Impact of aging on spreading depolarizations induced by focal brain ischemia in rats

Neurobiology of Aging

Volumn 35, Issue 12, 2014, Pages 2803-2811

  Clark, Darren ^a,b   Institoris, Ádám ^c   Kozák, Gábor ^a   Bere, Zsófia ^c   Tuor, Ursula ^b   Farkas, Eszter ^a   Bari, Ferenc ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Inverse neurovascular coupling; Middle cerebral artery occlusion; Multimodal imaging; Peri infarct depolarization; Voltage sensitive dye

Indexed keywords

ADULT; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN BLOOD VOLUME; BRAIN CORTEX; BRAIN ISCHEMIA; BRAIN PERFUSION; BRAIN TISSUE; CONTROLLED STUDY; GREEN LIGHT REFLECTANCE; HEMODYNAMICS; IMAGE ANALYSIS; IMAGING AND DISPLAY; LASER SPECKLE IMAGING; LIGHT EMITTING DIODE; MALE; MEMBRANE POTENTIAL; MIDDLE AGED; MIDDLE CEREBRAL ARTERY OCCLUSION; MULTIMODAL IMAGING; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; RAT; SPREADING DEPOLARIZATION; VOLTAGE SENSITIVE DYE IMAGING; ANIMAL; BRAIN CIRCULATION; ELECTROPHYSIOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULARIZATION; WISTAR RAT;

AGING; ANIMALS; BRAIN ISCHEMIA; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; ELECTROPHYSIOLOGICAL PHENOMENA; HEMODYNAMICS; MALE; MEMBRANE POTENTIALS; RATS, WISTAR;

EID: 84911363904     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.06.013     Document Type: Article

References (51)

1. Allen C.L., Bayraktutan U. Risk factors for ischaemic stroke. Int. J. Stroke 2008, 3:105-116.
2. Ayata C., Shin H.K., Salomone S., Ozdemir-Gursoy Y., Boas D.A., Dunn A.K., Moskowitz M.A. Pronounced hypoperfusion during spreading depression in mouse cortex. J.Cereb. Blood Flow Metab. 2004, 24:1172-1182.
3. Ay H., Arsava E.M., Koroshetz W.J., Sorensen A.G. Middle cerebral artery infarcts encompassing the insula are more prone to growth. Stroke 2008, 39:373-378.
4. Ba A.M., Guiou M., Pouratian N., Muthialu A., Rex D.E., Cannestra A.F., Chen J.W., Toga A.W. Multiwavelength optical intrinsic signal imaging of cortical spreading depression. J.Neurophysiol. 2002, 88:2726-2735.
5. Baron J.C. Perfusion thresholds in human cerebral ischemia: historical perspective and therapeutic implications. Cerebrovasc. Dis. 2001, 11(Suppl 1):2-8.
6. Busija D.W., Bari F., Domoki F., Horiguchi T., Shimizu K. Mechanisms involved in the cerebrovascular dilator effects of cortical spreading depression. Prog. Neurobiol. 2008, 86:379-395.
7. Chen R.L., Balami J.S., Esiri M.M., Chen L.K., Buchan A.M. Ischemic stroke in the elderly: an overview of evidence. Nat. Rev. Neurol. 2010, 6:256-265.
8. Clark D., Tuor U.I., Thompson R., Institoris A., Kulynych A., Zhang X., Kinniburgh D.W., Bari F., Busija D.W., Barber P.A. Protection against recurrent stroke with resveratrol: endothelial protection. PLoS One 2012, 7:e47792.
9. Copen W.A., Schwamm L.H., Gonzalez R.G., Wu O., Harmath C.B., Schaefer P.W., Koroshetz W.J., Sorensen A.G. Ischemic stroke: effects of etiology and patient age on the time course of the core apparent diffusion coefficient. Radiology 2001, 221:27-34.
10. Dahlem Y.A., Hanke W. Intrinsic optical signal of retinal spreading depression: second phase depends on energy metabolism and nitric oxide. Brain Res. 2005, 1049:15-24.
11. Dijkhuizen R.M., Beekwilder J.P., van der Worp H.B., Berkelbach van der Sprenkel J.W., Tulleken K.A., Nicolay K. Correlation between tissue depolarizations and damage in focal ischemic rat brain. Brain Res. 1999, 840:194-205.
12. Dohmen C., Sakowitz O.W., Fabricius M., Bosche B., Reithmeier T., Ernestus R.I., Brinker G., Dreier J.P., Woitzik J., Strong A.J., Graf R. Spreading depolarizations occur in human ischemic stroke with high incidence. Ann. Neurol. 2008, 63:720-728.
13. Dreier J.P. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat. Med. 2011, 17:439-447.
14. Dreier J.P., Major S., Manning A., Woitzik J., Drenckhahn C., Steinbrink J., Tolias C., Oliveira-Ferreira A.I., Fabricius M., Hartings J.A., Vajkoczy P., Lauritzen M., Dirnagl U., Bohner G., Strong A.J. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 2009, 132(Pt 7):1866-1881.
15. Dyall S.C., Michael G.J., Whelpton R., Scott A.G., Michael-Titus A.T. Dietary enrichment with omega-3 polyunsaturated fatty acids reverses age-related decreases in the GluR2 and NR2B glutamate receptor subunits in rat forebrain. Neurobiol. Aging 2007, 28:424-439.
16. Fabricius M., Fuhr S., Bhatia R., Boutelle M., Hashemi P., Strong A.J., Lauritzen M. Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 2006, 129(Pt 3):778-790.
17. Farkas E., Pratt R., Sengpiel F., Obrenovitch T.P. Direct, live imaging of cortical spreading depression and anoxic depolarisation using a fluorescent, voltage-sensitive dye. J.Cereb. Blood Flow Metab. 2008, 28:251-262.
18. Farkas E., Bari F., Obrenovitch T.P. Multi-modal imaging of anoxic depolarization and hemodynamic changes induced by cardiac arrest in the rat cerebral cortex. Neuroimage 2010, 51:734-742.
19. Farkas E., Obrenovitch T.P., Institoris A., Bari F. Effects of early aging and cerebral hypoperfusion on spreading depression in rats. Neurobiol. Aging 2011, 32:1707-1715.
20. Fonarow G.C., Reeves M.J., Zhao X., Olson D.M., Smith E.E., Saver J.L., Schwamm L.H. Age-related differences in characteristics, performance measures, treatment trends, and outcomes in patients with ischemic stroke. Circulation 2010, 121:879-891.
21. Fordsmann J.C., Ko R.W., Choi H.B., Thomsen K., Witgen B.M., Mathiesen C., Lonstrup M., Piilgaard H., MacVicar B.A., Lauritzen M. Increased 20-HETE synthesis explains reduced cerebral blood flow but not impaired neurovascular coupling after cortical spreading depression in rat cerebral cortex. J.Neurosci. 2013, 33:2562-2570.
22. Gonzalez de la Aleja J., Ramos A., Mato-Abad V., Martinez-Salio A., Hernandez-Tamames J.A., Molina J.A., Hernandez-Gallego J., Alvarez-Linera J. Higher glutamate to glutamine ratios in occipital regions in women with migraine during the interictal state. Headache 2013, 53:365-375.
23. Grinvald A., Hildesheim R. VSDI: a new era in functional imaging of cortical dynamics. Nat. Rev. Neurosci. 2004, 5:874-885.
24. Gursoy-Ozdemir Y., Qiu J., Matsuoka N., Bolay H., Bermpohl D., Jin H., Wang X., Rosenberg G.A., Lo E.H., Moskowitz M.A. Cortical spreading depression activates and upregulates MMP-9. J.Clin. Invest. 2004, 113:1447-1455.
25. Hartings J.A., Rolli M.L., Lu X.C., Tortella F.C. Delayed secondary phase of peri-infarct depolarizations after focal cerebral ischemia: relation to infarct growth and neuroprotection. J.Neurosci. 2003, 23:11602-11610.
26. Hoehn-Berlage M., Norris D.G., Kohno K., Mies G., Leibfritz D., Hossmann K.A. Evolution of regional changes in apparent diffusion coefficient during focal ischemia of rat brain: the relationship of quantitative diffusion NMR imaging to reduction in cerebral blood flow and metabolic disturbances. J.Cereb. Blood Flow Metab. 1995, 15:1002-1011.
27. Hossmann K.A. Viability thresholds and the penumbra of focal ischemia. Ann. Neurol. 1994, 36:557-565.
28. Hossmann K.A. Periinfarct depolarizations. Cerebrovasc. Brain Metab. Rev. 1996, 8:195-208.
29. Knoflach M., Matosevic B., Rucker M., Furtner M., Mair A., Wille G., Zangerle A., Werner P., Ferrari J., Schmidauer C., Seyfang L., Kiechl S., Willeit J. Functional recovery after ischemic stroke-a matter of age: data from the Austrian Stroke Unit Registry. Neurology 2012, 78:279-285.
30. Knox C.A. Effects of aging and chronic arterial hypertension on the cell populations in the neocortex and archicortex of the rat. Acta Neuropathol. 1982, 56:139-145.
31. Kudo C., Nozari A., Moskowitz M.A., Ayata C. The impact of anesthetics and hyperoxia on cortical spreading depression. Exp. Neurol. 2008, 212:201-206.
32. Liu P., Smith P.F., Appleton I., Darlington C.L., Bilkey D.K. Age-related changes in nitric oxide synthase and arginase in the rat prefrontal cortex. Neurobiol. Aging 2004, 25:547-552.
33. Luckl J., Zhou C., Durduran T., Yodh A.G., Greenberg J.H. Characterization of periinfarct flow transients with laser speckle and Doppler after middle cerebral artery occlusion in the rat. J.Neurosci. Res. 2009, 87:1219-1229.
34. Magnusson K.R., Brim B.L., Das S.R. Selective vulnerabilities of N-methyl-D-aspartate (NMDA) receptors during brain aging. Front Aging Neurosci. 2010, 2:11.
35. Matchett G.A., Allard M.W., Martin R.D., Zhang J.H. Neuroprotective effect of volatile anesthetic agents: molecular mechanisms. Neurol. Res. 2009, 31:128-134.
36. Mayhan W.G., Arrick D.M., Sharpe G.M., Sun H. Age-related alterations in reactivity of cerebral arterioles: role of oxidative stress. Microcirculation 2008, 15:225-236.
37. Nakamura H., Strong A.J., Dohmen C., Sakowitz O.W., Vollmar S., Sue M., Kracht L., Hashemi P., Bhatia R., Yoshimine T., Dreier J.P., Dunn A.K., Graf R. Spreading depolarizations cycle around and enlarge focal ischaemic brain lesions. Brain 2010, 133(Pt 7):1994-2006.
38. Obrenovitch T.P., Chen S., Farkas E. Simultaneous, live imaging of cortical spreading depression and associated cerebral blood flow changes, by combining voltage-sensitive dye and laser speckle contrast methods. Neuroimage 2009, 45:68-74.
39. Oliveira-Ferreira A.I., Milakara D., Alam M., Jorks D., Major S., Hartings J.A., Luckl J., Martus P., Graf R., Dohmen C., Bohner G., Woitzik J., Dreier J.P. Experimental and preliminary clinical evidence of an ischemic zone with prolonged negative DC shifts surrounded by a normally perfused tissue belt with persistent electrocorticographic depression. J.Cereb. Blood Flow Metab. 2010, 30:1504-1519.
40. Petcu E.B., Sfredel V., Platt D., Herndon J.G., Kessler C., Popa-Wagner A. Cellular and molecular events underlying the dysregulated response of the aged brain to stroke: a mini-review. Gerontology 2008, 54:6-17.
41. Piilgaard H., Witgen B.M., Rasmussen P., Lauritzen M. Cyclosporine A, FK506, and NIM811 ameliorate prolonged CBF reduction and impaired neurovascular coupling after cortical spreading depression. J.Cereb. Blood Flow Metab. 2011, 31:1588-1598.
42. Shin H.K., Dunn A.K., Jones P.B., Boas D.A., Moskowitz M.A., Ayata C. Vasoconstrictive neurovascular coupling during focal ischemic depolarizations. J.Cereb. Blood Flow Metab. 2006, 26:1018-1030.
43. Sonn J., Mayevsky A. Effects of anesthesia on the responses to cortical spreading depression in the rat brain invivo. Neurol. Res. 2006, 28:206-219.
44. Strong A.J., Fabricius M., Boutelle M.G., Hibbins S.J., Hopwood S.E., Jones R., Parkin M.C., Lauritzen M. Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke 2002, 33:2738-2743.
45. Strong A.J., Anderson P.J., Watts H.R., Virley D.J., Lloyd A., Irving E.A., Nagafuji T., Ninomiya M., Nakamura H., Dunn A.K., Graf R. Peri-infarct depolarizations lead to loss of perfusion in ischaemic gyrencephalic cerebral cortex. Brain 2007, 130(Pt 4):995-1008.
46. Uchino H., Minamikawa-Tachino R., Kristian T., Perkins G., Narazaki M., Siesjo B.K., Shibasaki F. Differential neuroprotection by cyclosporin A and FK506 following ischemia corresponds with differing abilities to inhibit calcineurin and the mitochondrial permeability transition. Neurobiol. Dis. 2002, 10:219-233.
47. Ungvari Z., Kaley G., de Cabo R., Sonntag W.E., Csiszar A. Mechanisms of vascular aging: new perspectives. J.Gerontol. A Biol. Sci. Med. Sci. 2010, 65:1028-1041.
48. Weimer M.S., Hanke W. Propagation velocity and triggering threshold of retinal spreading depression are not correlated. Exp. Brain Res. 2005, 164:185-193.
49. Weimar C., Konig I.R., Kraywinkel K., Ziegler A., Diener H.C. Age and National Institutes of Health Stroke Scale Score within 6 hours after onset are accurate predictors of outcome after cerebral ischemia: development and external validation of prognostic models. Stroke 2004, 35:158-162.
50. Windmuller O., Lindauer U., Foddis M., Einhaupl K.M., Dirnagl U., Heinemann U., Dreier J.P. Ion changes in spreading ischaemia induce rat middle cerebral artery constriction in the absence of NO. Brain 2005, 128(Pt 9):2042-2051.
51. Zandt B.J., ten Haken B., van Putten M.J. Diffusing substances during spreading depolarization: analytical expressions for propagation speed, triggering, and concentration time courses. J.Neurosci. 2013, 33:5915-5923.