Injury severity differentially affects short- and long-term neuroendocrine outcomes of traumatic brain injury

Journal of Neurotrauma

Volumn 25, Issue 4, 2008, Pages 311-323

  Taylor, Anna N ^a,b   Rahman, Shayan U ^a   Sanders, Nicole C ^c   Tio, Delia L ^a,b   Prolo, Paolo ^d   Sutton, Richard L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^c WILLIAMS COLLEGE   (United States)

^d UCLA SCHOOL OF DENTISTRY   (United States)

Author keywords

Allostasis; Controlled cortical impact; Corticosterone; Rat; Stress

Indexed keywords

CORTICOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; FORELIMB; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INJURY SEVERITY; MALE; MAZE TEST; MOTOR PERFORMANCE; NEUROENDOCRINE SYSTEM; NONHUMAN; PARIETAL LOBE; RADIOIMMUNOASSAY; RAT; STRESS; TRAUMATIC BRAIN INJURY; WORKING MEMORY;

ALLOSTASIS; ANIMALS; BRAIN INJURIES; CORTICOSTERONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; PITUITARY-ADRENAL SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; STRESS; TIME FACTORS; TRAUMA SEVERITY INDICES;

EID: 41449084241     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2007.0486     Document Type: Article

References (79)

1. Agha, A., Phillips, J.O., and Thompson, C.J. (2007). Hypopituitarism following traumatic brain injury (TBI). Br. J. Neurosurg. 21, 210-216.
2. Anderson, K.J., Miller, K.M., Fugaccia, I., and Scheff, S.W. (2005). Regional distribution of Fluoro-jade B staining in the hippocampus following traumatic brain injury. Exp. Neurol. 193, 125-130.
3. Baldwin, S.A., Gibson, T., Callihan, C.T., Sullivan, P.G., Palmer, E., and Scheff, S.W. (1997). Neuronal cell loss in the CA3 subfield of the hippocampus following cortical contusion utilizing the optical dissector method for cell counting. J. Neurotrauma 14, 385-398.
4. Bale, T.L. (2006). Stress sensitivity and the development of affective disorders. Horm. Behav. 50, 529-533.
5. Bale, T.L., Contarino, A., Smith, G.W., Chan, R., Gold, L.H., Sawchenko, P.E., Koob, G.F., Vale, W.W., and Lee, K.-F. (2000). Mice deficient for corticotropin-releasing hormone receptor-2 display anxiety-like behavior and are hypersensitive to stress. Nat. Genet. 24, 410-414.
6. Benvenga, S., Campenni, A., Ruggeri, R.M., and Trimarchi, F. (2000). Hypopituitarism secondary to head trauma. J. Clin. Endocrinol. Metab. 85, 1353-1361.
7. Bhatnagar, S., and Dallman, M. (1998). Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 84, 1025-1039.
8. Bramlett, H.M., and Dietrich, W.D (2002). Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats. Acta Neuropathol. (Berl.) 103, 607-614.
9. Bramlett, H.M., Kraydieh, S., Green, E.J., and Dietrich, W.D. (1997). Temporal and regional patterns of axonal damage following traumatic brain injury: a beta-amyloid precursor protein immunocytochemical study in rats. J. Neuropathol. Exp. Neurol. 56, 1132-1141.
10. Cernak, I., Savic, V.J., Lazarov, A., Joksimovic, M., and Markovic, S. (1999). Neuroendocrine responses following graded traumatic brain injury in male adults. Brain Inj. 13, 1005-1015.
11. Chatzipanteli, K., Alonso, O.F., Kraydieh, S., and Dietrich, W.D. (2000). Importance of posttraumatic hypothermia and hyperthermia on the inflammatory response after fluid percussion brain injury: biochemical and immunocytochemical studies. J. Cereb. Blood Flow Metab. 20, 531-542.
12. Cherian, L., Robertson, C.S., Contant, C.F., and Bryan, R.M. (1994). Lateral cortical impact injury in rats: cerebrovascular effects of varying depth of cortical deformation and impact velocity. J. Neurotrauma 11, 573-585.
13. Childers, M.K., Rupright, J., Jones, P.S., and Merveille, O. (1998). Assessment of neuroendocrine dysfunction following traumatic brain injury. Brain Inj. 12, 547-553.
14. Clark, R.S.B., Schiding, J.K., Kaczorowski, S.L., Marion, D.W., and Kochanek P.M. (1994). Neutrophil accumulation after traumatic brain injury in rats: comparison of weight drop and controlled cortical impact models. J. Neurotrauma 11, 499-506.
15. Clifton, G.L., Jiang, J.Y., Lyeth, B.G., Jenkins, L.W., Hamm, R.J., and Hayes, R.L. (1991). Marked protection by moderate hypothermia after experimental traumatic brain injury. J. Cereb. Blood Flow Metab. 11, 114-121.
16. Cohan, P., Wang, C., McArthur, D.L., Cook, S.W., Dusick, J.R., Armin, B., Swerdloff, R., Vespa, P., Muizelaar, J.P., Cryer, H.G., Christenson, P.D., and Kelly, D.F. (2005). Acute secondary adrenal insufficiency after traumatic brain injury: a prospective study. Crit. Care Med. 33, 2358-2366.
17. Colicos, M.A., Dixon, C.E., and Dash, P.K. (1996). Delayed, selective neuronal death following experimental cortical impact injury in rats: possible role in memory deficits. Brain Res. 739, 111-119.
18. Conrad, C.D., Lupien, S.L., and McEwen, B.S. (1999). Support for a bimodal role for type II adrenal steroid receptors in spatial memory. Neurobiol. Learn. Memory 71, 39-46.
19. Coste, S.C., Kesterson, R.A., Heldwein, K.A., Stevens, S.L., Heard, A.D., Hollis, J.H., Murray, S.E., Hill, K., Pantely, G.A., Hohimer, A.R., Hatton, D.C., Phillips. T.J., Finn. D.A., Low, M.J., Rittenberg, M.B., Stenzel, P., and Stenzel-Poore, M.P. (2000). Abnormal adaptions to stress and impaired cardiovascular function in mice lacking corticotropin-releasing hormone receptor-2. Nat. Genet. 24, 403-409.
20. DeKosky, S.T., Scheff, S.W., and Cotman, C.W. (1984). Elevated corticosterone levels. A possible cause of reduced axon sprouting in aged animals. Neuroendocrinology 38, 33-38.
21. Delahunty, T.M., Jiang, J.Y., Gong, Q.Z., Black, R.T., and Lyeth, B.G. (1995). Differential consequences of lateral and central fluid percussion brain injury on receptor coupling in rat hippocampus. J. Neurotrauma 12, 1045-1057.
22. Dietrich, W.D., Alonso, O., Halley, M., and Busto, R. (1996). Delayed posttraumatic brain hyperthermia worsens outcome after fluid percussion brain injury: a light and electron microscopic study in rats. Neurosurgery 38, 533-541.
23. Dikmen, S.S., Bombardier, C.H., Machamer, J.E., Fann, J.R., and Temkin, N.R. (2004). Natural history of depression in traumatic brain injury. Arch. Phys. Med. Rehabil. 85, 1457-1464.
24. Dinkel, K., MacPherson, A., and Sapolsky, R.M. (2003). Novel glucocorticoid effects on acute inflammation in the CNS. J. Neurochem. 84, 705-716.
25. Dixon, C.E., Clifton, G.L., Lighthall, J.W., Yaghami, 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.
26. Dixon, C.E., Kochanek, P.M., Yan, H.Q., Schiding, J.K., Griffity, R.G., Baum, E., Marion, D.W., and DeKosky, S.T. (1999). One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J. Neurotrauma 16, 109-122.
27. Dunn-Meynell, A.A., and Levin, B.E. (1997). Histological markers of neuronal, axonal and astrocytic changes after lateral rigid impact traumatic brain injury. Brain Res. 761, 25-41.
28. Fann, J.R., Burington, B., Leonetti, A., Jaffe, K., Katon, W.J., and Thompson, R.S. (2004). Psychiatric illness following traumatic brain injury in an adult health maintenance organization population. Arch. Gen. Psychiatry 61, 53-61.
29. Giza, C.C., Maria, N.S., and Hovda, D.A. (2006). N-Methyl- D-aspartate receptor subunit changes after traumatic injury to the developing brain. J. Neurotrauma 23, 950-961.
30. Goel, N., and Bale, T.L. (2007). Identifying early behavioral and molecular markers of future stress sensitivity. Endocrinology 148, 4585-4591.
31. Goodman, J.C., Cherian, L., Bryan, R.M. Jr., and Robertson, C.S. (1994). Lateral cortical impact injury in rats: pathological effects of varying cortical compression and impact velocity. J. Neurotrauma 11, 587-597.
32. Goodman, Y., Bruce, A.J., Cheng, B., and Mattson, M.P. (1996). Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. J. Neurochem. 66, 1836-1844.
33. Gottesfeld, Z., Moore, A.N., and Dash, P.K. (2002). Acute ethanol intake attenuates inflammatory cytokines after brain injury in rats: a possible role for corticosterone. J. Neurotrauma 19, 317-326.
34. Grundy, P.L., Harbuz, M.S., Jessop, D.S., Lightman, S.L., and Sharples, P.M. (2001). The hypothalamo-pituitary-adrenal axis response to experimental traumatic brain injury. J. Neurotrauma 18, 1373-1381.
35. Gurkoff, G.G., Giza, C.C., and Hovda, D.A. (2006). Lateral fluid percussion injury in the developing rat causes an acute, mild behavioral dysfunction in the absence of significant cell death. Brain Res. 1077, 24-36.
36. Hall, E.D., Sulliivan, P.G., Gibson, T.R., Pavel, K.M., Thompson, B.M., and Scheff, S.W. (2005). Spatial and temporal characteristics of neurodegeneration after controlled cortical impact in mice: more than a focal brain injury. J. Neurotrauma 22, 252-265.
37. Hamm, R.J., Pike, B.R., Phillips, L.L., O'Dell, D.M., Temple, M.D., and Lyeth, B.G. (1995). Impaired gustatory neophobia following traumatic brain injury in rats. J. Neurotrauma 12, 307-314.
38. Hannay, H.J., Feldman, Z., Phan, P., Keyani, A., Panwar, N., Goodman, J.C., and Robertson, C.S. (1999). Validation of a controlled cortical impact model of head injury in mice. J. Neurotrauma 16, 1103-1114.
39. Herman, J.P., Figueiredo, H., Mueller, N.K., Ulrich-Lai, Y., Ostrander, M.M., Choi, D.C., and Cullinan, W.E. (2003). Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary- adrenocortical responsiveness. Front. Neuroendocrinol. 24, 151-180.
40. Houshyar, H., Galigniana, M.D., Pratt, W.B., and Woods, J.H. (2001). Differential responsivity of the hypothalamic-pituitary-adrenal axis to glucocorticoid negative-feedback and corticotropin releasing hormone in rats undergoing morphine withdrawal: possible mechanisms involved in facilitated and attenuated stress responses. J. Neuroendocrinol. 13, 875-886.
41. Jiang, J.Y., Lyeth, B.G., Delahunty, T.M., Phillips, L.L., and Hamm, R.J. (1994). Muscarinic cholinergic receptor binding in rat brain at 15 days following traumatic brain injury. Brain Res. 651, 123-128.
42. Kelly, D.F., Gaw Gonzalo, I.T., Cohan, P., Berman, N., Swerdloff, R., and Wang, C. (2000). Hypopituitarism following traumatic brain injury and aneurysmal subarachnoid hemorrhage: a preliminary report. J. Neurosurg. 93, 743-752.
43. Levin, B.E., Brown, K.L., Pawar, G., and Dunn-Meynell, A. (1995). Widespread and lateralized effects of acute traumatic brain injury on norepinephrine turnover in the rat brain. Brain Res. 674, 307-313.
44. Levin, B.E., Pan, S., and Dunn-Meynell, A. (1994). Chronic alterations in rat brain α-adrenoceptors following traumatic brain injury. Restor. Neurol. Neurosci. 7, 5-12.
45. Li, H.H., Lee, S.M., Cai, Y., Sutton, R.L., and Hovda, D.A. (2004). Differential gene expression in hippocampus following experimental brain trauma reveals distinct features of moderate and severe injuries. J. Neurotrauma 21, 1141-1153.
46. Lieberman, S.A., Oberoi, A.L., Gilkison, C.R., Masel, B.E., and Urban, R.J. (2001). Prevalence of neuroendocrine dysfunction in patients recovering from traumatic brain injury. J. Clin. Endocrinol. Metab. 86, 2752-2756.
47. Lifshitz, J., Kelley, B.J., and Povlishock, J.T. (2007). Perisomatic thalamic axotomy after diffuse traumatic brain injury is associated with atrophy rather than cell death. J. Neuropathol. Exp. Neurol. 66, 218-229.
48. 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.
49. Lyeth, B.G., Jenkins, L.W., Hamm, R.J., Dixon, C.E., Phillips, L.L., Clifton, G.L., Young, H.F., and Hayes, R.L. (1990). Prolonged memory impairment in the absence of hippocampal cell death following traumatic brain injury in the rat. Brain Res. 526, 249-258.
50. Markgraf, C.G., Clifton, G.L., Aguirre, M., Chaney, S.F., Knox-Du Bois, C., Kennon, K., and Verma, N. (2001). Injury severity and sensitivity to treatment after controlled cortical impact in rats. J. Neurotrauma 18, 175-186.
51. Masera, R.G., Prolo, P., Sartori, M.L., Staurenghi, A., Griot, G., Ravizza, L., Dovio, A., Chiappelli, F., and Angeli, A. (2002). Mental deterioration correlates with response of natural killer (NK) cell activity to physiological modifiers in patients with short history of Alzheimer's disease. Psychoneuroendocrinology 27, 447-461.
52. McCullers, D.L., Sullivan, P.G., Scheff, S.W., and Herman, J.P. (2002a). Traumatic brain injury regulates adrenocorticosteroid receptor mRNA levels in rat hippocampus. Brain Res. 947, 41-49.
53. McCullers, D.L., Sullivan, P.G., Scheff, S.W., and Herman, J.P. (2002b). Mifepristone protects CA1 hippocampal neurons following traumatic brain injury in rat. Neuroscience 109, 219-230.
54. McEwen, B. (2004). Protection and damage from acute and chronic atress. Allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann. N.Y. Acad. Sci. 1032, 1-7.
55. McIntosh, L.J., and Sapolsky, R.M. (1996). Glucocorticoids increase the accumulation of reactive oxygen species and enhance adriamycin-induced toxicity in neuronal culture. Exp. Neurol. 141, 201-206.
56. McNay, E.C., McCarty, R.C., and Gold, P.E. (2001). Fluctuations in brain glucose concentration during behavioral testing: dissociations between brain areas and between brain and blood. Neurobiol. Learn. Mem. 75, 325-337.
57. Miyazaki, S., Katayama, Y., Lyeth, B.G., Jenkins, L.W., Dewitt, D.S., Goldberg, S.J., Newlon, P.G., and Hayes, R.L. (1992). Enduring suppression of hippocampal long-term potentiation following traumatic brain injury in rat. Brain Res. 585, 335-339.
58. Paxinos, G., and Watson, C. (2005). The Rat Brain in Stereotaxic Coordinates, 5th ed. Elsevier: New York.
59. Reeves, T.M., Lyeth, B.G., Phillips, L.L., Hamm, R.J., and Povlishock, J.T. (1997). The effects of traumatic brain injury on inhibition in the hippocampus and dentate gyrus. Brain Res. 757, 119-132.
60. Roe, S.Y., McGowan, E.M., and Rothwell, N.J. (1998). Evidence for the Involvement of corticotrophin-releasing hormone in the pathogenesis of traumatic brain injury. Eur. J. Neurosci. 10, 553-559.
61. Ryan, L.M., and Warden, D.L. (2003). Post concussion syndrome. Int. Rev. Psychiatry 15, 310-316.
62. 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.
63. Saija, A., Hayes, R.L., Lyeth, B.G., Dixon, C.E., Yamamoto, T., and Robinson, S.E. (1988). The effect of concussive head injury on central cholinergic neurons. Brain Res. 452, 303-311.
64. Sapolsky, R.M. (1985). A mechanism for glucocorticoid toxicity in the hippocampus: increased neuronal vulnerability to metabolic insults. J. Neurosci. 5, 1228-1232.
65. Schallert, T., and Woodlee, M.T. (2005). Orienting and Placing, in: The Behavior of the Laboratory Rats: A Handbook with Tests. I. Whishaw, and B. Kolb (eds.). Oxford University Press: New York. pps. 129-140.
66. Scheff, S.W., Baldwin, S.A., Brown, R.W., and Kraemer, P.J. (1997). Morris water maze deficits in rats following traumatic brain injury: lateral controlled cortical impact. J. Neurotrauma 14, 615-627.
67. Shohami, E., Bass, R., Trembovler, V., and Weidenfeld, J. (1995). The effect of the adrenocortical axis upon recovery from closed head injury. J. Neurotrauma 12, 1069-1077.
68. Smith, D.H., Chen, X.H., Pierce, J.E., Trojanowski, J.Q., Graham, D.I., and McIntosh, T.K. (1997). Progressive atrophy and neuron death for one year following brain trauma in the rat. J. Neurotrauma 14, 715-727.
69. Smith, M.A. Makino, S., Kvetnansky, R., and Post, R.M. (1995). Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J. Neurosci. 15, 1768-1777.
70. Suh, S.W., Frederickson, C.J., and Danscher, G. (2006). Neurotoxic zinc translocation into hippocampal neurons is inhibited by hypothermia and is aggravated by hyperthermia after traumatic brain injury in rats. J. Cereb. Blood Flow Metab. 26, 161-169.
71. Sutton, R.L., Lescaudron, L., and Stein, D.G. (1993). Unilateral cortical contusion injury in the rat: vascular disruption and temporal development of cortical necrosis. J. Neurotrauma 10, 135-149.
72. Taylor, A.N., Bando, J.K., Oluwadara, O., Rahman, S.U., Romeo, H.E., Sanders, M.J., and Tio, D.L. (2004). Interleukin-1 receptor antagonist improves traumatic brain injury outcome. Presented at the 7th International Neurotrauma Symposium, Adelaide, Australia.
73. Taylor, A.N., Rahman, S.U., Tio, D.L., Sanders, M.J., Bando, J.K., Truong, A.H., and Prolo, P. (2006). Lasting neuroendocrine-immune effects of traumatic brain injury in rats. J. Neurotrauma 23, 1802-1813.
74. Taylor, A.N., Rahman, S.U., Gardner, S., Li, W., Kim, C.J., Siu, C., Truong, A.H., Tio, D.L., Prolo, P., and Sutton, R.L. (2007). Injury severity differentially affects short- and long-term neuroendocrine outcomes of traumatic brain injury. Soc. Neuroscience Abst. 33, 381.10.
75. Taylor, A.N., Romeo, H.E., Beylin, A.V., Tio, D.L., Rahman, S.U., and Hovda, D.A. (2002). Alcohol consumption in traumatic brain injury: attenuation of tbi-induced hyperthermia and neurocognitive deficits. J. Neurotrauma 19, 1597-1608.
76. Wei, Q., Hebda-Bauer, E.K., Pletsch, A., Luo, J., Hoversten, M.T., Osetek, A.J., Evans, S.J., Watson, S.J., Seasholtz, A.F., and Akil, H. (2007). Overexpressing the glucocorticoid receptor in forebrain causes an aging-like neuroendocrine phenotype and mild cognitive dysfunction. J. Neurosci. 27, 8836-8844.
77. Whishaw, I.I.Q., Piecharka, C.M., Zeeb, F., and Stein, D.G. (2004). Unilateral frontal lobe contusion and forelimb function: chronic quantitative and qualitative impairments in reflexive and skilled forelimb movements in rats. J. Neurotrauma 21, 1584-1600.
78. Wilde, E.A., Bigler, E.D., Hunter, J.V., Fearing, M.A., Scheibel, R.S., Newsome, M.R., Johnson, J.L., Bachevalier, J., Li, X., and Levin, H.S. (2007). Hippocampus, amygdala, and basal ganglia morphometrics in children after moderate-to-severe traumatic brain injury. Dev. Med. Child Neurol. 49, 294-299.
79. Yuan, X.-Q., and Wade, C.E. (1991). Neuroendocrine abnormalities in patients with traumatic brain injury. Front. Neuroendocrinol. 12, 209-230.