Repetitive mild traumatic brain injury in a mouse model produces learning and memory deficits accompanied by histological changes

Journal of Neurotrauma

Volumn 29, Issue 18, 2012, Pages 2761-2773

  Mouzon, Benoit ^a,b,c   Chaytow, Helena ^a,d   Crynen, Gogce ^a,c   Bachmeier, Corbin ^a,b,c   Stewart, Janice ^e   Mullan, Michael ^a,b,c   Stewart, William ^e,f   Crawford, Fiona ^a,b,c  

^a ROSKAMP INSTITUTE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c OPEN UNIVERSITY   (United Kingdom)

^d CARDIFF UNIVERSITY   (United Kingdom)

^e SOUTHERN GENERAL HOSPITAL   (United Kingdom)

^f UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

behavior; immunohistochemistry; in vivo studies; models of injury; TBI

Indexed keywords

AMYLOID PRECURSOR PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; BRAIN CELL; BRAIN STEM; CELL LOSS; CEREBELLUM; COGNITIVE DEFECT; CONTROLLED STUDY; CORPUS CALLOSUM; ELECTROMAGNETIC FIELD; EXPERIMENTAL MODEL; GLIOSIS; HIPPOCAMPUS; HISTOLOGY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LEARNING DISORDER; MALE; MAZE TEST; MEMORY DISORDER; MOTOR DYSFUNCTION; MOUSE; NONHUMAN; REPRODUCIBILITY; ROTAROD TEST; TRAUMATIC BRAIN INJURY;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; BRAIN CONCUSSION; BRAIN INJURIES; CALCIUM-BINDING PROTEINS; COGNITION; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; LEARNING DISORDERS; MALE; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICROFILAMENT PROTEINS; POSTURAL BALANCE; PSYCHOMOTOR PERFORMANCE; RECURRENCE; REFLEX, RIGHTING;

EID: 84870936795     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2498     Document Type: Article

References (64)

1. .Faul, M., Xu, L., Wald, M.M., and Coronado, V.G. (2010). Traumatic Brain Injury in The United States: Emergency Department Visits, Hospitalizations, and Deaths 2002-2006. Centers for Disease Control and Prevention, National Center for Injury Prevention and Control: Atlanta.
2. Corsellis J.A., Bruton, C.J., Freeman-Browne, D. (1973). The aftermath of boxing. Psychol. Med. 3, 270-303.
3. Guskiewicz, K.M., McCrea, M., Marshall, S.W., Cantu, R.C., Randolph, C., Barr, W., Onate, J.A., and Kelly, J.P. (2003). Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA concussion study. JAMA 290, 2549-2555.
4. Guskiewicz, K.M., Marshall, S.W., Bailes, J., McCrea, M., Cantu, R.C., Randolph, C., and Jordan, B.D. (2005). Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery 57, 719-726.
5. Guskiewicz, K.M., Marshall, S.W., Bailes, J., McCrea, M., Harding, H.P., Matthews, A., Mihalik, J.R., and Cantu, R.C. (2007). Recurrent concussion and risk of depression in retired professional football players. Med. Sci. Sports Exerc. 39, 903-909.
6. Omalu, B.I., DeKosky, S.T., and Minster, R.L. (2005). Chronic traumatic encephalopathy in a national football league player. Neurosurgery 57, 128-134.
7. Omalu, B.I, DeKosky, S.T., and Hamilton, R.L. (2006). Chronic traumatic encephalopathy in a national football league player: part II. Neurosurgery 59, 1086-1092.
8. Omalu, B.I., Hamilton, R.L., Kamboh, M.I., DeKosky, S.T., and Bailes J. (2010). Chronic traumatic encephalopathy in a national football league player: case report and emerging medico-legal practice questions. J. Forensic Nurs. 6, 40-46.
9. Omalu, B.I., Fitzsimmons, R.P., Hammers, J., and Bailes, J. (2010). Chronic traumatic encephalopathy in a professional American wrestler. J. Forensic Nurs. 6, 130-136.
10. Omalu, B., Bailes, J., Hamilton, R.L., Kamboh, M.I., Hammers, J., Case, M., and Fitzsimmons, R. (2011). Emerging histomorphologic phenotypes of chronic traumatic encephalopathy in American athletes. Neurosurgery 69, 173-183.
11. Broglio, S.P., Eckner, J.T., Martini, D., Sosnoff, J.J., Kutcher J.S., and Randolph, C. (2011). Cumulative head impact burden in high school football. J. Neurotrauma 28, 2069-2078.
12. Gavett, B.E., Stern, R.A., Cantu, R.C., Nowinski, C.J., and McKee, A.C. (2010). Mild traumatic brain injury: a risk factor for neurodegeneration. Alzheimers Res. Ther. 2, 18.
13. Gavett, B.E., Stern, R.A., and McKee, A.C. (2011). Chronic traumatic encephalopathy: a potential late effect of sport-related concussive and subconcussive head trauma. Clin. Sports Med. 30, 179-188.
14. Stern, R.A., Riley, D.O., Daneshvar, D.H., Nowinski, C.J., Cantu, R.C., and McKee, A.C. (2011). Long-term consequences of repetitive brain trauma: chronic traumatic encephalopathy. PM R 3, Suppl. 2, S460-467.
15. McKee, A.C., Cantu, R.C., Nowinski, C.J., Hedley-Whyte, E.T., Gavett, B.E., Budson, A.E., Santini,V.E., Lee, H.S., Kubilus, C.A., and Stern, R.A. (2009). Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J. Neuropathol. Exp. Neurol. 68, 709-735.
16. Costanza, A., Weber, K., Gandy, S., Bouras, C., Hof, P.R., Giannakopoulos, P., and Canuto, A. (2011). Contact sport-related chronic traumatic encephalopathy in the elderly: clinical expression and structural substrates. Neuropathol. Appl. Neurobiol. 37, 570-584.
17. Johnson, V.E., Stewart, W., and Smith, D.H. (2010). Traumatic brain injury and amyloid-b pathology: a link to Alzheimer's disease? Nat. Rev. Neurosci. 11, 361-370.
18. Van Den Heuvel, C., Thornton, E., and Vink, R. (2007). Traumatic brain injury and Alzheimer's disease: a review. Prog. Brain Res, 161, 303-316.
19. Fö rstl, H., Haass, C., Hemmer, B., Meyer, B., and Halle, M. (2010). Boxing-acute complications and late sequelae: from concussion to dementia. J. Forensic Nurs. 6, 40-46.
20. Raghupathi, R., and Margulies, S.S. (2002). Traumatic axonal injury after closed head injury in the neonatal pig. J. Neurotrauma 19, 843-853.
21. Raghupathi, R., Mehr, M., Helfaer, M.A., and Margulies, S.S. (2004). Traumatic axonal injury is exacerbated following repetitive closed head injury in the neonatal pig. J. Neurotrauma 21, 307-316.
22. Browne, K.D., Chen, X.H., Meaney, D.F., and Smith, D.H. (2011). Mild traumatic brain injury and diffuse axonal injury in swine. J. Neurotrauma 28, 1747-1755.
23. Gennarelli, T.A., Thibault, L.E., Adams, J.H., Graham, D.I., Thompson, C.J., and Marcincin, R.P. (1982). Diffuse axonal injury and traumatic coma in the primate. Ann. Neurol. 12, 564-574.
24. Laurer, H.L., Bareyre, F.M., and Lee, V.M. (2001). Mild head injury increasing the brain's vulnerability to a second concussive impact. J. Neurosurg. 95, 859-870.
25. DeFord, S.M., Wilson, M.S., and Rice, A.C. (2002). Repeated mild brain injuries result in cognitive impairment in B6C3F1 mice. J. Neurotrauma 19, 427-438.
26. Uryu, K., Laurer, H., McIntosh, T., Praticò, D., Martinez, D., Leight, S., Lee, V.M., and Trojanowski, J.Q. (2002). Repetitive mild brain trauma accelerates Abeta deposition, lipid peroxidation, and cognitive impairment in a transgenic mouse model of Alzheimer amyloidosis. J. Neurosci. 22, 446-454.
27. Longhi, L., Saatman, K.E., Fujimoto, S., Raghupathi, R., Meaney, D.F., Davis, J., McMillan, B.S., Conte, V., Laurer, H.L., Stein, S., Stocchetti, N., and McIntosh, T.K. (2005).Temporal window of vulnerability to repetitive experimental concussive brain injury. Neurosurgery 56, 364-374.
28. Creeley, C.E., Wozniak, D.F., Bayly, P.V., Olney, J.W., and Lewis, L.M. (2004). Multiple episodes of mild traumatic brain injury result in impaired cognitive performance in mice. Acad. Emerg. Med. 11, 809- 819.
29. Nakajima, Y., Horiuchi, Y., Kamata, H., Yukawa, M., Kuwabara, M., and Tsubokawa, T. (2010). Distinct time courses of secondary brain damage in the hippocampus following brain concussion and contusion in rats. Tohoku J. Exp. Med. 221, 229-235.
30. Prins, M.L., Hales, A., Reger, M., Giza, C.C., and Hovda, D.A. (2010). Repeat traumatic brain injury in the juvenile rat is associated with increased axonal injury and cognitive impairments. Dev. Neurosci. 32, 510-518.
31. Shitaka, Y., Tran, H.T., Bennett, R.E., Sanchez, L., Levy, M.A., Dikranian, K., and Brody, D.L. (2011). Repetitive closed-skull traumatic brain injury in mice causes persistent multifocal axonal injury and microglial reactivity. J. Neuropathol. Exp. Neurol. 70, 551-567.
32. Cole, J.T., Yarnell, A., Kean, W.S., Gold, E., Lewis, B., Ren, M., McMullen, D.C., Jacobowitz, D.M., Pollard, H.B., O'Neill, J.T., Grunberg, N.E., Dalgard, C.L., Frank, J.A., and Watson, W.D. (2011). Craniotomy: true sham for traumatic brain injury, or a sham of a sham? J. Neurotrauma 28, 359-369.
33. Brody, D.L., Mac Donald, C., Kessens, C.C., Yuede, C., Parsadanian, M., Spinner, M., Kim, E., Schwetye, K.E., Holtzman, D.M., and Bayly, P.V. (2007). Electromagnetic controlled cortical impact device for precise, graded experimental traumatic brain injury. J. Neurotrauma 24, 657-673.
34. Albert-Weissenberger, C., and Siren, A.L. (2010). Experimental traumatic brain injury. Exp. Transl. Stroke Med. 2, 16.
35. Conte, V., Uryu, K., Fujimoto, S., Yao, Y., Rokach, J., Longhi, L., Trojanowski, J. Q., Lee, V. M.-Y., McIntosh, T. K., and Praticò, D. (2004). Vitamin E reduces amyloidosis and improves cognitive function in Tg2576 mice following repetitive concussive brain injury. J. Neurochem. 90, 758-764.
36. Yoshiyama, Y., Uryu, K., Higuchi, M., Longhi, L., Hoover, R., Fujimoto, S., McIntosh, T., Lee, V.M., and Trojanowski, J.Q. (2005). Enhanced neurofibrillary tangle formation, cerebral atrophy, and cognitive deficits induced by repetitive mild brain injury in a transgenic tauopathy mouse model. J. Neurotrauma 22, 1134-1141.
37. Kane, M.J., Angoa-Pérez, M., Briggs, D.I., Viano, D.C., Kreipke, C.W., and Kuhn, D.M. (2012). A mouse model of human repetitive mild traumatic brain injury. J. Neurosci. Methods 203, 41-49.
38. Franklin, K.B.J., and Paxinos, G. (2001). The Mouse Brain in Stereotaxic Coordinates, 2nd ed. Elsevier/Academic Press: San Diego, London.
39. Ruifrok, A.C., and Johnston, D.A. (2001). Quantification of histochemical staining by color deconvolution. Anal. Quant. Cytol. Histol. 23, 291-299.
40. Park, H.K., Fernandez, I.I., Dujovny, M., and Diaz, F.G. (1999). Experimental animal models of traumatic brain injury: medical and biomechanical mechanism. Crit. Rev. Neurosurg. 9, 44-52.
41. LaPlaca, M.C., Simon, C.M., Prado, G.R., and Cullen, D.K. (2007). CNS injury biomechanics and experimental models. Prog. Brain Res. 161, 13-26.
42. Huh, J.W., Widing, A.G., and Raghupathi, R. (2008).Midline brain injury in the immature rat induces sustained cognitive deficits, bihemispheric axonal injury and neurodegeneration. Exp. Neurol. 213, 84- 92.
43. Guskiewicz, K.M. (2011). Balance assessment in the management of sport-related concussion. Clin. Sports Med. 30, 89-102.
44. Shultz, S.R., Bao, F., Omana, V., Chiu, C., Brown, A., and Cain, D.P. (2012). 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 29, 281-294.
45. Eakin, K., and Miller, J.P. (2012). Mild traumatic brain injury is associated with impaired hippocampal spatiotemporal representation in the absence of histological changes. J. Neurotrauma 29, 1180-1187.
46. Pierce, J.E., Trojanowski, J.Q., Graham, D.I., Smith, D.H., and McIntosh, T.K. (1996). Immunohistochemical characterization of alterations in the distribution of amyloid precursor proteins and betaamyloid peptide after experimental brain injury in the rat. J. Neurosci. 16, 1083-1090.
47. Huh, J.W., Widing, A.G., and Raghupathi, R. (2007). Basic science; repetitive mild non-contusive brain trauma in immature rats exacerbates traumatic axonal injury and axonal calpain activation: a preliminary report. J. Neurotrauma 24, 15-27.
48. Sivanandam, T.M., and Thakur, M.K. (2012). Traumatic brain injury: a risk factor for Alzheimer's disease. Neurosci. Biobehav. Rev. 36, 1376-1381.
49. Hamberger, A., Viano, D.C., Säljö, A., and Bolouri, H. (2009). Concussion in professional football: morphology of brain injuries in the NFL concussion model - part 16. Neurosurgery 64, 1174-1182.
50. Hellewell, S.C., Yan, E.B., Agyapomaa, D.A., Bye, N., and Morganti- Kossmann, M.C. (2010). Post-traumatic hypoxia exacerbates brain tissue damage: analysis of axonal injury and glial responses. J. Neurotrauma 27, 1997-2010.
51. Kelley, B.J., Lifshitz, J., and Povlishock, J.T. (2007). Neuroinflammatory responses after experimental diffuse traumatic brain injury. J. Neuropathol. Exp. Neurol. 66, 989-1001.
52. Chen, S., Pickard, J.D., and Harris, N.G. (2003). Time course of cellular pathology after controlled cortical impact injury. Exp. Neurol. 182, 87-102.
53. Haselkorn, M.L., Shellington, D.K., Jackson, E.K., Vagni, V.A., Janesko-Feldman, K., Dubey, R.K., Gillespie, D.G., Cheng, D., Bell, M.J., Jenkins, L.W., Homanics, G.E., Schnermann, J., and Kochanek, P.M. (2010). Adenosine A1 receptor activation as a brake on the microglial response after experimental traumatic brain injury in mice. J. Neurotrauma 27, 901-910.
54. Neumann, H., Kotter, M.R., and Franklin, R.J. (2009). Debris clearance by microglia: an essential link between degeneration and regeneration. Brain. 132 (Pt. 2), 288-295.
55. Morganti-Kossmann, M.C., Rancan, M., Stahel, P.F., and Kossmann, T. (2002). Inflammatory response in acute traumatic brain injury: a double-edged sword. Curr. Opin. Crit. Care 8, 101-105.
56. Neumann, J., Gunzer, M., Gutzeit, H.O., Ullrich, O., Reymann, K.G., and Dinkel, K. (2006). Microglia provide neuroprotection after ischemia. FASEB J. 20, 714-716.
57. Lalancette-Hebert, M., Gowing, G., Simard, A., Weng, Y.C., and Kriz, J. (2007). Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 27, 2596-2605.
58. Thored, P., Heldmann, U., Gomes-Leal, W., Gisler, R., Darsalia, V., Taneera, J., Nygren, J.M., Jacobsen, S.E.W., Ekdahl, C.T., Kokaia, Z., and Lindvall, O. (2009). Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 57, 835-849.
59. Lloyd, E., Somera-Molina, K., Van Eldik, L.J., Watterson, D.M., and Wainwright, M.S. (2008). Suppression of acute proinflammatory cytokine and chemokine upregulation by post-injury administration of a novel small molecule improves long-term neurologic outcome in a mouse model of traumatic brain injury. J. Neuroinflammation 30, 28.
60. Schmidt, O., Heyde, C., Ertel, W., and Stahel, P. (2005). Closed head injury-an inflammatory disease? Brain Res. Rev. 48, 388-399.
61. Homsi, S., Piaggio, T., Croci, N., Noble, F., Plotkine, M., Marchand- Leroux, C., and Jafarian-Tehrani, M. (2010). Blockade of acute microglial activation by minocycline promotes neuroprotection and reduces locomotor hyperactivity after closed head injury in mice: a twelve-week follow-up study. J. Neurotrauma 27, 911-921.
62. Siopi, E., Cho, A.H., Homsi, S., Croci, N., Plotkine, M., Marchand- Leroux, C., and Jafarian-Tehrani, M. (2011). Minocycline restores sAPPa levels and reduces the late histopathological consequences of traumatic brain injury in mice. J. Neurotrauma 28, 2135-2143.
63. Siopi, E., Calabria, S., Plotkine, M., Marchand-Leroux, C., and Jafarian-Tehrani, M. (2012). Minocycline restores olfactory bulb volume and olfactory behavior after traumatic brain injury in mice. J. Neurotrauma 29, 354-361.
64. Siopi, E., Llufriu-Dabén, G., Fanucchi, F., Plotkine, M., Marchand- Leroux, C., and Jafarian-Tehrani, M. (2012). Evaluation of late cognitive impairment and anxiety states following traumatic brain injury in mice: the effect of minocycline. Neurosci. Lett. 511, 110-115.