Delayed thalamic astrocytosis and disrupted sleep-wake patterns in a preclinical model of traumatic brain injury

Journal of Neuroscience Research

Volumn 92, Issue 11, 2014, Pages 1434-1445

  Hazra, Anupam ^a,b   Macolino, Christine ^a,b   Elliott, Melanie B ^a,b   Chin, Jeannie ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Inflammation; Sleep fragmentation; Sleep wake; Thalamus; Traumatic brain injury

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AROUSAL; ARTICLE; ASTROCYTOSIS; CELL ACTIVATION; CONTROLLED STUDY; INFLAMMATION; LATERAL RETICULAR NUCLEUS; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SELF CARE; SLEEP DISORDER; SLEEP PATTERN; SLEEP WAKING CYCLE; THALAMOCORTICAL TRACT; THALAMUS; THALAMUS RETICULAR NUCLEUS; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURY; C57BL MOUSE; COMPLICATION; DISEASE MODEL; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GLIOSIS; GROOMING; METABOLISM; PATHOLOGY; PHYSIOLOGY; SLEEP-WAKE TRANSITION DISORDERS;

ACTIN BINDING PROTEIN; AIF1 PROTEIN, MOUSE; CALCIUM BINDING PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMALS; BRAIN INJURIES; CALCIUM-BINDING PROTEINS; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; GROOMING; MICE; MICE, INBRED C57BL; MICROFILAMENT PROTEINS; SLEEP-WAKE TRANSITION DISORDERS; THALAMUS;

EID: 84906320951     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23430     Document Type: Article

References (72)

1. Acosta SA, Tajiri N, Shinozuka K, Ishikawa H, Grimmig B, Diamond D, Sanberg PR, Bickford PC, Kaneko Y, Borlongan CV. 2013. Long-term upregulation of inflammation and suppression of cell proliferation in the brain of adult rats exposed to traumatic brain injury using the controlled cortical impact model. PLoS One 8:e53376.
2. Adamah-Biassi EB, Stepien I, Hudson RL, Dubocovich ML. 2013. Automated video analysis system reveals distinct diurnal behaviors in C57BL/6 and C3H/HeN mice. Behav Brain Res 243:306-312.
3. Ajao DO, Pop V, Kamper JE, Adami A, Rudobeck E, Huang L, Vlkolinsky R, Hartman RE, Ashwal S, Obenaus A, Badaut J. 2012. Traumatic brain injury in young rats leads to progressive behavioral deficits coincident with altered tissue properties in adulthood. J Neurotrauma 29:2060-2074.
4. Amenta PS, Jallo JI, Tuma RF, Elliott MB. 2012. A cannabinoid type 2 receptor agonist attenuates blood-brain barrier damage and neurodegeneration in a murine model of traumatic brain injury. J Neurosci Res 90:2293-2305.
5. 2+ channel plays a crucial role in stabilizing sleep. Proc Natl Acad Sci U S A 102:1743-1748.
6. Arciniegas DB, McAllister TW. 2008. Neurobehavioral management of traumatic brain injury in the critical care setting. Crit Care Clin 24:737-765, viii.
7. Beenhakker MP, Huguenard JR. 2009. Neurons that fire together also conspire together: is normal sleep circuitry hijacked to generate epilepsy? Neuron 62:612-632.
8. Ben Achour S, Pascual O. 2012. Astrocyte-neuron communication: functional consequences. Neurochem Res 37:2464-2473.
9. Blethyn KL, Hughes SW, Toth TI, Cope DW, Crunelli V. 2006. Neuronal basis of the slow (<1 Hz) oscillation in neurons of the nucleus reticularis thalami in vitro. J Neurosci 26:2474-2486.
10. Bogdanova Y, Verfaellie M. 2012. Cognitive sequelae of blast-induced traumatic brain injury: recovery and rehabilitation. Neuropsychol Rev 22:4-20.
11. Bohnen N, Van Zutphen W, Twijnstra A, Wijnen G, Bongers J, Jolles J. 1994. Late outcome of mild head injury: results from a controlled postal survey. Brain Inj 8:701-708.
12. Bouilleret V, Cardamone L, Liu YR, Fang K, Myers DE, O'Brien TJ. 2009. Progressive brain changes on serial manganese-enhanced MRI following traumatic brain injury in the rat. J Neurotrauma 26:1999-2013.
13. Carbonell WS, Grady MS. 1999. Regional and temporal characterization of neuronal, glial, and axonal response after traumatic brain injury in the mouse. Acta Neuropathol 98:396-406.
14. Carter MD, Shah CR, Muller CL, Crawley JN, Carneiro AM, Veenstra-VanderWeele J. 2011. Absence of preference for social novelty and increased grooming in integrin beta3 knockout mice: initial studies and future directions. Autism Res 4:57-67.
15. Castriotta RJ, Wilde MC, Lai JM, Atanasov S, Masel BE, Kuna ST. 2007. Prevalence and consequences of sleep disorders in traumatic brain injury. J Clin Sleep Med 3:349-356.
16. Coronado VG, Xu L, Basavaraju SV, McGuire LC, Wald MM, Faul MD, Guzman BR, Hemphill JD. 2011. Surveillance for traumatic brain injury-related deaths-United States, 1997-2007. MMWR Surveill Summ 60:1-32.
17. Crabtree JW, Lodge D, Bashir ZI, Isaac JT. 2013. GABAA, NMDA and mGlu2 receptors tonically regulate inhibition and excitation in the thalamic reticular nucleus. Eur J Neurosci 37:850-859.
18. 2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites. Nat Neurosci 11:683-692.
19. Daneshvar DH, Nowinski CJ, McKee AC, Cantu RC. 2011. The epidemiology of sport-related concussion. Clin Sports Med 30:1-17, vii.
20. Elliott MB, Jallo JJ, Barbe MF, Tuma RF. 2009. Hypertonic saline attenuates tissue loss and astrocyte hypertrophy in a model of traumatic brain injury. Brain Res 1305:183-191.
21. Elliott MB, Oshinsky ML, Amenta PS, Awe OO, Jallo JI. 2012. Nociceptive neuropeptide increases and periorbital allodynia in a model of traumatic brain injury. Headache 52:966-984.
22. Elliott MB, Tuma RF, Amenta PS, Barbe MF, Jallo JI. 2011. Acute effects of a selective cannabinoid-2 receptor agonist on neuroinflammation in a model of traumatic brain injury. J Neurotrauma 28:973-981.
23. Faul M, Xu L, Wald MM, Coronado VG. 2010. Traumatic brain injury in the United States: emergency department visits, hospitalizations and deaths 2002-2006.
24. (http://www.cdc.gov/traumaticbraininjury/tbi_ed.html).
25. Fujita M, Sugama S, Sekiyama K, Sekigawa A, Tsukui T, Nakai M, Waragai M, Takenouchi T, Takamatsu Y, Wei J, Rockenstein E, Laspada AR, Masliah E, Inoue S, Hashimoto M. 2010. A beta-synuclein mutation linked to dementia produces neurodegeneration when expressed in mouse brain. Nat Commun 1:110.
26. Garcia-Panach J, Lull N, Lull JJ, Ferri J, Martinez C, Sopena P, Robles M, Chirivella J, Noe E. 2011. A voxel-based analysis of FDG-PET in traumatic brain injury: regional metabolism and relationship between the thalamus and cortical areas. J Neurotrauma 28:1707-1717.
27. Grossman EJ, Ge Y, Jensen JH, Babb JS, Miles L, Reaume J, Silver JM, Grossman RI, Inglese M. 2012. Thalamus and cognitive impairment in mild traumatic brain injury: a diffusional kurtosis imaging study. J Neurotrauma 29:2318-2327.
28. Hall ED, Bryant YD, Cho W, Sullivan PG. 2008. Evolution of post-traumatic 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 25:235-247.
29. Hirsch LJ. 2008. Nonconvulsive seizures in traumatic brain injury: what you don't see can hurt you. Epilepsy Curr 8:97-99.
30. Hunt RF, Boychuk JA, Smith BN. 2013. Neural circuit mechanisms of post-traumatic epilepsy. Front Cell Neurosci 7:89.
31. Ito S, Ogiwara I, Yamada K, Miyamoto H, Hensch TK, Osawa M, Yamakawa K. 2012. Mouse with Na(v)1.1 haploinsufficiency, a model for Dravet syndrome, exhibits lowered sociability and learning impairment. Neurobiol Dis 49C:29-40.
32. Jacobowitz DM, Cole JT, McDaniel DP, Pollard HB, Watson WD. 2012. Microglia activation along the corticospinal tract following traumatic brain injury in the rat: a neuroanatomical study. Brain Res 1465:80-89.
33. Jhuang H, Garrote E, Mutch J, Yu X, Khilnani V, Poggio T, Steele AD, Serre T. 2010. Automated home-cage behavioural phenotyping of mice. Nat Commun 1:68.
34. Ji RR, Berta T, Nedergaard M. 2013. Glia and pain: Is chronic pain a gliopathy? Pain 154 Suppl 1.
35. Jones EG. 2009. Synchrony in the interconnected circuitry of the thalamus and cerebral cortex. Ann N Y Acad Sci 1157:10-23.
36. Kasturi BS, Stein DG. 2009. Traumatic brain injury causes long-term reduction in serum growth hormone and persistent astrocytosis in the cortico-hypothalamo-pituitary axis of adult male rats. J Neurotrauma 26:1315-1324.
37. Laird MD, Vender JR, Dhandapani KM. 2008. Opposing roles for reactive astrocytes following traumatic brain injury. Neurosignals 16:154-164.
38. Lange RT, Brickell TA, Ivins B, Vanderploeg RD, French LM. 2013. Variable, not always persistent, postconcussion symptoms after mild TBI in U.S. military service members: a five-year cross-sectional outcome study. J Neurotrauma 30:958-969.
39. Lee J, Kim D, Shin HS. 2004. Lack of delta waves and sleep disturbances during non-rapid eye movement sleep in mice lacking alpha1G-subunit of T-type calcium channels. Proc Natl Acad Sci U S A 101:18195-18199.
40. Llinas RR, Steriade M. 2006. Bursting of thalamic neurons and states of vigilance. J Neurophysiol 95:3297-3308.
41. Lull N, Noe E, Lull JJ, Garcia-Panach J, Chirivella J, Ferri J, Lopez-Aznar D, Sopena P, Robles M. 2010. Voxel-based statistical analysis of thalamic glucose metabolism in traumatic brain injury: relationship with consciousness and cognition. Brain Inj 24:1098-1107.
42. Martinowich K, Schloesser RJ, Jimenez DV, Weinberger DR, Lu B. 2011. Activity-dependent brain-derived neurotrophic factor expression regulates cortistatin-interneurons and sleep behavior. Mol Brain 4:11.
43. Mathias JL, Alvaro PK. 2012. Prevalence of sleep disturbances, disorders, and problems following traumatic brain injury: a meta-analysis. Sleep Med 13:898-905.
44. McMahon PJ, Hricik AJ, Yue JK, Puccio AM, Inoue T, Lingsma H, Beers SR, Gordon W, Valadka A, Manley GTMDPD, Okonkwo DO. 2013. Symptomatology and functional outcome in mild traumatic brain injury: results from the prospective TRACK-TBI Study. J Neurotrauma [E-pub ahead of print].
45. Mochel F, Durant B, Durr A, Schiffmann R. 2011. Altered dopamine and serotonin metabolism in motorically asymptomatic R6/2 mice. PLoS One 6:e18336.
46. Nakayama N, Okumura A, Shinoda J, Nakashima T, Iwama T. 2006. Relationship between regional cerebral metabolism and consciousness disturbance in traumatic diffuse brain injury without large focal lesions: an FDG-PET study with statistical parametric mapping analysis. J Neurol Neurosurg Psychiatry 77:856-862.
47. Nardone R, Bergmann J, Kunz A, Caleri F, Seidl M, Tezzon F, Gerstenbrand F, Trinka E, Golaszewski S. 2011. Cortical excitability changes in patients with sleep-wake disturbances after traumatic brain injury. J Neurotrauma 28:1165-1171.
48. Nilsson P, Ronne-Engstrom E, Flink R, Ungerstedt U, Carlson H, Hillered L. 1994. Epileptic seizure activity in the acute phase following cortical impact trauma in rat. Brain Res 637:227-232.
49. Onyszchuk G, LeVine SM, Brooks WM, Berman NE. 2009. Post-acute pathological changes in the thalamus and internal capsule in aged mice following controlled cortical impact injury: a magnetic resonance imaging, iron histochemical, and glial immunohistochemical study. Neurosci Lett 452:204-208.
50. Orff HJ, Ayalon L, Drummond SP. 2009. Traumatic brain injury and sleep disturbance: a review of current research. J Head Trauma Rehabil 24:155-165.
51. Ouellet MC, Morin CM. 2006. Subjective and objective measures of insomnia in the context of traumatic brain injury: a preliminary study. Sleep Med 7:486-497.
52. Parcell DL, Ponsford JL, Rajaratnam SM, Redman JR. 2006. Self-reported changes to nighttime sleep after traumatic brain injury. Arch Phys Med Rehabil 87:278-285.
53. Roozenbeek B, Maas AI, Menon DK. 2013. Changing patterns in the epidemiology of traumatic brain injury. Nat Rev Neurol 9:231-236.
54. Ryan LM, Warden DL. 2003. Post concussion syndrome. Int Rev Psychiatry 15:310-316.
55. Sandhir R, Onyszchuk G, Berman NE. 2008. Exacerbated glial response in the aged mouse hippocampus following controlled cortical impact injury. Exp Neurol 213:372-380.
56. Santarnecchi E, Sicilia I, Richiardi J, Vatti G, Polizzotto NR, Marino D, Rocchi R, Van De Ville D, Rossi A. 2013. Altered cortical and subcortical local coherence in obstructive sleep apnea: a functional magnetic resonance imaging study. J Sleep Res 22:337-347.
57. Sayer NA. 2012. Traumatic brain injury and its neuropsychiatric sequelae in war veterans. Annu Rev Med 63:405-419.
58. Statler KD, Swank S, Abildskov T, Bigler ED, White HS. 2008. Traumatic brain injury during development reduces minimal clonic seizure thresholds at maturity. Epilepsy Res 80:163-170.
59. Steele AD, Jackson WS, King OD, Lindquist S. 2007. The power of automated high-resolution behavior analysis revealed by its application to mouse models of Huntington's and prion diseases. Proc Natl Acad Sci U S A 104:1983-1988.
60. Steriade M, Contreras D, Curro Dossi R, Nunez A. 1993a. The slow (<1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci 13:3284-3299.
61. Steriade M, McCormick DA, Sejnowski TJ. 1993b. Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679-685.
62. Tang L, Ge Y, Sodickson DK, Miles L, Zhou Y, Reaume J, Grossman RI. 2011. Thalamic resting-state functional networks: disruption in patients with mild traumatic brain injury. Radiology 260:831-840.
63. Taylor RA, Sansing LH. 2013. Microglial responses after ischemic stroke and intracerebral hemorrhage. Clin Dev Immunol 2013:746068.
64. Thomas WE. 1992. Brain macrophages: evaluation of microglia and their functions. Brain Res Brain Res Rev 17:61-74.
65. Vanderploeg RD, Belanger HG. 2013. Screening for a remote history of mild traumatic brain injury: when a good idea is bad. J Head Trauma Rehabil 28:211-218.
66. Verma A, Anand V, Verma NP. 2007. Sleep disorders in chronic traumatic brain injury. J Clin Sleep Med 3:357-362.
67. Vespa PM, McArthur DL, Xu Y, Eliseo M, Etchepare M, Dinov I, Alger J, Glenn TP, Hovda D. 2010. Nonconvulsive seizures after traumatic brain injury are associated with hippocampal atrophy. Neurology 75:792-798.
68. Vespa PM, Nuwer MR, Nenov V, Ronne-Engstrom E, Hovda DA, Bergsneider M, Kelly DF, Martin NA, Becker DP. 1999. Increased incidence and impact of nonconvulsive and convulsive seizures after traumatic brain injury as detected by continuous electroencephalographic monitoring. J Neurosurg 91:750-760.
69. Washington PM, Forcelli PA, Wilkins T, Zapple DN, Parsadanian M, Burns MP. 2012. The effect of injury severity on behavior: a phenotypic study of cognitive and emotional deficits after mild, moderate, and severe controlled cortical impact injury in mice. J Neurotrauma 29:2283-2296.
70. Wortzel HS, Arciniegas DB. 2012. Treatment of post-traumatic cognitive impairments. Curr Treat Options Neurol 14:493-508.
71. Zafonte RD, Watanabe TK, Mann NR, Ko DH. 1997. Psychogenic polydipsia after traumatic brain injury. A case report. Am J Phys Med Rehabil 76:246-248.
72. Zhou Y, Lui YW, Zuo XN, Milham MP, Reaume J, Grossman RI, Ge Y. 2013. Characterization of thalamo-cortical association using amplitude and connectivity of functional MRI in mild traumatic brain injury. J Magn Reson Imaging (in press).