Comparing the predictive value of multiple cognitive, affective, and motor tasks after rodent traumatic brain injury

Journal of Neurotrauma

Volumn 29, Issue 15, 2012, Pages 2475-2489

  Zhao, Zaorui ^a   Loane, David J ^a   Murray, Michael G ^a   Stoica, Bogdan A ^a   Faden, Alan I ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

behavior; composite score; controlled cortical impact; correlation; traumatic brain injury

Indexed keywords

ISOFLURANE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DAMAGE; BRAIN INJURY; COGNITIVE DEFECT; CONTROLLED STUDY; HISTOPATHOLOGY; INJURY SEVERITY; LEARNING; MALE; MAZE TEST; MEMORY; MOOD DISORDER; MOTOR PERFORMANCE; MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; OPEN FIELD TEST; PASSIVE AVOIDANCE; PREDICTIVE VALUE; SCORING SYSTEM; SCREENING; TRAUMATIC BRAIN INJURY; WALKING;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN INJURIES; DISEASE MODELS, ANIMAL; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PREDICTIVE VALUE OF TESTS; RECOVERY OF FUNCTION; SEVERITY OF ILLNESS INDEX;

EID: 84867506098     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2511     Document Type: Article

References (75)

1. Roberts, G.W., Allsop, D., and Bruton, C. (1990). The occult aftermath of boxing. J. Neurol. Neurosurg. Psychiatry 53, 373-378.
2. Levy, M.L., Ozgur, B.M., Berry, C., Aryan, H.E., and Apuzzo, M.L. (2004). Analysis and evolution of head injury in football. Neurosur-gery 55, 649-655.
3. 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.
4. Warden, D. (2006). Military TBI during the Iraq and Afghanistan wars. J. Head Trauma Rehabil. 21, 398-402.
5. Loane, D.J., and Faden, A.L. (2010). Neuroprotection for traumatic brain injury: translational challenges and emerging therapeutic strategies. Trends Pharmacol. Sci. 31, 596-604.
6. Bilgen, M. (2005). A new device for experimental modeling of central nervous system injuries. Neurorehabil. Neural Repair 19, 219-226.
7. Brody, D.L., Mac Donald, C., Kessens, C.C., Yuede, C., Parsandanian, M., Spinner, M., Kim, E., Schwetye, K.E., Holtzman, D.M., and Bayly, P.V. (2008). Electromagnetic controlled cortical impact device for precise, graded experimental traumatic brain injury. J. Neuro-trauma 24, 657-673.
8. Faden, A.I., Fox, G.B., Fan, L., Araldi, G.L., Qiao, L., Wang, S., and Kozikowski, A.P. (1999). Novel TRH analogy improves motor and cognitive recovery after traumatic brain injury in rodents. Am. J. Physiol. 277, R1196-R1204.
9. Faden, A.I., Fox, G.B., Di, X., Knoblach, S.M., Cernak, I., Mullins, P., Nikolaeva, M., and Kozikowski, A.P. (2003a). Neuroprotective and nootropic actions of a novel cyclized dipeptide after controlled cortical impact injury in mice. J. Cereb. Blood Flow Metab. 23, 355-363.
10. Hamm, R.J., Dixon, C.E., and Gbadebo, D.M. (1992). Cognitive deficits following traumatic brain injury produced by controlled cortical impact. J. Neurotrauma 9, 11-20.
11. Smith, D.H., Soares, H.D., Pierce, J.S., Perlman, K.G., Saatman, K.E., Meaney, D.F., Dixon, C.E., and McIntosh, T.K. (1995). A model of parasagittal controlled cortical impact in the mouse: cognitive and histopathologic effects. J. Neurotrauma 12, 169-178.
12. Fox, G.B., Fan, L., Levasseur, R.A., and Faden, A.I. (1998b). Sustained sensory/motor and cognitive deficits with neuronal apoptosis following controlled cortical impact brain injury in the mouse. J. Neurotrauma 15, 599-614.
13. You, Z., Savitz, S.I., Yang, J., Degterev, A., Yuan, J., Cuny, G.D., Moskowitz, M.A., and Whalen, M.J. (2008). Necrostatin-1 reduces histopathology and improves functional outcome after controlled cortical impact. J. Cereb. Blood Flow Metab. 28, 1564-1573.
14. Mbye, L.H., Singh, I.N., Carrico, K.M., Saatman, K.E., and Hall, E.D. (2008). Comparative neuroprotective effects of cyclosporin A and NIM811, a nonimmunosuppressive cyclosporin A analog, following traumatic brain injury. J. Cereb. Blood Flow Metab. 29, 87-97.
15. Yu, S., Kaneko, Y., Bae, E., Stahl, C.E., Wang, Y., Van Loveren, H., Sanberg, P.R., and Borlongan, C.V. (2009). Severity of controlled cortical impact traumatic brain injury in rats and mice dictates degree of behavioral deficits. Brain Res. 1287, 157-163.
16. Chauhan et al., 2010
17. Dixon, C.E., Clifton, G.L., Lighthall, J.W., Yaghmai, A.A., and Hayes, R.L. (1991). A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39, 253-262.
18. Goodman, J.C., Cherian, L., Bryan, R.M., and Robertson, C.S. (1994). Lateral cortical impact injury in rats: pathologic effects of varying cortical compression and impact velocity. J. Neurotrauma 11, 587-597.
19. Saatman, K.E., Feeko, K.J., Pape, R.L., and Raghupathi, R. (2006). Differential behavioral and histopathological responses to graded cortical impact injury in mice. J. Neurotrauma 23, 1241-1253.
20. Faden, A.I., Knoblach, S.M., Cernak, I., Fan, L., Vink, R., Araldi, G.L., Fricke, S.T., Roth, B.L., and Kozikowski, A.P. (2003b). Novel diketopiperazine enhances motor and cognitive recovery after traumatic brain injury in rats and shows neuroprotection in vitro and in vivo. J. Cereb. Blood Flow Metab. 23, 342-354.
21. Fox, G.B., and Faden, A.I. (1998a). Traumatic brain injury causes delayed motor and cognitive impairment in a mutant mouse strain known to exhibit delayed wallerian degeneration. J. Neurosci. Res. 53, 718-727.
22. Duffy, S., Labrie, V., and Roder, J.C. (2008). D-serine augments NMDA-NR2B receptor-dependent hippocampal long-term depression and spatial reversal learning. Neuropsychopharmacology 33, 1004-1018.
23. Xu, J., Zhu, Y., Contractor, A., and Heinemann, S.F. (2009). mGluR5 has a critical role in inhibitory learning. J. Neurosci. 29, 3676-3684.
24. Brody, D.L., and Holtzman, D.M. (2006). Morris water maze search strategy analysis in PDAPP mice before and after experimental traumatic brain injury. Exp. Neurol. 197, 330-340.
25. Janus, C. (2004). Search strategies used by APP transgenic mice during navigation in the Morris water maze. Learn. Mem. 11, 337-346.
26. Gresack, J.E., Kerr, K.M., and Frick, K.M. (2007). Life-long environmental enrichment differentially affects the mnemonic response to estrogen in young, middle-aged, and aged female mice. Neurobiol. Learn. Mem. 88, 393-408.
27. Zhao, Z., Fan, L., and Frick, K.M. (2010). Epigenetic alterations regulate estradiol-induced enhancement of memory consolidation. Proc. Natl. Acad. Sci. USA 107, 5605-5610.
28. Clark, R.E., Zola, S.M., Squire, L.R. (2000). Impaired recognition memory in rats after damage to the hippocampus. J. Neurosci. 2, 8853-8860.
29. Milman, A., Rosenberg, A., Weizman, R., and Pick, C.G. (2005). Mild traumatic brain injury induces persistent cognitive deficits and behavioral disturbances in mice. J. Neurotrauma 22, 1003-1010.
30. Steru, R.C., Thierry, B., and Simon, P. (1985). The tail suspension test: a new method for screening antidepressants in mice. Psycho-pharmacology (Berl.) 85, 367-370.
31. Cryan, J.F., Mombereau, C., and Vassout, A. (2005). The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci. Biobehav. Rev. 29, 571-625.
32. Zhang, H.T., Huang, Y., Masood, A., Stolinski, L.R., Li, Y., Zhang, L., Dlaboga, D., Jin, S.-L.C., Conti, M., and O'Donnell, J.M. (2008). Anxiogenic-like behavioral phenotype of mice deficient in phospho-diesterase 4B (PDE4B). Neruopsychopharmacology 33, 1611-1623.
33. Kabadi, S.V., Stoica, B.A., Byrnes, K.R., Hanscom, M., Loane, D.J., and Faden, A.I. (2012). Selective CDK inhibitor limits neuroinflammation and progressive neurodegeneration after brain trauma. J. Cereb. Blood Flow Metab. 32, 137-149.
34. Lister, R.G. (1987). The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl.) 92, 180-185.
35. Schwarzbold, M.L., Rial, D., De Bem, T.D., Machado, D.D., Cunha, M.P., Dos Santos, A.A., Dos Santos, D.B., Figueiredo, C.P., Farina, M., Goldfeder, E.M., Rodrigues, A.L., Prediger, R.D., and Walz, R. (2010). Effects of traumatic brain injury of different severity on emotional, cognitive and oxidative stress-related parameters in mice. J. Neurotrauma 27, 1883-1893.
36. Morris, R.G.M. (1984). Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47-60.
37. Whiting, M.D., Baranova, A.I., and Hamm R.J. (2006). Cognitive impairment following traumatic brain injury, in: Animal Models of Cognitive Impairment. E.D. Levin and J.J. Buccafusco, (eds). CRC Press, Boca Raton, FL, Chap. 14.
38. Rossato, J.I., Bevilaqua, L.R., Medina, J.H., Izquierdo, I., and Cam-marota, M. (2006). Retrieval induces hippocampal-dependent reconsolidation of spatial memory. Learn. Mem. 13, 431-440.
39. Varvel, S.A., Anum, E.A., and Lichtman, A.H. (2005). Disruption of CB(1) receptor signaling impairs extinction of spatial memory in mice. Psychopharmacology 179, 863-872.
40. Lattal, K.M., and Abel, T. (2001). Different requirements for protein synthesis in acquisition and extinction of spatial preferences and context-evoked fear. J. Neurosci. 21, 5773-5780.
41. Bouton, M.E. (1993). Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol. Bull. 114, 80-99.
42. Labrie, V., Duffy, S., Wang, W., Barger, S.W., Baker, G.B., and Roder, J.C. (2009). Genetic inactivation of D-amino acid oxidase enhances extinction and reversal learning in mice. Learn. Mem. 16, 28-37.
43. Morris, R.G.M., Garrud, P., Rawlins, J.N.P., and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683.
44. Barnes, C.A. (1979). Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 93, 74-104.
45. O'Leary, T.P., Savoie, V., and Brown, R.E. (2011). Learning, memory and search strategies of inbred mouse strains with different visual abilities in the Barnes maze. Behav. Brain Res. 216, 531-542.
46. 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. Neu-rosci. 32, 510-518.
47. Han, X., Tong, J., Zhang, J., Farahvar, A., Wang, E., Yang, J., Sa-madani, U., Smith, D.H., and Huang, J.H. (2011). Imipramine treatment improves cognitive outcome associated with enhanced hippocampal neurogenesis after traumatic brain injury in mice. J. Neurotrauma 28, 995-1007.
48. Donkin, J.J., Cernak, I., Blumbergs, P.C., and Vink, R. (2011). A substance P antagonist reduces axonal injury and improves neurologic outcome when administered up to 12 hours after traumatic brain injury. J. Neurotrauma 28, 217-224.
49. Russo, N.J. II, Kapp, B.S., Holmquist, B.K., and Musty, R.E. (1976). Passive avoidance and amygdala lesions: relationship with pituitary-adrenal system. Physiol. Behav. 16, 191-199.
50. Best, P.J., and Orr, J. Jr. (1979). Effects of hippocampal lesions on passive avoidance and taste aversion conditioning. Physiol. Behav. 10, 193-196.
51. Fanselow, M.S., and Dong, H. (2009). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65, 7-19.
52. Moser, E., Moser, M.B., and Andersen, P. (1993). Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J. Neurosci. 13, 3916-3925.
53. Moser, M.B., Moser, E.I., Forrest, E., Andersen, P., and Morris, R.G. (1995). Spatial learning with a minislab in the dorsal hippocampus. PNAS 92, 9697-9701.
54. Morris, R.G.M., Anderson, E., Lynch, G.S., and Baudry, M. (1986). Selective impairment of learning and blockage of long-term potenti-ation by an N-methyl-d-aspartate receptor antagonist, AP5. Nature 319, 774-776.
55. Hicks, R.R, Smith, D.H, Lowenstern, D.H., Satin-Marie, R., and McIntosh, T.K. (1993). Mild experimental brain injury in the rat induces cognitive deficits associated with regional neuronal loss in the hippocampus. J. Neurotrauma 10, 405-414.
56. Grant, S.G.N., and Silva, A.J. (1994). Targeting learning. Trends Neurosci. 17, 71-75.
57. O'Keefe, J., and Nadel, L. (1978). The Hippocampus as a Cognitive Map. London: Oxford University Press.
58. Tulving, E., and Markowitsch, H.J. (1998). Episodic and declarative memory: role of the hippocampus. Hippocampus 8, 198-204.
59. Broadbent, N.J., Squire, L.R., and Clark, R.E. (2004). Spatial memory, recognition memory, and the hippocampus. Proc. Natl. Acad. Sci. USA 101, 14515-14520.
60. Wan, H., Aggleton, J.P., and Brown, M.W. (1999). Different contributions of the hippocampus and perirhinal cortex to recognition memory. J. Neurosci. 19, 1142-1148.
61. Feeney, D.M., Gonzalez, A., and Law, W.A. (1982). Amphetamine, haloperidol and experience interact to affect rate of recovery after motor cortex injury. Science 217, 855-857.
62. McIntosh, T.K., Noble, L., Andrews, B., and Faden, A.I. (1987). Traumatic brain injury in the rat: characterization of a midline fluid-percussion model. Cent. Nerv. Syst. Trauma 4, 119-134.
63. Dixon, C.E., Lyeth, B.G., Povlishock, J.T., Findling, R., Hamm, R., and Marmarou, A. (1987). A fluid percussion model of experimental brain injury in the rat: neurological, physiological, and histopatho-logical characteristics. J. Neurosurg. 67, 110-119.
64. Schmanke, T.D., Avery, R.A., and Barth, T.M. (1996). The effects of amphetamine on recovery of function after cortical damage in the rat depend on the behavioral requirements of the task. J. Neurotrauma 13, 293-307.
65. Smith, D.C., Modglin, A.A., Roosevelt, R.W., Neese, S.L., Jensen, R.A., Browning, R.A., and Clough, R.W. (2005). Electrical stimulation of the vagus nerve enhances cognitive and motor recovery following moderate fluid percussion injury in the rat. J. Neurotrauma 22, 1485-1502.
66. Flierl, M.A., Stahel, P.F., Beauchamp, K.M., Morgan, S.J., Smith, W.R., and Shohami, E. (2009). Mouse closed head injury model induced by a weight-drop device. Nat. Protoc. 4, 1328-1337.
67. Byrnes, K.R., Stoica, B., Riccio, A., Pajoohesh-Ganji, A., Loane, D.J., and Faden, A.I. (2009). Activation of metabotropic glutamate receptor 5 improves recovery after spinal cord injury in rodents. Ann. Neurol. 66, 63-74.
68. Fujimoto, S.T., Longhi, L., Saatman, K.E., and McIntosh, T.K. (2004). Motor and cognitive function evaluation following experimental traumatic brain injury. Neurosci. Biobehav. Rev. 28, 365-378.
69. Faden, A.I. (1989). TRH analog YM-14673 improves outcome following traumatic brain and spinal cord injury in rats: dose-response studies. Brain Res. 486, 228-235.
70. Li, Y., Chen, J., Chen, X.G., Wang, L., Gautam, S.C., Xu, Y.X., Katakowski, M., Zhang, L.J., Lu, M., Janakiraman, N., and Chopp, M. (2002). Human marrow stromal cell therapy for stroke in rat: neuro-trophins and functional recovery. Neurology 59, 514-523.
71. Pajoohesh-Ganji, A., Byrnes, K.R., Fatemi, G., and Faden, A.I. (2010). A combined scoring method to assess behavioral recovery after mouse spinal cord injury. Neurosci. Res. 67, 117-125.
72. Sun, F., and Faden, A.I. (1995). Neuroprotective effects of 619C89, a use-dependent sodium channel blocker, in rat traumatic brain injury. Brain Res. 673, 133-140.
73. Knoblach, S.M., Fan, L., and Faden, A.I. (1999). Early neuronal expression of tumor necrosis factor-A after experimental brain injury contributes to neurological impairment. J. Neuroimmunol. 95, 115-125.
74. Knoblach, S.M., and Faden, A.I. (2000). Cortical interleukin-1b elevation after traumatic brain injury in the rat: no effect of two selective antagonists on motor recovery. Neurosci. Lett. 289, 5-8.
75. Hamm, R.J. (2001). Neurobehavioral assessment of outcome following traumatic brain injury in rats: an evaluation of selected measures. J. Neurotrauma 18, 1207-1216.