Longitudinal characterization of motor and cognitive deficits in a model of penetrating ballistic-like brain injury

Journal of Neurotrauma

Volumn 27, Issue 10, 2010, Pages 1911-1923

  Shear, Deborah A ^a   Lu, Xi Chun May ^a   Bombard, Matthew C ^a,b   Pedersen, Rebecca ^a,b   Chen, Zhiyong ^a   Davis, Angela ^a,b   Tortella, Frank C ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b Geneva Foundation   (United States)

Author keywords

behavioral assessments; cognitive function; models of injury; penetrating ballistic like brain injury; traumatic brain injury

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITION; COGNITIVE DEFECT; LEARNING; MALE; MAZE TEST; MEMORY CONSOLIDATION; NONHUMAN; PENETRATING TRAUMA; RAT; TASK PERFORMANCE; TRAUMATIC BRAIN INJURY;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN INJURIES; COGNITION; FRONTAL LOBE; MALE; MAZE LEARNING; MOTOR ACTIVITY; RATS; RATS, SPRAGUE-DAWLEY; ROTAROD PERFORMANCE TEST; SPATIAL BEHAVIOR;

EID: 77958185183     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1399     Document Type: Article

References (52)

1. Bederson, J. B., Pitts, L. H., Tsuji, M., Nishimura, M. C., Davis, R. L., and Bartkowski, H. (1986). Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 17, 472-476.
2. Bell, R. S., Vo, A. H., Neal, C. J., Tigno, J., Roberts, R., Mossop, C., Dunne, J. R., and Armonda, R. A. (2009). Military traumatic brain and spinal column injury: A 5-year study of the impact blast and other military grade weaponry on the central nervous system. Trauma 66, S104-S111.
3. Blatter, D. D., Bigler, E. D., Gale, S. D., Johnson, S. C., Anderson, C. V., Burnett, B. M., Ryser, D., Macnamara, S. E., and Bailey, B. J. (1997). MR-based brain and cerebrospinal fluid measurement after traumatic brain injury: correlation with neuropsychological outcome. AJNR Am. J. Neuroradiol. 18, 1-10.
4. Bohlen, M., Cameron, A., Metten, P., Crabbe, J. C., and Wahlsten, D. (2009). Calibration of rotational acceleration for the rotarod test of rodent motor coordination. J. Neurosci. Methods 178, 10-14.
5. Carlson, J. N., Visker, K. E., Nielsen, D. M., Keller, R. W., Jr., and Glick, S. D. (1996). Chronic antidepressant drug treatment reduces turning behavior and increases dopamine levels in the medial prefrontal cortex. Brain Res. 707, 122-126.
6. Carter, R. J., Lione, L. A., Humby, T., Mangiarini, L., Mahal, A., Bates, G. P., Dunnett, S. B., and Morton, A. J. (1999). Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J. Neurosci. 19, 3248-3257.
7. Clausen, F., Hanell, A., Bjork, M., Hillered, L., Mir, A. K., Gram, H., and Marklund, N. (2009). Neutralization of interleukin-1beta modifies the inflammatory response and improves histological and cognitive outcome following traumatic brain injury in mice. Eur. J. Neurosci. 30, 385-396.
8. Cowey, A., and Bozek, T. (1974). Contralateral 'neglect' after unilateral dorsomedial prefrontal lesions in rats. Brain Res. 72, 53-63.
9. Daffner, K. R., Mesulam, M. M., Holcomb, P. J., Calvo, V., Acar, D., Chabrerie, A., Kikinis, R., Jolesz, F. A., Rentz, D. M., and Scinto, L. F. (2000b). Disruption of attention to novel events after frontal lobe injury in humans. J. Neurol. Neurosurg. Psychiatry 68, 18-24.
10. Daffner, K. R., Mesulam, M. M., Scinto, L. F., Acar, D., Calvo, V., Faust, R., Chabrerie, A., Kennedy, B., and Holcomb, P. (2000a). The central role of the prefrontal cortex in directing attention to novel events. Brain 123, 927-939.
11. Dunham, N. W., and Miya, T. S. (1957). A note on a simple apparatus for detecting neurological deficit in rats and mice. J. Am. Pharm. Assoc. Am. Pharm. Assoc. (Baltim.) 46, 208-209.
12. Frey, L. C., Hellier, J., Unkart, C., Lepkin, A., Howard, A., Hasebroock, K., Serkova, N., Liang, L., Patel, M., Soltesz, I., and Staley, K. (2009). A novel apparatus for lateral fluid percussion injury in the rat. J. Neurosci. Methods 177, 267-272.
13. Glick, S. D., Jerussi, T. P., and Fleisher, L. N. (1976). Turning in circles: the neuropharmacology of rotation. Life Sci. 18, 889-896.
14. Guyot, L. L., and Michael, D. B. (2000). Post-traumatic hydrocephalus. Neurol. Res. 22, 25-28.
15. Hamm, R. J., Pike, B. R., O'Dell, D. M., Lyeth, B. G., and Jenkins, L. W. (1994). The rotarod test: an evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. J. Neurotrauma 11, 187-196.
16. Hellawell, D. J., Taylor, R. T., and Pentland, B. (1999). Cognitive and psychosocial outcome following moderate or severe traumatic brain injury. Brain Inj. 13, 489-504.
17. Henry, J. D., Phillips, L. H., Crawford, J. R., Kliegel, M., Theodorou, G., and Summers, F. (2007). Traumatic brain injury and prospective memory: influence of task complexity. J. Clin. Exp. Neuropsychol. 29, 457-466.
18. Hochman, M. S. (1983). Rotatory seizures associated with frontal lobe malignant neoplasm: a case report. Epilepsia 24, 11-14.
19. Hoffman, S. W., Fulop, Z., and Stein, D. G. (1994). Bilateral frontal cortical contusion in rats: behavioral and anatomic consequences. J. Neurotrauma 11, 417-431.
20. Jones, B. J., and Roberts, D. J. (1968). The quantiative measurement of motor inco-ordination in naive mice using an acelerating rotarod. J. Pharm. Pharmacol. 20, 302-304.
21. Katz, R. T., Brander, V., and Sahgal, V. (1989). Updates on the diagnosis and management of posttraumatic hydrocephalus. Am. J. Phys. Med. Rehabil. 68, 91-96.
22. Kolb, B. (1984). Functions of the frontal cortex of the rat: a comparative review. Brain Res. 320, 65-98.
23. Lindner, M. D., Plone, M. A., Cain, C. K., Frydel, B., Francis, J. M., Emerich, D. F., and Sutton, R. L. (1998). Dissociable long-term cognitive deficits after frontal versus sensorimotor cortical contusions. J. Neurotrauma 15, 199-216.
24. Lu, X. C., Chen, R. W., Yao, C., Wei, H., Yang, X., Liao, Z., Dave, J. R., and Tortella, F. C. (2009). NNZ-2566, a glypromate analog, improves functional recovery and attenuates apoptosis and inflammation in a rat model of penetrating ballistic-type brain injury. J. Neurotrauma 26, 141-154.
25. Marmarou, A., Foda, M. A., Bandoh, K., Yoshihara, M., Yamamoto, T., Tsuji, O., Zasler, N., Ward, J. D., and Young, H. F. (1996). Posttraumatic ventriculomegaly: hydrocephalus or atrophy? A new approach for diagnosis using CSF dynamics. J. Neurosurg. 85, 1026-1035.
26. Martins, R. S., Siqueira, M. G., Santos, M. T., Zanon-Collange, N., and Moraes, O. J. (2003). Prognostic factors and treatment of penetrating gunshot wounds to the head. Surg. Neurol. 60, 98-104; discussion 104.
27. Mazzini, L., Cossa, F. M., Angelino, E., Campini, R., Pastore, I., and Monaco, F. (2003). Posttraumatic epilepsy: neuroradiologic and neuropsychological assessment of long-term outcome. Epilepsia 44, 569-574.
28. Nestor, S. M., Rupsingh, R., Borrie, M., Smith, M., Accomazzi, V., Wells, J. L., Fogarty, J., and Bartha, R. (2008). Ventricular enlargement as a possible measure of Alzheimer's disease progression validated using the Alzheimer's disease neuroimaging initiative database. Brain 131, 2443-2454.
29. O'Connor, C., Heath, D. L., Cernak, I., Nimmo, A. J., and Vink, R. (2003). Effects of daily versus weekly testing and pretraining on the assessment of neurologic impairment following diffuse traumatic brain injury in rats. J. Neurotrauma 20, 985-993.
30. Owens, B. D., Kragh, J. F., Jr., Wenke, J. C., Macaitis, J., Wade, C. E., and Holcomb, J. B. (2008). Combat wounds in operation Iraqi Freedom and Operation Enduring Freedom. J. Trauma 64, 295-299.
31. Peeling, J., Corbett, D., Del Bigio, M. R., Hudzik, T. J., Campbell, T. M., and Palmer, G. C. (2001). Rat middle cerebral artery occlusion: correlations between histopathology, T2-weighted magnetic resonance imaging, and behavioral indices. J. Stroke Cerebrovasc. Dis. 10, 166-177.
32. Rapoport, M. J., Herrmann, N., Shammi, P., Kiss, A., Phillips, A., and Feinstein, A. (2006). Outcome after traumatic brain injury sustained in older adulthood: a one-year longitudinal study. Am. J. Geriatr. Psychiatry 14, 456-465.
33. Rapoport, M., McCauley, S., Levin, H., Song, J., and Feinstein, A. (2002). The role of injury severity in neurobehavioral outcome 3 months after traumatic brain injury. Neuropsychiatry Neuropsychol. Behav. Neurol. 15, 123-132.
34. Roche, N. L., Moody, A., Szabo, K., Fleming, J. M., and Shum, D. H. (2007). Prospective memory in adults with traumatic brain injury: an analysis of perceived reasons for remembering and forgetting. Neuropsychol. Rehabil. 17, 314-334.
35. Roof, R. L., Schielke, G. P., Ren, X., and Hall, E. D. (2001). A comparison of long-term functional outcome after 2 middle cerebral artery occlusion models in rats. Stroke 32, 2648-2657.
36. Rustay, N. R., Wahlsten, D., and Crabbe, J. C. (2003). Influence of task parameters on rotarod performance and sensitivity to ethanol in mice. Behav. Brain Res. 141, 237-249.
37. Sapsford, W. (2003). Penetrating brain injury in military conflict: does it merit more research? J. R. Army Med. Corps 149, 5-14.
38. Schallert, T., Fleming, S. M., Leasure, J. L., Tillerson, J. L., and Bland, S. T. (2000). CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39, 777-787.
39. Schallert, T., Woodlee, M. T., and Fleming, S. M. (2002). Disentangling multiple types of recovery from brain injury, in: Pharmacology of Cerebral Ischemia. J. Krieglstein (ed), Medpharm Scientific Publishers: Stuttgart, pps. 210-216.
40. Schrimsher, G. W., Billingsley, R. L., Jackson, E. F., and Moore, B. D., 3rd. (2002). Caudate nucleus volume asymmetry predicts attention-deficit hyperactivity disorder (ADHD) symptomatology in children. J. Child Neurol. 17, 877-884.
41. Shaffrey, M. E., Polin, R. S., Phillips, C. D., Germanson, T., Shaffrey, C. I., and Jane, J. A. (1992). Classification of civilian craniocerebral gunshot wounds: a multivariate analysis predictive of mortality. J. Neurotrauma 9 (Suppl. 1), S279-S285.
42. Shear, D. A., Galani, R., Hoffman, S. W., and Stein, D. G. (2002). Progesterone protects against necrotic damage and behavioral abnormalities caused by traumatic brain injury. Exp. Neurol. 178, 59-67.
43. Shear, D. A., Tate, M. C., Archer, D. R., Hoffman, S. W., Hulce, V. D., Laplaca, M. C., and Stein, D. G. (2004). Neural progenitor cell transplants promote long-term functional recovery after traumatic brain injury. Brain Res. 1026, 11-22.
44. Shear, D. A., Williams, A. J., Sharrow, K., Lu, X. C., and Tortella, F. C. (2009). Neuroprotective profile of dextromethorphan in an experimental model of penetrating ballistic-like brain injury. Pharmacol. Biochem. Behav. 94, 56-62.
45. Smith, D. H., Okiyama, K., Thomas, M. J., Claussen, B., and McIntosh, T. K. (1991). Evaluation of memory dysfunction following experimental brain injury using the Morris water maze. J. Neurotrauma 8, 259-269.
46. Thurman, D. J., Alverson, C., Browne, D., Dunn, K. A., Guerrero, J., Johnson, R., Langlois, J. A., Pilkey, D., Sniezek, J. E., and Toal, S. (1999) Traumatic brain injury in the United States-A report to Congress. Centers for Disease Control and Prevention (CDC), National Center for Injury Prevention and Control.
47. Watzman, N., and Barry, H., 3rd. (1968). Drug effects on motor coordination. Psychopharmacologia 12, 414-423.
48. Wei, H. H., Lu, X. C., Shear, D. A., Waghray, A., Yao, C., Tortella, F. C., and Dave, J. R. (2009). NNZ-2566 treatment inhibits neuroinflammation and pro-inflammatory cytokine expression induced by experimental penetrating ballistic-like brain injury in rats. J. Neuroinflammation 6, 19.
49. Williams, A. J., Hartings, J. A., Lu, X. C., Rolli, M. L., and Tortella, F. C. (2006b). Penetrating ballistic-like brain injury in the rat: differential time courses of hemorrhage, cell death, inflammation, and remote degeneration. J. Neurotrauma 23, 1828-1846.
50. Williams, A. J., Hartings, J. A., Lu, X. C., Rolli, M. L., Dave, J. R., and Tortella, F. C. (2005). Characterization of a new rat model of penetrating ballistic brain injury. J. Neurotrauma 22, 313-331.
51. Williams, A. J., Ling, G. S., and Tortella, F. C. (2006a). Severity level and injury track determine outcome following a penetrating ballistic-like brain injury in the rat. Neurosci. Lett. 408, 183-188.
52. Williams, A. J., Wei, H. H., Dave, J. R., and Tortella, F. C. (2007). Acute and delayed neuroinflammatory response following experimental penetrating ballistic brain injury in the rat. J. Neuroinflammation 4, 17.