Blast wave exposure impairs memory and decreases axon initial segment length

Journal of Neurotrauma

Volumn 30, Issue 9, 2013, Pages 741-751

  Baalman, Kelli L ^a   Cotton, R James ^a   Rasband, S Neil ^b   Rasband, Matthew N ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Brigham Young University   (United States)

Author keywords

Axon initial segment; Ion channel; Traumatic brain injury

Indexed keywords

ALBUMIN; ALLOGRAFT INFLAMMATORY FACTOR 1; GLIAL FIBRILLARY ACIDIC PROTEIN; SPECTRIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXON INITIAL SEGMENT LENGTH; BLAST INJURY; BLOOD PRESSURE MEASUREMENT; BRAIN CORTEX; COGNITIVE DEFECT; COMPRESSED AIR; CONTROLLED STUDY; CORPUS CALLOSUM; CYTOARCHITECTURE; DIASTOLIC BLOOD PRESSURE; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE POTENTIAL; MEMORY DISORDER; MOTOR PERFORMANCE; NERVE CELL CHARACTERISTICS AND FUNCTIONS; NERVE EXCITABILITY; NONHUMAN; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SYSTOLIC BLOOD PRESSURE; TRAUMATIC BRAIN INJURY;

ANIMALS; AXONS; BLAST INJURIES; BRAIN CONCUSSION; COMPUTER SIMULATION; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOBLOTTING; MALE; MEMORY DISORDERS; MODELS, NEUROLOGICAL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84876275633     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2478     Document Type: Article

References (50)

1. Okie, S. (2005) Traumatic brain injury in the war zone. N. Engl. J. Med. 352:2043-2047. (Pubitemid 40664304)
2. Ling, G.S., and Ecklund, J.M. (2011) Traumatic brain injury in modern war. Curr. Opin. Anaesthesiol. 24:124-130.
3. Elsayed, N.M. (1997) Toxicology of blast overpressure. Toxicology 121:1-15. (Pubitemid 27259670)
4. Mayorga, M.A. (1997) The pathology of primary blast overpressure injury. Toxicology 121:17-28. (Pubitemid 27259671)
5. Leung, L.Y., VandeVord, P.J., Dal Cengio, A.L., Bir, C., Yang, K.H., and King, A.I. (2008) Blast related neurotrauma: A review of cellular injury. Mol Cell Biomech 5:155-168.
6. Ritenour AE, Baskin TW (2008) Primary blast injury: Update on diagnosis and treatment. Crit Care Med 36:S311-317.
7. Champion, H.R., Holcomb, J.B., and Young, L.A. (2009) Injuries from explosions: Physics, biophysics, pathology, and required research focus. J. Trauma 66:1468-1477.
8. Ling, G., Bandak, F., Armonda, R., Grant, G., and Ecklund, J. (2009) Explosive blast neurotrauma. J. Neurotrauma 26:815-825.
9. Cernak, I., and Noble-Haeusslein, L.J. (2010) Traumatic brain injury: An overview of pathobiology with emphasis on military populations. J. Cereb. Blood Flow Metab. 30:255-266.
10. Wilk, J.E., Thomas, J.L., McGurk, D.M., Riviere, L.A., Castro, C.A., Hoge, C.W. (2010) Mild traumatic brain injury (concussion) during combat: Lack of association of blast mechanism with persistent postconcussive symptoms. J. Head Trauma Rehabil. 25:9-14.
11. Taber, K.H., Warden, D.L., Hurley, R.A. (2006) Blast-related traumatic brain injury: What is known? J. Neuropsychiatry Clin. Neurosci. 18:141-145.
12. Warden, D. (2006) Military TBI during the Iraq and Afghanistan wars. J. Head Trauma Rehabil. 21:398-402. (Pubitemid 44413113)
13. Carroll, L.J., Cassidy, J.D., Peloso, P.M., Borg, J., von Holst, H., Holm, L., Paniak, C., and Pepin, M. (2004) Prognosis for mild traumatic brain injury: Results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. J. Rehabil. Med. Suppl 43:84-105. (Pubitemid 38268224)
14. Hoge, C.W., McGurk, D., Thomas, J.L., Cox, A.L., Engel, C.C., and Castro, C.A. (2008) Mild traumatic brain injury in U.S. Soldiers returning from Iraq. N. Engl. J. Med. 358:453-463.
15. Elder, G.A., Mitsis, E.M., Ahlers, S.T., and Cristian, A. (2010) Blastinduced mild traumatic brain injury. Psychiatr. Clin. North Am. 33:757-781.
16. Bradbury, E.J., and McMahon, S.B. (2006) Spinal cord repair strategies: Why do they work? Nat. Rev. Neurosci. 7:644-653. (Pubitemid 44106746)
17. Buffington, S.A., and Rasband, M.N. (2011) The axon initial segment in nervous system disease and injury. Eur. J. Neurosci. 34:1609-1619.
18. Rasband MN (2010) The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci.
19. Schafer DP, Jha S, Liu F, Akella T, McCullough LD, Rasband MN (2009) Disruption of the axon initial segment cytoskeleton is a new mechanism for neuronal injury. J Neurosci 29:13242-13254.
20. Grubb, M.S., and Burrone, J. (2010) Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature. 465:1070-1074.
21. Kuba, H., Oichi, Y., and Ohmori, H. (2010) Presynaptic activity regulates Na(+) channel distribution at the axon initial segment. Nature. 465:1075-1078.
22. Wimmer, V.C., Reid, C.A., So, E.Y., Berkovic, S.F., Petrou, S. (2010) Axon initial segment dysfunction in epilepsy. J. Physiol. 588:1829-1840.
23. Kaphzan, H., Buffington, S.A., Jung, J.I., Rasband, M.N., and Klann, E. (2011) Alterations in intrinsic membrane properties and the axon initial segment in a mouse model of angelman syndrome. J. Neurosci. 31:17637-17648.
24. Li, X., Kumar, Y., Zempel, H., Mandelkow, E.M., Biernat, J., and Mandelkow, E. (2011) Novel diffusion barrier for axonal retention of Tau in neurons and its failure in neurodegeneration. Embo. J. 30:4825-4837.
25. Grubb, M.S., Shu, Y., Kuba, H., Rasband, M.N., Wimmer, V.C., and Bender, K.J. (2011) Short- and long-term plasticity at the axon initial segment. J. Neurosci. 31:16049-16055.
26. Kole, M.H., Ilschner, S.U., Kampa, B.M., Williams, S.R., Ruben, P.C., and Stuart, G.J. (2008) Action potential generation requires a high sodium channel density in the axon initial segment. Nat. Neurosci. 11:178-186. (Pubitemid 351170500)
27. Bevins, R.A., and Besheer, J. (2006) Object recognition in rats and mice: A one-trial non-matching-to-sample learning task to study 'recognition memory.' Nat. Protoc. 1:1306-1311.
28. Douglas, R.M., Alam, N.M., Silver, B.D., McGill, T.J., Tschetter, W.W., and Prusky, G.T. (2005) Independent visual threshold measurements in the two eyes of freely moving rats and mice using a virtual-reality optokinetic system. Vis. Neurosci. 22:677-684. (Pubitemid 43237762)
29. Ogawa, Y., Schafer, D.P., Horresh, I., Bar, V., Hales, K., Yang, Y., Susuki, K., Peles, E., Stankewich, M.C., and Rasband, M.N. (2006) Spectrins and ankyrinB constitute a specialized paranodal cytoskeleton. J. Neurosci. 26:5230-5239. (Pubitemid 44315305)
30. Schafer DP, Bansal R, Hedstrom KL, Pfeiffer SE, Rasband MN (2004) Does paranode formation and maintenance require partitioning of neurofascin 155 into lipid rafts? J Neurosci 24:3176-3185. (Pubitemid 38451884)
31. Jeong, H.K., Ji, K.M., Kim, B., Kim, J., Jou, I., and Joe, E.H. (2011) Inflammatory responses are not sufficient to cause delayed neuronal death in ATP-induced acute brain injury. PLoS One 5:e13756.
32. Svetlov, S.I., Prima, V., Kirk, D.R., Gutierrez, H., Curley, K.C., Hayes, R.L., Wang, K.K. (2010) Morphologic and biochemical characterization of brain injury in a model of controlled blast overpressure exposure. J. Trauma 69:795-804.
33. Burggraf, D., Trinkl, A., Burk, J., Martens, H.K., Dichgans, M., and Hamann, G.F. (2008) Vascular integrin immunoreactivity is selectively lost on capillaries during rat focal cerebral ischemia and reperfusion. Brain Res. 1189:189-197. (Pubitemid 351842540)
34. Siman R, Baudry M, Lynch G (1984) Brain fodrin: Substrate for calpain I, an endogenous calcium-activated protease. Proc Natl Acad Sci U S A 81:3572-3576. (Pubitemid 14122716)
35. Mondello, S., Robicsek, S.A., Gabrielli, A., Brophy, G.M., Papa, L., Tepas, J., Robertson, C., Buki, A., Scharf, D., Jixiang, M., Akinyi, L., Muller, U., Wang, K.K., and Hayes, R.L. (2010) alphaII-spectrin breakdown products (SBDPs): Diagnosis and outcome in severe traumatic brain injury patients. J Neurotrauma 27:1203-1213.
36. Barker, G.R., and Warburton, E.C. (2011) When is the hippocampus involved in recognition memory? J. Neurosci. 31:10721-10731.
37. Yang, Y., Ogawa, Y., Hedstrom, K.L., Rasband, M.N. (2007) {beta} IV spectrin is recruited to axon initial segments and nodes of Ranvier by ankyrinG. J. Cell Biol. 176:509-519.
38. Galiano, M.R., Jha, S., Ho, T.S., Zhang, C., Ogawa, Y., Chang, K.J., Stankewich, M.C., Mohler, P.J., and Rasband, M.N. (2012) A distal axonal cytoskeleton forms an intra-axonal boundary that controls axon initial segment assembly. Cell 149:1125-1139.
39. Gerstner, W., Kreiter, A.K., Markram, H., and Herz, A.V. (1997) Neural codes: Firing rates and beyond. Proc. Natl. Acad. Sci. U. S. A. 94:12740-12741. (Pubitemid 27518414)
40. Rathbun DL, Alitto HJ, Weyand TG, Usrey WM (2007) Interspike interval analysis of retinal ganglion cell receptive fields. J Neurophysiol 98:911-919. (Pubitemid 47236041)
41. Delcour, M., Russier, M., Amin, M., Baud, O., Paban, V., Barbe, M.F., and Coq, J.O. (2012) Impact of prenatal ischemia on behavior, cognitive abilities and neuroanatomy in adult rats with white matter damage. Behav. Brain Res. 232:233-244.
42. Cernak, I., Wang, Z., Jiang, J., Bian, X., and Savic, J. (2001) Cognitive deficits following blast injury-induced neurotrauma: Possible involvement of nitric oxide. Brain Inj. 15:593-612. (Pubitemid 32640293)
43. Moochhala, S.M., Md, S., Lu, J., Teng, C.H., and Greengrass C. (2004) Neuroprotective role of aminoguanidine in behavioral changes after blast injury. J. Trauma 56:393-403. (Pubitemid 38295386)
44. Long, J.B., Bentley, T.L., Wessner, K.A., Cerone, C., Sweeney, S., and Bauman, R.A. (2009) Blast overpressure in rats: Recreating a battlefield injury in the laboratory. J. Neurotrauma 26:827-840.
45. Svetlov, S.I., Prima, V., Glushakova, O., Svetlov, A., Kirk, D.R., Gutierrez, H., Serebruany, V.L., Curley, K.C., Wang, K.K., Hayes, R.L. (2012) Neuro-glial and systemic mechanisms of pathological responses in rat models of primary blast overpressure compared to ''composite'' blast. Front Neurol. 3:15.
46. Iwata, A., Stys, P.K., Wolf, J.A., Chen, X.H., Taylor, A.G., Meaney, D.F., and Smith, D.H. (2004) Traumatic axonal injury induces proteolytic cleavage of the voltage-gated sodium channels modulated by tetrodotoxin and protease inhibitors. J. Neurosci. 24:4605-4613. (Pubitemid 38656616)
47. Singleton RH, Povlishock JT (2004) Identification and characterization of heterogeneous neuronal injury and death in regions of diffuse brain injury: Evidence for multiple independent injury phenotypes. J Neurosci 24:3543-3553. (Pubitemid 38481111)
48. Hinzman, J., Thomas, T.C., Quintero, J., Gerhardt, G., and Lifshitz, J. (2012) Disruptions in the regulation of extracellular glutamate by neurons and glia in the rat striatum two days after diffuse brain injury. J. Neurotrauma. 29:1197-1208.
49. Wolf, J.A., Stys, P.K., Lusardi, T., Meaney, D., Smith, D.H. (2001) Traumatic axonal injury induces calcium influx modulated by tetrodotoxin- sensitive sodium channels. J Neurosci. 21:1923-1930. (Pubitemid 32221376)
50. Hedstrom, K.L., Ogawa, Y., and Rasband, M.N. (2008) AnkyrinG is required for maintenance of the axon initial segment and neu ronal polarity. J. Cell Biol. 183:635-640.