Cortical spreading depression impairs oxygen delivery and metabolism in mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 2, 2012, Pages 376-386

  Yuzawa, Izumi ^a   Sakadžić, Sava ^a   Srinivasan, Vivek J ^a   Shin, Hwa Kyoung ^a   Eikermann Haerter, Katharina ^a   Boas, David A ^a   Ayata, Cenk ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

cerebral metabolic rate of oxygen; laser speckle flowmetry; mouse; multispectral reflectance imaging; spreading depression

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE;

ANIMAL EXPERIMENT; ARTICLE; BLOOD VOLUME; CEREBRAL METABOLIC RATE OF OXYGEN; FEMALE; FLUORESCENCE; MALE; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; OXYGEN SUPPLY; PRIORITY JOURNAL; SPREADING CORTICAL DEPRESSION; VASOCONSTRICTION;

ANIMALS; BLOOD VOLUME; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; CORTICAL SPREADING DEPRESSION; FEMALE; HEMODYNAMICS; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; NAD; OXYGEN;

EID: 84856450961     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2011.148     Document Type: Article

References (42)

1. Ayata C (2010) Cortical spreading depression triggers migraine attack: pro. Headache 50:725-30
2. Ayata C, Dunn AK, Gursoy OY, Huang Z, Boas DA,Moskowitz MA (2004a) Laser speckle flowmetry for the study of cerebrovascular physiology in normal and ischemic mouse cortex. J Cereb Blood Flow Metab 24:744-55 (Pubitemid 38880219)
3. Ayata C, Shin HK, Salomone S, Ozdemir-Gursoy Y, Boas DA, Dunn AK, Moskowitz MA (2004b) Pronounced hypoperfusion during spreading depression in mouse cortex. J Cereb Blood Flow Metab 24:1172-82 (Pubitemid 39332157)
4. Brennan KC, Beltran-Parrazal L, Lopez-Valdes HE, Theriot J, Toga AW, Charles AC (2007) Distinct vascular conduction with cortical spreading depression. J Neurophysiol 97:4143-51 (Pubitemid 47080646)
5. Chang JC, Shook LL, Biag J, Nguyen EN, Toga AW, Charles AC, Brennan KC (2010) Biphasic direct current shift, haemoglobin desaturation and neurovascular uncoupling in cortical spreading depression. Brain 133:996-1012
6. Chia TH, Williamson A, Spencer DD, Levene MJ (2008) Multiphoton fluorescence lifetime imaging of intrinsic fluorescence in human and rat brain tissue reveals spatially distinct NADH binding. Opt Express 16:4237-49 (Pubitemid 351434392)
7. Dohmen C, Sakowitz OW, Fabricius M, Bosche B, Reithmeier T, Ernestus RI, Brinker G, Dreier JP, Woitzik J, Strong AJ, Graf R (2008) Spreading depolarizations occur in human ischemic stroke with high incidence. Ann Neurol 63:720-8 (Pubitemid 351945531)
8. Dora E, Gyulai L, Kovach AG (1984) Determinants of brain activation-induced cortical NAD/NADH responses in vivo. Brain Res 299:61-72 (Pubitemid 14143639)
9. Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, Lehmann TN, Sarrafzadeh A, Willumsen L, Hartings JA, Sakowitz OW, Seemann JH, Thieme A, Lauritzen M, Strong AJ (2006) Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 129:3224-37 (Pubitemid 44871438)
10. Dunn AK, Devor A, Bolay H, Andermann ML, Moskowitz MA, Dale AM, Boas DA (2003) Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation. Opt Lett 28:28-30
11. Dunn AK, Devor A, Dale AM, Boas DA (2005) Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex. Neuroimage 27:279-90 (Pubitemid 41074831)
12. Eikermann-Haerter K, Yuzawa I, Qin T, Wang Y, Baek K, Kim YR, Hoffmann U, Dilekoz E, Waeber C, Ferrari MD, van den Maagdenberg AM, Moskowitz MA, Ayata C (2011) Enhanced subcortical spreading depression in familial hemiplegic migraine type 1 mutant mice. J Neurosci 31:5755-63
13. Galeffi F, Somjen GG, Foster KA, Turner DA (2011) Simultaneous monitoring of tissue PO(2) and NADH fluorescence during synaptic stimulation and spreading depression reveals a transient dissociation between oxygen utilization and mitochondrial redox state in rat hippocampal slices. J Cereb Blood Flow Metab 31:626-39
14. Gjedde A, Johannsen P, Cold GE, Ostergaard L (2005) Cerebral metabolic response to low blood flow: possible role of cytochrome oxidase inhibition. J Cereb Blood Flow Metab 25:1183-96 (Pubitemid 41710743)
15. Haselgrove JC, Bashford CL, Barlow CH, Quistorff B, Chance B, Mayevsky A (1990) Time resolved 3-dimensional recording of redox ratio during spreading depression in gerbil brain. Brain Res 506:109-14 (Pubitemid 20020081)
16. Hashemi P, Bhatia R, Nakamura H, Dreier JP, Graf R, Strong AJ, Boutelle MG (2009) Persisting depletion of brain glucose following cortical spreading depression, despite apparent hyperaemia: evidence for risk of an adverse effect of Leao's spreading depression. J Cereb Blood Flow Metab 29:166-75
17. Jones PB, Shin HK, Boas DA, Hyman BT, Moskowitz MA, Ayata C, Dunn AK (2008) Simultaneous multispectral reflectance imaging and laser speckle flowmetry of cerebral blood flow and oxygen metabolism in focal cerebral ischemia. J Biomed Opt 13:044007
18. Kasischke KA, Lambert EM, Panepento B, Sun A, Gelbard HA, Burgess RW, Foster TH, Nedergaard M (2010) Twophoton NADH imaging exposes boundaries of oxygen diffusion in cortical vascular supply regions. J Cereb Blood Flow Metab 31:68-81
19. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305:99-103 (Pubitemid 38869381)
20. Leao AAP (1944) Spreading depression of activity in cerebral cortex. J Neurophysiol 7:359-90
21. Lothman E, Lamanna J, Cordingley G, Rosenthal M, Somjen G (1975) Responses of electrical potential, potassium levels, and oxidative metabolic activity of the cerebral neocortex of cats. Brain Res 88:15-36
22. Lukyanova LD, Bures J (1967) Changes in pO2 due to spreading depression in the cortex and nucleus caudatus of the rat. Physiol Bohemoslov 16:449-55
23. Marshall WH (1959) Spreading cortical depression of Leao. Physiol Rev 39:239-79
24. Mayevsky A, Sclarksy DL (1983) Correlation of brain NADH redox state, K+, PO2 and electrical activity during hypoxia, ischemia and spreading depression. Adv Exp Med Biol 159:129-41
25. Mayevsky A, Zarchin N, Friedli CM (1982) Factors affecting the oxygen balance in the awake cerebral cortex exposed to spreading depression. Brain Res 236:93-105 (Pubitemid 12184982)
26. Mayevsky A, Zeuthen T, Chance B (1974) Measurements of extracellular potassium, ECoG and pyridine nucleotide levels during cortical spreading depression in rats. Brain Res 76:347-9
27. Piilgaard H, Lauritzen M (2009) Persistent increase in oxygen consumption and impaired neurovascular coupling after spreading depression in rat neocortex. J Cereb Blood Flow Metab 29:1517-27
28. Rex A, Pfeifer L, Fink F, Fink H (1999) Cortical NADH during pharmacological manipulations of the respiratory chain and spreading depression in vivo. J Neurosci Res 57:359-70 (Pubitemid 29339792)
29. Rosenthal M, Somjen G (1973) Spreading depression, sustained potential shifts, and metabolic activity of cerebral cortex of cats. J Neurophysiol 36:739-49
30. Sakadzic S, Roussakis E, Yaseen MA, Mandeville ET, Srinivasan VJ, Arai K, Ruvinskaya S, Devor A, Lo EH, Vinogradov SA, Boas DA (2010) Two-photon highresolution measurement of partial pressure of oxygen in cerebral vasculature and tissue. Nat Methods 7: 755-9
31. Sakadzic S, Yuan S, Dilekoz E, Ruvinskaya S, Vinogradov SA, Ayata C, Boas DA (2009) Simultaneous imaging of cerebral partial pressure of oxygen and blood flow during functional activation and cortical spreading depression. Appl Opt 48:D169-77
32. Schechter M, Sonn J, Mayevsky A (2009) Brain oxygen balance under various experimental pathophysiologycal conditions. Adv Exp Med Biol 645:293-9
33. Shuttleworth CW (2009) Use of NAD(P)H and flavoprotein autofluorescence transients to probe neuron and astrocyte responses to synaptic activation. Neurochem Int 56:379-86
34. Somjen GG (2001) Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81:1065-96 (Pubitemid 32606666)
35. Strong AJ, Harland SP, Meldrum BS, Whittington DJ (1996) The use of in vivo fluorescence image sequences to indicate the occurrence and propagation of transient focal depolarizations in cerebral ischemia. J Cereb Blood Flow Metab 16:367-77 (Pubitemid 26125325)
36. Strong AJ, Hartings JA, Dreier JP (2007) Cortical spreading depression: an adverse but treatable factor in intensive care? Curr Opin Crit Care 13:126-33 (Pubitemid 46328325)
37. Strong AJ, Smith SE, Whittington DJ, Meldrum BS, Parsons AA, Krupinski J, Hunter AJ, Patel S, Robertson C (2000) Factors influencing the frequency of fluorescence transients as markers of peri-infarct depolarizations in focal cerebral ischemia. Stroke 31:214-22 (Pubitemid 30035777)
38. Takano T, Tian GF, Peng W, Lou N, Lovatt D, Hansen AJ, Kasischke KA, Nedergaard M (2007) Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 10:754-62 (Pubitemid 46828508)
39. Theer P, DenkW(2006) On the fundamental imaging-depth limit in two-photon microscopy. J Opt Soc Am A Opt Image Sci Vis 23:3139-49 (Pubitemid 46023808)
40. Van Harreveld A, Stamm JS (1952) Vascular concomitants of spreading cortical depression. J Neurophysiol 15:487-96
41. Yaseen MA, Srinivasan VJ, Sakadzic S, Radhakrishnan H, Gorczynska I, Wu W, Fujimoto JG, Boas DA (2011) Microvascular oxygen tension and flow measurements in rodent cerebral cortex during baseline conditions and functional activation. J Cereb Blood Flow Metab 31:1051-63
42. Zhou N, Gordon GR, Feighan D, MacVicar BA (2010) Transient swelling, acidification, and mitochondrial depolarization occurs in neurons but not astrocytes during spreading depression. Cereb Cortex 20:2614-24