Cognitive impairment and persistent anxiety-related responses following bilateral common carotid artery occlusion in mice

Behavioural Brain Research

Volumn 249, Issue , 2013, Pages 28-37

  Soares, Lígia Mendes ^a   Schiavon, Angélica Pupin ^a   Milani, Humberto ^a   De Oliveira, Rúbia Maria Weffort ^a  

^a STATE UNIVERSITY OF MARINGÁ   (Brazil)

Author keywords

Anxiety; Bilateral common carotid artery occlusion; Mice; Neurodegeneration; Neurogenesis; Spatial memory

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN ISCHEMIA; CAROTID ARTERY OBSTRUCTION; COGNITIVE DEFECT; COMMON CAROTID ARTERY; CONTROLLED STUDY; HIPPOCAMPAL CA3 REGION; HISTOPATHOLOGY; LOCOMOTION; MALE; MAZE TEST; MEMORY; MOUSE; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REPERFUSION; SPATIAL LEARNING;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BRAIN ISCHEMIA; CAROTID ARTERY, COMMON; CAROTID STENOSIS; CELL COUNT; COGNITION DISORDERS; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; NEUROGENESIS; NEURONS;

EID: 84877818111     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.04.010     Document Type: Article

References (74)

1. Sunnerhagen K.S., Johanssona O., Herlitzb J., Grimbya G. Life after cardiac arrest; a retrospective study. Resuscitation 1996, 31(2):135-140.
2. Anderson C.A., Arciniegas D.B. Cognitive sequelae of hypoxic-ischemic brain injury: a review. NeuroRehabilitation 2010, 26(1):47-63.
3. Peskine A., Picq C., Pradat-diehl P. Neurological sequelae after cerebral anoxia. Brain Injury 2010, 24(5):755-761.
4. Zola-Morgan S., Squire L.R., Amaral D.G. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the Hippocampus. Journal of Neuroscience 1986, 6(10):2950-2967.
5. Kartsounis L.D., Rudge P., Stevens J.M. Bilateral lesions of CA1 and CA2 fields of the hippocampus are sufficient to cause a severe amnesic syndrome in humans. Journal of Neurology, Neurosurgery and Psychiatry 1995, 59(1):95-98.
6. Moulaert V.R., Wachelder E.M., Verbunt J.A., Wade D.T., van Heugten C.M. Determinants of quality of life in survivors of cardiac arrest. Journal of Rehabilitation Medicine 2010, 42(6):553-558.
7. Mateen F.J., Josephs K.A., Trenerry M.R., Felmlee-Devine M.D., Weaver A.L., Carone M., et al. Long-term cognitive outcomes following out-of-hospital cardiac arrest: a population-based study. Neurology 2011, 77(15):1438-1445.
8. Bachevalier J., Meunier M. Cerebral ischemia: are the memory deficits associated with hippocampal cell loss?. Hippocampus 1996, 6(5):553-560.
9. Kimura M., Tateno A., Robinson R.G. Treatment of poststroke generalized anxiety disorder comorbid with poststroke depression: merged analysis of nortriptyline trials. American Journal of Geriatric Psychiatry 2003, 11:320-327.
10. Leppävuori A., Pohjasvaara T., Vataja R., Kaste M., Erkinjuntti T. Generalized anxiety disorders three to four months after ischemic stroke. Cerebrovascular Diseases 2003, 16(3):257-264.
11. Ladwig K.H., Schoefinius A., Dammann G., Danner R., Gürtler R., Herrmann R. Long-acting psychotraumatic properties of a cardiac arrest experience. American Journal of Psychiatry 1999, 156(6):912-919.
12. Wellons J.C., Sheng H., Laskowitz D.T., BurkhardMackensen G., Pearlstein R.D., Warner D.S. A comparison of strain-related susceptibility in two murine recovery models of global cerebral ischemia. Brain Research 2000, 868(1):14-21.
13. Zhang L., Fu F., Zhang X., Zhu M., Wang T., Fan H. Escin attenuates cognitive deficits and hippocampal injury after transient global cerebral ischemia in mice via regulating certain inflammatory genes. Neurochemistry International 2010, 57(2):119-127.
14. Kumaran D., Udayabanu M., Nair R.U., Katyal R.A.A. Benzamide protects delayed neuronal death and behavioural impairment in a mouse model of global cerebral ischemia. Behavioural Brain Research 2008, 192(2):178-184.
15. Bora K.S., Arora S., Shri R. Role of Ocimum basilicum L in prevention of ischemia and reperfusion-induced cerebral damage, and motor dysfunctions in mice brain. Journal of Ethnopharmacology 2011, 137(3):1360-1365.
16. Rajput S.K., Siddiqui M.A., Kumar V., Meena C.L., Pant A.B., Jain R., et al. Protective effects of L-pGlu-(2-propyl)-L-His-L-ProNH2, a newer thyrotropin releasing hormone analog in in vitro and in vivo models of cerebral ischemia. Peptides 2011, 32(6):1225-1231.
17. Rehni A.K., Singh T.G. Involvement of CCR-2 chemokine receptor activation in ischemic preconditioning and postconditioning of brain in mice. Cytokine 2012, 60(1):83-89.
18. Yan B., He J., Xu H., Zhang Y., Bi X., Thakur S., et al. Quetiapine attenuates the depressive and anxiolytic-like behavioural changes induced by global cerebral ischemia in mice. Behavioural Brain Research 2007, 182(1):36-41.
19. Shen J., Bai X.Y., Qin Y., Jin W.W., Zhou J.Y., Zhou J.P., et al. Interrupted reperfusion reduces the activation of NADPH oxidase after cerebral I/R injury. Free Radical Biology and Medicine 2011, 50(12):1780-1786.
20. Corbett D., Nurse S. The problem of assessing effective neuroprotection in experimental cerebral ischemia. Progress in Neurobiology 1998, 54(5):531-548.
21. Langdon K.D., Granter-button S., Corbett D. Persistent behaviour impairments and neuroinflammation following global ischemia in the rat. European Journal of Neuroscience 2008, 28:2310-2318.
22. Fujii M., Hara H., Meng W., Vonsattel J.P., Huang Z., Moskowitz M.A. Strain-related differences in susceptibility to transient forebrain ischemia in SV-129 and C57black/6 mice. Stroke 1997, 28(9):1805-1810.
23. Sheng H., Laskowitz D.T., Pearlstein R.D., Warner D.S. Characterization of a recovery global cerebral ischemia model in the mouse. Journal of Neuroscience Methods 1999, 88:103-109.
24. Kawahara N., Kawai K., Toyoda T., Nakatomi H., Furuya K., Kirino T. Cardiac arrest cerebral ischemia model in mice failed to cause delayed neuronal death in the hippocampus. Neuroscience Letters 2002, 322:91-94.
25. Macrae I.M. Preclinical stroke research-advantages and disadvantages of the most common rodent models of focal ischaemia. British Journal of Pharmacology 2011, 164(4):1062-1078.
26. Nakashima M.N., Aijiki K., Nakashima K., Takashi M. Possible role of nitric oxide in anxiety following transient cerebral ischemia in mice. Journal of Pharmacological Sciences 2003, 91:47-52.
27. Neigh G.N., Karelina K., Glasper E.R., Bowers S.L., Zhang N., Popovich P.G., et al. Anxiety after cardiac arrest/cardiopulmonary resuscitation: exacerbated by stress and prevented by minocycline. Stroke 2009, 40(11):3601-3607.
28. Prediger R.D., Fernandes M.S., Rial D., Wopereis S., Pereira V.S., Bosse T.S., et al. Effects of acute administration of the hydroalcoholic extract of mate tea leaves (Ilex paraguariensis) in animal models of learning and memory. Journal of Ethnopharmacology 2008, 120(3):465-473.
29. Royce J.R. On the construct validity of open-field measures. Psychological Bulletin 1977, 84(6):1098-1106.
30. Lister R.G. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 1987, 92(2):180-185.
31. Franklin K.B.J., Paxinos G. The mouse brain in stereotaxic coordinates 1997, Academic Press, San Diego. 2nd ed.
32. Schmued L.C., Stowers C.C., Scallet A.C., Xu L. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Research 2005, 1035(1):24-31.
33. Sato M., Chang E., Igarashi T., Noble L.J. Neuronal injury and loss after traumatic brain injury: time course and regional variability. Brain Research 2001, 917(1):45-54.
34. Altman J. Autoradiographic and histological studies of postnatal neurogenesis IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. Journal of Comparative Neurology 1969, 137:433-457.
35. Brown J.P., Couillard-Després S., Cooper-Kuhn C.M., Winkler J., Aigner L., Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. Journal of Comparative Neurology 2003, 467(1):1-10.
36. Von Bohlen Halbach O. Immunohistological markers for staging neurogenesis in adult hippocampus. Cell and Tissue Research 2007, 329(3):409-420.
37. Yang G., Kitagawa K., Matsushita K., Mabuchi T., Yagita Y., Yanagihara T. Matsumoto M.C57BL/6 strain is most susceptible to cerebral ischemia following bilateral common carotid occlusion among seven mouse strains: selective neuronal death in the murine transient forebrain ischemia. Brain Research 1997, 752(1-2):209-218.
38. Braeuninger S., Kleinschnitz C. Rodent models of focal cerebral ischemia: procedural pitfalls and translational problems. Experimental & Translational Stroke Medicine 2009, 1:8.
39. Woodruff T.M., Thundyil J., Tang S.C., Sobey C.G., Taylor S.M., Arumugam T.V. Pathophysiology, treatment, and animal and cellular models of human ischemic stroke. Molecular Neurodegeneration 2011, 6(1):11.
40. Gupta R., Singh M., Sharma A. Neuroprotective effect of antioxidants on ischaemia and reperfusion-induced cerebral injury. Pharmacological Research 2003, 48(2):209-215.
41. Von Euler M., Bendel O., Bueters T., Sandin J., von Euler G. Profound but transient deficits in learning and memory after global ischemia using a novel water maze test. Behavioural Brain Research 2006, 166(2):204-210.
42. Aoyagi A., Saito H., Abe K., Nishiyama N. Early impairment and late recovery of synaptic transmission in the rat dentate gyrus following transient forebrain ischemia in vivo. Brain Research 1998, 799(1):130-137.
43. Lee I., Kesner R.P. Differential roles of dorsal hippocampal subregions in spatial working memory with short versus intermediate delay. Behavioral Neuroscience 2003, 117(5):1044-1053.
44. Dalley J.W., Cardinal R.N., Robbins T.W. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neuroscience and Biobehavioral Reviews 2004, 28(7):771-784.
45. Maki T., Ihara M., Fujita Y., Nambu T., Miyashita K., Yamada M., et al. Angiogeni and vasoprotective effects of adrenomedullin on prevention of cognitive decline after chronic cerebral hypoperfusion in mice. Stroke 2011, 42(4):1122-1128.
46. Raber J., Fan Y., Matsumori Y., Liu Z., Weinstein P.R., Fike J.R., et al. Irradiation attenuates neurogenesis and exacerbates ischemia-induced deficits. Annals of Neurology 2004, 55(3):381-389.
47. Yasuda Y., Shimoda T., Uno K., Tateishi N., Furuya S., Tsuchihashi Y., et al. Temporal and sequential changes of glial cells and cytokine expression during neuronal degeneration after transient global ischemia in rats. Journal of Neuroinflammation 2011, 8:70.
48. Nakatomi H., Kuriu T., Okabe S., Yamamoto S., Hatano O., Kawahara N., et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 2002, 110(4):429-441.
49. Kawai T., Takagi N., Miyake-Takagi K., Okuyama N., Mochizuki N., Takeo S. Characterization of BrdU-positive neurons induced by transient global ischemia in adult hippocampus. Journal of Cerebral Blood Flow and Metabolism 2004, 24(5):548-555.
50. Bendel O., Bueters T., von Euler M., OveOgren S., Sandin J., von Euler G. Reappearance of hippocampal CA1 neurons after ischemia is associated with recovery of learning and memory. Journal of Cerebral Blood Flow and Metabolism 2005, 25(12):1586-1595.
51. Briones T.L., Woods J., Wadowska M., Rogozinska M. Amelioration of cognitive impairment and changes in microtubule-associated protein 2 after transient global cerebral ischemia are influenced by complex environment experience. Behavioural Brain Research 2006, 168(2):261-271.
52. Yagita Y., Kitagawa K., Ohtsuki T., Takasawa K., Miyata T., Okano H., et al. Neurogenesis by progenitor cells in the ischemic adult rat hippocampus. Stroke 2001, 32:1890-1896.
53. Schiavon A.P., Milani H., Romanini C.V., Foresti M.L., Castro O.W., Garcia-cairasco N., et al. Imipramine enhances cell proliferation and decreases neurodegeneration in the hippocampus after transient global cerebral ischemia in rats. Neuroscience Letters 2010, 470:43-48.
54. Liu J., Solway K., Messing R.O., Sharp F.R. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. Journal of Neuroscience 1998, 18(19):7768-7778.
55. Arvidsson A., Collin T., Kirik D., Kokaia Z., Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nature Medicine 2002, 8(9):963-970.
56. Pforte C., Henrich-Noack P., Baldauf K., Reymann K.G. Increase in proliferation and gliogenesis but decrease of early neurogenesis in the rat forebrain shortly after transient global ischemia. Neuroscience 2005, 136(4):1133-1146.
57. Schloesser RJ, Jimenez DV, Hardy NF, Paredes D, Catlow BJ, Manji HK, et al. Atrophy of pyramidal neurons and increased stress-induced glutamate levels in CA3 following chronic suppression of adult neurogenesis. Brain Struct Funct 2013; doi:10.1007/s00429-013-0532-8.
58. Ramos A. Animal models of anxiety: do I need multiple tests?. Trends in Pharmacological Sciences 2008, 29(10):493-498.
59. Ramos A., Correia E.C., Izídio G.S., Brüske G.R. Genetic selection of two new rat lines displaying different levels of anxiety-related behaviors. Behavior Genetics 2003, 33(6):657-668.
60. Milot M.R., Plamondon H. Changes in HPA reactivity and noradrenergic functions regulate spatial memory impairments at delayed time intervals following cerebral ischemia. Hormones and Behavior 2011, 59(4):594-604.
61. Pittenger C., Duman R.S. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 2008, 33(1):88-109.
62. Revest J.M., Dupret D., Koehl M., Funk-Reiter C., Grosjean N., Piazza P.V., et al. Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Molecular Psychiatry 2009, 14(10):959-967.
63. Sah A, Schmuckermair C, Sartori SB, Gaburro S, Kandasamy M, Irschick R, Klimaschewski L, Landgraf R, Aigner L, Singewald N, Anxiety-rather than depression-like behavior is associated with adult neurogenesis in a female mouse model of higher trait anxiety- and comorbid depression-like behavior. Transl Psychiatry 2012;16(2):e171.
64. Carty M.L., Wixey J.A., Kesby J., Reinebrant H.E., Colditz P.B., Gobe G., et al. Long-term losses of amygdala corticotropin-releasing factor neurons are associated with behavioural outcomes following neonatal hypoxia-ischemia. Behavioural Brain Research 2010, 208(2):609-618.
65. Teschendorf P., Padosch S.A., Spöhr F., Albertsmeier M., Schneider A., Vogel P., et al. Time course of caspase activation in selectively vulnerable brain areas following global cerebral ischemia due to cardiac arrest in rats. Neuroscience Letters 2008, 448(2):194-199.
66. Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Research 1982, 239:57-69.
67. Pulsinelli W.A., Brierley J.B., Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Annals of Neurology 1982, 11:491-498.
68. Sugawara T., Kawase M., Lewén A., Noshita N., Gasche Y., Fujimura M., et al. Effect of hypotension severity on hippocampal CA1 neurons in a rat global ischemia model. Brain Research 2000, 877(2):281-287.
69. Kim D.H., Kim S., Jung W.Y., Park S.J., Park D.H., Kim J.M., et al. The neuroprotective effects of the seeds of Cassia obtusifolia on transient cerebral global ischemia in mice. Food and Chemical Toxicology 2009, 47:1473-1479.
70. Lee J-H, Lee S-R. The effect of baicalein on hippocampal neuronal damage and metalloproteinase activity following transient global cerebral ischaemia. Phytother Res 2012. doi:10.1002/ptr.4644.
71. Yoshioka H., Niizuma K., Katsu M., Sakata H., Okami N., Chan P.H. Consistent injury to medium spiny neurons and white matter in the mouse striatum after prolonged transient global cerebral ischemia. Journal of Neurotrauma 2011, 28(4):649-660.
72. Magariños A.M., McEwen B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 1995, 69(1):83-88.
73. File S.E., Kenny P.J., Cheeta S. The role of the dorsal hippocampal serotonergic and cholinergic systems in the modulation of anxiety. Pharmacology Biochemistry and Behavior 2000, 66(1):65-72.
74. Soetanto A., Wilson R.S., Talbot K., Un A., Schneider J.A., Sobiesk M., et al. Association of anxiety and depression with microtubule-associated protein 2- and synaptopodin-immunolabeled dendrite and spine densities in hippocampal CA3 of older humans. Archives of General Psychiatry 2010, 67(5):448-457.