Chen J (2008) Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration. Mol Neurobiol 38:78–100
Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L (2014) The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol 13:1045–1060
Watanabe J, Shetty AK, Hattiangady B, Kim DK, Foraker JE, Nishida H, Prockop DJ (2013) Administration of TSG-6 improves memory after traumatic brain injury in mice. Neurobiol Dis 59:86–99
White RJ, Reynolds IJ (1995) Mitochondria and Na+/Ca2+ exchange buffer glutamate-induced calcium loads in cultured cortical neurons. J Neurosci 15:1318–1328
White RJ, Reynolds IJ (1996) Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J Neurosci 16:5688–5697
Wiggins-Dohlvik K, Merriman M, Shaji CA, Alluri H, Grimsley M, Davis ML, Smith RW, Tharakan B (2014) Tumor necrosis factor-alpha disruption of brain endothelial cell barrier is mediated through matrix metalloproteinase-9. Am J Surg 208:954–960; discussion 60
Willard SS, Koochekpour S (2013) Glutamate, glutamate receptors, and downstream signaling pathways. Int J Biol Sci 9:948–959
Wolburg H, Lippoldt A (2002) Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul Pharmacol 38:323–337
Wolf JA, Stys PK, Lusardi T, Meaney D, Smith DH (2001) Traumatic axonal injury induces calcium influx modulated by tetrodotoxin-sensitive sodium channels. J Neurosci 21:1923–1930
Won SM, Lee JH, Park UJ, Gwag J, Gwag BJ, Lee YB (2011) Iron mediates endothelial cell damage and blood-brain barrier opening in the hippocampus after transient forebrain ischemia in rats. Exp Mol Med 43:121–128
Xiong Y, Gu Q, Peterson PL, Muizelaar JP, Lee CP (1997) Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury. J Neurotrauma 14:23–34
Yang Y, Estrada EY, Thompson JF, Liu W, Rosenberg GA (2007) Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab 27:697–709
Yu SP, Yeh C, Strasser U, Tian M, Choi DW (1999) NMDA receptor-mediated K+ efflux and neuronal apoptosis. Science 284:336–339
Yu Y, Herman P, Rothman DL, Agarwal D, Hyder F (2017) Evaluating the gray and white matter energy budgets of human brain function. J Cereb Blood Flow Metab: 271678x17708691
Zhao X, Gorin FA, Berman RF, Lyeth BG (2008) Differential hippocampal protection when blocking intracellular sodium and calcium entry during traumatic brain injury in rats. J Neurotrauma 25:1195–1205
Zhu XH, Qiao H, Du F, Xiong Q, Liu X, Zhang X, Ugurbil K, Chen W (2012) Quantitative imaging of energy expenditure in human brain. Neuroimage 60:2107–2117
Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6:43–50
Author information
Authors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Schmitt, KU., Niederer, P.F., Cronin, D.S., Morrison III, B., Muser, M.H., Walz, F. (2019). Cellular Injury Biomechanics of Central Nervous System Trauma. In: Trauma Biomechanics. Springer, Cham. https://doi.org/10.1007/978-3-030-11659-0_3
Download citation
DOI: https://doi.org/10.1007/978-3-030-11659-0_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-11658-3
Online ISBN: 978-3-030-11659-0
eBook Packages: EngineeringEngineering (R0)