Dynamic correlations between hemodynamic, metabolic, and neuronal responses to acute whole-brain ischemia

NMR in Biomedicine

Volumn 28, Issue 11, 2015, Pages 1357-1365

  Taylor, Jennifer M ^a,b   Zhu, Xiao Hong ^a   Zhang, Yi ^a   Chen, Wei ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b University of Minnesota   (United States)

Author keywords

Brain hemodynamics; Brain ischemia; Brain metabolism; Electrophysiology; MRS; Simultaneous acquisition

Indexed keywords

ADENOSINETRIPHOSPHATE; BLOOD VESSELS; ELECTROPHYSIOLOGY; HEMODYNAMICS; METABOLISM; NEURONS; PHOSPHATES; PHYSIOLOGY;

BRAIN ISCHEMIA; BRAIN METABOLISM; DYNAMIC CORRELATION; HEMODYNAMIC CHANGES; HIGH TEMPORAL RESOLUTION; MRS; NEURONAL ACTIVITIES; SIMULTANEOUS ACQUISITION;

BRAIN;

ADENOSINE TRIPHOSPHATE; CREATINE PHOSPHATE; GLUCOSE; GLYCOGEN; LACTIC ACID; PHOSPHORUS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BOLD SIGNAL; BRAIN BLOOD FLOW; BRAIN BLOOD VOLUME; BRAIN DEATH; BRAIN ELECTROPHYSIOLOGY; BRAIN ISCHEMIA; BRAIN LEVEL; BRAIN METABOLISM; BRAIN MITOCHONDRION; BRAIN OXYGEN CONSUMPTION; BRAIN PERFUSION; CELL PH; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTRIC POTENTIAL; ENERGY CONVERSION; GLUCOSE BLOOD LEVEL; GLYCOLYSIS; HEMODYNAMICS; IN VIVO STUDY; MALE; NERVE CELL; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROMETER; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OCCLUSIVE CEREBROVASCULAR DISEASE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; RAT; REPERFUSION; SIGNAL NOISE RATIO; STEADY STATE; ACUTE DISEASE; ANIMAL; BLOOD FLOW VELOCITY; BRAIN; BRAIN CIRCULATION; ELECTROENCEPHALOGRAPHY; METABOLIC CLEARANCE RATE; METABOLISM; OXYGEN CONSUMPTION; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; PROTON NUCLEAR MAGNETIC RESONANCE; SPRAGUE DAWLEY RAT; STATISTICS;

ACUTE DISEASE; ADENOSINE TRIPHOSPHATE; ANIMALS; BLOOD FLOW VELOCITY; BRAIN; BRAIN ISCHEMIA; CEREBROVASCULAR CIRCULATION; ELECTROENCEPHALOGRAPHY; MALE; METABOLIC CLEARANCE RATE; NEURONS; OXYGEN CONSUMPTION; PHOSPHORUS ISOTOPES; PROTON MAGNETIC RESONANCE SPECTROSCOPY; RATS; RATS, SPRAGUE-DAWLEY; STATISTICS AS TOPIC;

EID: 84945465083     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.3408     Document Type: Article

References (40)

1. 1H magnetic resonance spectroscopy of cerebral ischemia in rats. Biochem. Cell Biol. 1998; 76(2-3): 487-496.
2. Howe FA, Maxwell RJ, Saunders DE, Brown MM, Griffiths JR. Proton spectroscopy in vivo. Magn. Reson. Q. 1993; 9(1): 31-59.
3. 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review. Magn. Reson. Q. 1994; 10(1): 43-63.
4. 31P NMR using surface coils. Nature 1980; 283(5743): 167-170.
5. 31P NMR magnetization transfer study. Magn. Reson. Med. 1997; 38(4): 551-557.
6. Du F, Zhu XH, Zhang Y, Friedman M, Zhang N, Ugurbil K, Chen W. Tightly coupled brain activity and cerebral ATP metabolic rate. Proc. Natl. Acad. Sci. U. S. A. 2008; 105(17): 6409-6414.
7. Pulsinelli WA, Brierley JB. A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 1979; 10(3): 267-272.
8. Sugio K, Horigome N, Sakaguchi T, Goto M. A model of bilateral hemispheric ischemia-modified four-vessel occlusion in rats. Stroke 1988; 19(7): 922.
9. Nagatomo Y, Wick M, Prielmeier F, Frahm J. Dynamic monitoring of cerebral metabolites during and after transient global ischemia in rats by quantitative proton NMR spectroscopy in vivo. NMR Biomed. 1995; 8(6): 265-270.
10. Bainbridge A, Tachtsidis I, Faulkner SD, Price D, Zhu T, Baer E, Broad KD, Thomas DL, Cady EB, Robertson NJ, Golay X. Brain mitochondrial oxidative metabolism during and after cerebral hypoxia-ischemia studied by simultaneous phosphorus magnetic-resonance and broadband near-infrared spectroscopy. Neuroimage 2014; 102(Pt1): 173-183.
11. 1H magnetic resonance spectroscopy. Stroke 1988; 19(5): 608-614.
12. 31P saturation transfer. J. Pharmacol. Exp. Ther. 1989; 251(2): 700-706.
13. Schmidt-Kastner R, Paschen W, Ophoff BG, Hossmann KA. A modified four-vessel occlusion model for inducing incomplete forebrain ischemia in rats. Stroke 1989; 20(7): 938-946.
14. Lowry OH, Passonneau JV, Hasselberger FX, Schulz DW. Effect of ischemia on known substrates and cofactors of the glycolytic pathway in brain. J. Biol. Chem. 1964; 239: 18-30.
15. Ljunggren B, Norberg K, Siesjo BK. Influence of tissue acidosis upon restitution of brain energy metabolism following total ischemia. Brain Res. 1974; 77(2): 173-186.
16. 1H-nuclear magnetic resonance studies of hypoxia and ischemia in the cat brain. J. Cereb. Blood Flow Metab. 1987; 7(5): 543-551.
17. 31P nmr spectroscopy. Magn. Reson. Med. 1990; 13(1): 6-13.
18. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001; 412(6843): 150-157.
19. Scholvinck ML, Maier A, Ye FQ, Duyn JH, Leopold DA. Neural basis of global resting-state fMRI activity. Proc. Natl. Acad. Sci. U. S. A. 2010; 107(22): 10 238-10 243.
20. Tomida S, Nowak TS, Jr, Vass K, Lohr JM, Klatzo I. Experimental model for repetitive ischemic attacks in the gerbil: the cumulative effect of repeated ischemic insults. J. Cereb. Blood Flow Metab. 1987; 7(6): 773-782.
21. 31P nuclear magnetic resonance spectroscopy. Magn. Reson. Med. 1988; 7(4): 412-424.
22. Price TB, Perseghin G, Duleba A, Chen W, Chase J, Rothman DL, Shulman RG, Shulman GI. NMR studies of muscle glycogen synthesis in insulin-resistant offspring of parents with non-insulin-dependent diabetes mellitus immediately after glycogen-depleting exercise. Proc. Natl. Acad. Sci. U. S. A. 1996; 93(11): 5329-5334.
23. Meyerspeer M, Kemp GJ, Mlynarik V, Krssak M, Szendroedi J, Nowotny P, Roden M, Moser E. Direct noninvasive quantification of lactate and high energy phosphates simultaneously in exercising human skeletal muscle by localized magnetic resonance spectroscopy. Magn. Reson. Med. 2007; 57(4): 654-660.
24. Bottomley PA. Spatial localization in NMR spectroscopy in vivo. Ann. NY Acad. Sci. 1987; 508(1 Physiological): 333-348.
25. 1H NMR spectroscopy of rat brain at 1ms echo time. Magn. Reson. Med. 1999; 41(4): 649-656.
26. Gruetter R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn. Reson. Med. 1993; 29(6): 804-811.
27. 1H NMR spectra of the rat brain. J. Magn. Reson. 1999; 141(1): 104-120.
28. 1H MRS study at 4T. Magn. Reson. Med. 2001; 46(5): 841-847.
29. 1H-MRS in investigating the metabolism of the activated human visual cortex at 7T. Magn. Reson. Imaging 2006; 24(4): 343-348.
30. Demanuele C, James CJ, Sonuga-Barke EJ. Distinguishing low frequency oscillations within the 1/f spectral behaviour of electromagnetic brain signals. Behav. Brain Funct. 2007; 3: 62.
31. Liu X, Zhu X-H, Zhang Y, Chen W. Neural origin of spontaneous hemodynamic fluctuations in rats under burst-suppression anesthesia condition. Cereb. Cortex 2011; 21(2): 374-384.
32. Du F, Zhang Y, Iltis I, Marjanska M, Zhu X-H, Henry P-G, Chen W. In vivo proton MRS to quantify anesthetic effects of pentobarbital on cerebral metabolism and brain activity in rat. Magn. Reson. Med. 2009; 62(6): 1385-1393.
33. Morgenthaler FD, Koski DM, Kraftsik R, Henry P-G, Gruetter R. Biochemical quantification of total brain glycogen concentration in rats under different glycemic states. Neurochem. Int. 2006; 48(6-7): 616-622.
34. Duverger D, MacKenzie ET. The quantification of cerebral infarction following focal ischemia in the rat: influence of strain, arterial pressure, blood glucose concentration, and age. J. Cereb. Blood Flow Metab. 1988; 8(4): 449-461.
35. Hoxworth JM, Xu K, Zhou Y, Lust WD, LaManna JC. Cerebral metabolic profile, selective neuron loss, and survival of acute and chronic hyperglycemic rats following cardiac arrest and resuscitation. Brain Res. 1999; 821(2): 467-479.
36. Fleidervish IA, Gebhardt C, Astman N, Gutnick MJ, Heinemann U. Enhanced spontaneous transmitter release is the earliest consequence of neocortical hypoxia that can explain the disruption of normal circuit function. J. Neurosci. 2001; 21(13): 4600-4608.
37. Raffin CN, Harrison M, Sick TJ, Rosenthal M. EEG suppression and anoxic depolarization: influences on cerebral oxygenation during ischemia. J. Cereb. Blood Flow Metab. 1991; 11(3): 407-415.
38. Pulsinelli WA, Brierley JB, Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 1982; 11(5): 491-498.
39. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 2001; 21(10): 1133-1145.
40. Howarth C, Gleeson P, Attwell D. Updated energy budgets for neural computation in the neocortex and cerebellum. J. Cereb. Blood Flow Metab. 2012; 32(7): 1222-1232.