Disconnection of the ascending arousal system in traumatic coma

Journal of Neuropathology and Experimental Neurology

Volumn 72, Issue 6, 2013, Pages 505-523

  Edlow, Brian L ^a,b   Haynes, Robin L ^c   Takahashi, Emi ^b,c   Klein, Joshua P ^a   Cummings, Peter ^d   Benner, Thomas ^b   Greer, David M ^b,e   Greenberg, Steven M ^b   Wu, Ona ^b   Kinney, Hannah C ^c   Folkerth, Rebecca D ^a,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d Office of the Chief Medical Examiner   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ARAS; Ascending reticular activating system; Coma; Consciousness; HARDI; High angular resolution diffusion imaging; TAI; TBI; Tractography; Traumatic axonal injury; Traumatic braininjury

Indexed keywords

AMYLOID BETA PROTEIN; FRESH FROZEN PLASMA; PROTHROMBIN COMPLEX; VITAMIN K GROUP;

ADULT; AROUSAL; ARTICLE; AWARENESS; BRAIN CORTEX; BRAIN EDEMA; BRAIN FORNIX; BRAIN STEM; CARDIOPULMONARY ARREST; CASE REPORT; CEREBELLUM VERMIS; CEREBRAL PEDUNCLE; CINGULATE GYRUS; COMA; COMPUTER ASSISTED TOMOGRAPHY; CONSCIOUSNESS; CONTROLLED STUDY; CORPUS CALLOSUM; DENTATE GYRUS; FEMALE; FOREBRAIN; FRONTAL LOBE; HEMISPHERE; HUMAN; HYPOTHALAMUS; INFERIOR FRONTAL GYRUS; INJURY SEVERITY; INTENSIVE CARE; MESENCEPHALON; NERVE CELL NETWORK; NERVE INJURY; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; POSTERIOR CINGULATE; PRIORITY JOURNAL; SUBCORTEX; SUBICULUM; SUBVENTRICULAR ZONE; THALAMOCORTICAL TRACT; THALAMUS; THALAMUS RETICULAR NUCLEUS; TRACTOGRAPHY; TRAUMATIC BRAIN INJURY; WHITE MATTER;

AROUSAL; BRAIN STEM; COMA, POST-HEAD INJURY; DIFFUSION TENSOR IMAGING; FATAL OUTCOME; FEMALE; HUMANS; MIDDLE AGED; NEURAL PATHWAYS;

EID: 84878652877     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3182945bf6     Document Type: Article

References (87)

1. Bruns J Jr, Hauser WA. The epidemiology of traumatic brain injury: A review. Epilepsia 2003;44(Suppl 10):2-10
2. Faul M, Xu L, Wald MM, Coronado VG. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations, and Deaths. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control, 2010
3. Perel P, Arango M, Clayton T, et al. Predicting outcome after traumatic brain injury: Practical prognostic models based on large cohort of international patients. BMJ 2008;336:425-29
4. Bell RS, Vo AH, Neal CJ, et al. 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. J Trauma 2009;66: S104-11
5. Jennett B, Plum F. Persistent vegetative state after brain damage. A syndrome in search of a name. Lancet 1972;1:734-37
6. Giacino JT, Ashwal S, Childs N, et al. The minimally conscious state: Definition and diagnostic criteria. Neurology 2002;58:349-53
7. Katz DI, Polyak M, Coughlan D, et al. Natural history of recovery from brain injury after prolonged disorders of consciousness: Outcome of patients admitted to inpatient rehabilitation with 1-4 year follow-up. Prog Brain Res 2009;177:73-88
8. Zoroya G. For Troops With Brain Trauma, A Long Journey Back. Tampa, FL: USA Today, 2010
9. Skandsen T, Kvistad KA, Solheim O, et al. Prognostic value of magnetic resonance imaging in moderate and severe head injury: A prospective study of early MRI findings and one-year outcome. J Neurotrauma 2011; 28:691-99
10. Gennarelli TA, Spielman GM, Langfitt TW, et al. Influence of the type of intracranial lesion on outcome from severe head injury. J Neurosurg 1982;56:26-32
11. Estraneo A, Moretta P, Loreto V, et al. Late recovery after traumatic, anoxic, or hemorrhagic long-lasting vegetative state. Neurology 2010;75: 239-45
12. Voss HU, Uluc AM, Dyke JP, et al. Possible axonal regrowth in late recovery from the minimally conscious state. J Clin Invest 2006;116:2005-11
13. Strich SJ. Shearing of nerve fibers as a cause of brain damage due to head injury: A pathological study of twenty cases. Lancet 1961;2: 443-48
14. Adams JH, Doyle D, Ford I, et al. Diffuse axonal injury in head injury: Definition, diagnosis and grading. Histopathology 1989;15:49-59
15. Povlishock JT, Katz DI. Update of neuropathology and neurological recovery after traumatic brain injury. J Head Trauma Rehabil 2005;20: 76-94
16. Kampfl A, Franz G, Aichner F, et al. The persistent vegetative state after closed head injury: Clinical and magnetic resonance imaging findings in 42 patients. J Neurosurg 1998;88:809-16
17. Ommaya AK, Gennarelli TA. Cerebral concussion and traumatic unconsciousness. Correlation of experimental and clinical observations of blunt head injuries. Brain 1974;97:633-54
18. Adams JH, Graham DI, Murray LS, Scott G. Diffuse axonal injury due to nonmissile head injury in humans: An analysis of 45 cases. Ann Neurol 1982;12:557-63
19. Adams H, Mitchell DE, Graham DI, et al. Diffuse brain damage of immediate impact type. Its relationship to ''primary brain-stem damage'' in head injury. Brain 1977;100:489-502
20. Smith DH, Nonaka M, Miller R, et al. Immediate coma following inertial brain injury dependent on axonal damage in the brainstem. J Neurosurg 2000;93:315-22
21. Steriade M. Arousal: Revisiting the reticular activating system. Science 1996;272:225-26
22. Parvizi J, Damasio A. Consciousness and the brainstem. Cognition 2001; 79:135-60
23. Gennarelli TA, Thibault LE, Adams JH, et al. Diffuse axonal injury and traumatic coma in the primate. Ann Neurol 1982;12:564-74
24. Parvizi J, Damasio AR. Neuroanatomical correlates of brainstem coma. Brain 2003;126:1524-36
25. Moruzzi G, Magoun HW. Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1949;1:455-73
26. Edlow BL, Takahashi E, Wu O, et al. Neuroanatomic connectivity of the human ascending arousal system critical to consciousness and its disorders. J Neuropathol Exp Neurol 2012;71:531-46
27. Hansen B, Flint JJ, Heon-Lee C, et al. Diffusion tensor microscopy in human nervous tissue with quantitative correlation based on direct histological comparison. Neuroimage 2011;57:1458-65
28. Schmahmann JD, Pandya DN, Wang R, et al. Association fibre pathways of the brain: Parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007;130:630-53
29. Catani M, Thiebaut de Schotten M. A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 2008;44: 1105-32
30. Shin SS, Verstynen T, Pathak S, et al. High-definition fiber tracking for assessment of neurological deficit in a case of traumatic brain injury: Finding, visualizing, and interpreting small sites of damage. J Neurosurg 2012;116:1062-69
31. Haynes RL, Billiards SS, Borenstein NS, et al. Diffuse axonal injury in periventricular leukomalacia as determined by apoptotic marker fractin. Pediatr Res 2008;63;656-61
32. El-Khodor BF, Burke RE. Medial forebrain bundle axotomy during development induces apoptosis in dopamine neurons of the substantia nigra and activation of caspases in their degenerating axons. J Comp Neurol 2002;452:65-79
33. McNab JA, Jbabdi S, Deoni SC, et al. High resolution diffusion-weighted imaging in fixed human brain using diffusion-weighted steady state free precession. Neuroimage 2009;46:775-85
34. Miller KL, Stagg CJ, Douaud G, et al. Diffusion imaging of whole, post-mortem human brains on a clinical MRI scanner. Neuroimage 2011; 57:167-81
35. Shepherd TM, Thelwall PE, Stanisz GJ, et al. Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue. Magn Reson Med 2009;62:26-34
36. D'Arceuil H, de Crespigny A. The effects of brain tissue decomposition on diffusion tensor imaging and tractography. Neuroimage 2007;36: 64-68
37. Shepherd TM, Flint JJ, Thelwall PE, et al. Postmortem interval alters the water relaxation and diffusion properties of rat nervous tissueV Implications forMRI studies of human autopsy samples. Neuroimage 2009; 44:820-26
38. Shapiro EM, Skrtic S, Sharer K, et al. MRI detection of single particles for cellular imaging. Proc Natl Acad Sci U S A 2004;101:10901-6
39. Paxinos G, Huang X. Atlas of the Human Brainstem. San Diego, CA: Academic Press, 1995
40. Morel A, Magnin M, Jeanmonod D. Multiarchitectonic and stereotactic atlas of the human thalamus. J Comp Neurol 1997;387:588-630
41. Irimia A, Chambers MC, Torgerson CM, et al. Circular representation of human cortical networks for subject and population-level connectomic visualization. Neuroimage 2012;60:1340-51
42. Mori S, Crain BJ, Chacko VP, et al. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 1999;45:265-69
43. Blumbergs PC, Scott G, Manavis J, et al. Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. J Neurotrauma 1995;12: 565-72
44. Kreutzberg GW, Blakemore WF, Graeber MB. Cellular pathology of the central nervous system. In: Graham DI, Lantos PL eds. Greenfield's Neuropathology. London, UK: Arnold, 1997:124
45. Tate-Ostroff B, Majocha RE, Marotta CA. Identification of cellular and extracellular sites of amyloid precursor protein extracytoplasmic domain in normal and Alzheimer disease brains. Proc Natl Acad Sci U S A 1989; 86:745-49
46. McKee AC, Cantu RC, Nowinski CJ, et al. Chronic traumatic encephalopathy in athletes: Progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 2009;68:709-35
47. Johnson VE, Stewart W, Smith DH. Traumatic brain injury and amyloidbeta pathology: A link to Alzheimer's disease? Nat Rev Neurosci 2010;11: 361-70
48. Reichard RR, Smith C, Graham DI. The significance of beta-APP immunoreactivity in forensic practice. Neuropathol Appl Neurobiol 2005; 31:304-13
49. Steriade M, McCormick DA, Sejnowski TJ. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993;262:679-85
50. Schiff ND, Plum F. The role of arousal and ''gating'' systems in the neurology of impaired consciousness. J Clin Neurophysiol 2000;17: 438-52.
51. Selden NR, Gitelman DR, Salamon-Murayama N, et al. Trajectories of cholinergic pathways within the cerebral hemispheres of the human brain. Brain 1998;121:2249-57
52. Geschwind N. Disconnexion syndromes in animals and man. Brain 1965; 88:237-94
53. Kinney HC, Korein J, Panigrahy A, et al. Neuropathological findings in the brain of Karen Ann Quinlan. The role of the thalamus in the persistent vegetative state. N Engl J Med 1994;330:1469-75
54. Adams JH, Graham DI, Jennett B. The neuropathology of the vegetative state after an acute brain insult. Brain 2000;123:1327-38
55. Murdoch I, Nicoll JA, Graham DI, et al. Nucleus basalis of Meynert pathology in the human brain after fatal head injury. J Neurotrauma 2002; 19:279-84
56. Kinomura S, Larsson J, Gulyas B, et al. Activation by attention of the human reticular formation and thalamic intralaminar nuclei. Science 1996;271:512-15
57. Schiff ND, Giacino JT, Kalmar K, et al. Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 2007;448:600-3
58. Moll CK, Sharott A, Hamel W, et al. Waking up the brain: A case study of stimulation-induced wakeful unawareness during anaesthesia. Prog Brain Res 2009;177:125-45
59. Benarroch EE. Thermoregulation: Recent concepts and remaining questions. Neurology 2007;69:1293-97
60. Coote JH. Cardiovascular function of the paraventricular nucleus of the hypothalamus. Biol Signals 1995;4:142-49
61. Irimia A, Chambers MC, Torgerson CM, et al. Patient-tailored connectomics visualization for the assessment of white matter atrophy in traumatic brain injury. Front Neurology 2012;3:10
62. Monti MM, Vanhaudenhuyse A, Coleman MR, et al. Willful modulation of brain activity in disorders of consciousness. N Engl J Med 2010;362: 579-89
63. Bardin JC, Fins JJ, Katz DI, et al. Dissociations between behavioural and functional magnetic resonance imaging-based evaluations of cognitive function after brain injury. Brain 2011;134:769-82
64. Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, et al. Default network connectivity reflects the level of consciousness in noncommunicative brain-damaged patients. Brain 2010;133:161-71
65. Goldfine AM, Victor JD, Conte MM, et al. Determination of awareness in patients with severe brain injury using EEG power spectral analysis. Clin Neurophysiol 2011;122:2157-68
66. Cruse D, Chennu S, Chatelle C, et al. Bedside detection of awareness in the vegetative state: A cohort study. Lancet 2011;378:2088-94
67. Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery Scale- Revised: Measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 2004;85:2020-29
68. Buki A, Povlishock JT. All roads lead to disconnection? Traumatic axonal injury revisited. Acta Neurochir (Wien) 2006;148:181-93
69. Graham DI, Gennarelli TA, McIntosh TK. Trauma. In: Graham DI, Lantos PL, eds. Greenfield's Neuropathology. London, UK: Arnold, 2002:823-98
70. Hortobagyi T, Wise S, Hunt N, et al. Traumatic axonal damage in the brain can be detected using beta-APP immunohistochemistry within 35 min after head injury to human adults. Neuropathol Appl Neurobiol 2007;33:226-37
71. Maxwell WL, MacKinnon MA, Smith DH, et al. Thalamic nuclei after human blunt head injury. J Neuropathol Exp Neurol 2006;65:478-88
72. Hall ED, Bryant YD, Cho W, et al. Evolution of posttraumatic neurodegeneration after controlled cortical impact traumatic brain injury in mice and rats as assessed by the de Olmos silver and fluorojade staining methods. J Neurotrauma 2008;25:235-47
73. Lifshitz J, Kelley BJ, Povlishock JT. Perisomatic thalamic axotomy after diffuse traumatic brain injury is associated with atrophy rather than cell death. J Neuropathol Exp Neurol 2007;66:218-29
74. Ding K, Marquez de la Plata C, Wang JY, et al. Cerebral atrophy after traumatic white matter injury: Correlation with acute neuroimaging and outcome. J Neurotrauma 2008;25:1433-40
75. Singleton RH, Povlishock JT. Identification and characterization of heterogeneous neuronal injury and death in regions of diffuse brain injury: Evidence for multiple independent injury phenotypes. J Neurosci 2004; 24:3543-53
76. Graham DI, Smith C, Reichard R, et al. Trials and tribulations of using beta-amyloid precursor protein immunohistochemistry to evaluate traumatic brain injury in adults. Forensic Sci Int 2004;146:89-96
77. Singleton RH, Zhu J, Stone JR, et al. Traumatically induced axotomy adjacent to the soma does not result in acute neuronal death. J Neurosci 2002;22:791-802
78. Favorov OV, Diamond ME. Demonstration of discrete place-defined columns-segregates in the cat SI. J Comp Neurol 1990;298:97-112
79. Sisodiya SM, Heffernan J, Harrison PJ, et al. Sulcogyral variation in NMDA receptor 2A/B subunit immunoreactivity in human brain. Neuroreport 2000;11:2601-6
80. Clinton J, Roberts GW, Gentleman SM, et al. Differential pattern of beta-amyloid protein deposition within cortical sulci and gyri in Alzheimer's disease. Neuropathol Appl Neurobiol 1993;19:277-81
81. Armstrong RA. A spatial pattern analysis of beta-amyloid (Abeta) deposition in the temporal lobe in Alzheimer's disease. Folia Neuropathol 2010;48:67-74
82. Leclerc SS, Rice FL, Dykes RW, et al. Electrophysiological examination of the representation of the face in the suprasylvian gyrus of the ferret: A correlative study with cytoarchitecture. Somatosens Mot Res 1993;10:133-59
83. Makris N, Kaiser J, Haselgrove C, et al. Human cerebral cortex: A system for the integration of volume- and surface-based representations. Neuroimage 2006;33:139-53
84. McNab JA, Polimeni JR, Wang R, et al. Surface based analysis of diffusion orientation for identifying architectonic domains in the in vivo human cortex. Neuroimage 2013;69:87-100
85. Edlow BL, Wu O. Advanced neuroimaging in traumatic brain injury. Sem Neurol 2012;32:372-98
86. Giacino JT, Whyte J, Bagiella E, et al. Placebo-controlled trial of amantadine for severe traumatic brain injury. N Engl J Med 2012;366: 819-26
87. Reese TG, Benner T, Wang R, et al. Halving imaging time of whole brain diffusion spectrum imaging and diffusion tractography using simultaneous image refocusing in EPI. J Magn Reson Imaging 2009;29: 517-22