Skip to main content
SpringerLink
Log in

Study of Brain Bioenergetics and Function Using In Vivo MRS

  • Chapter
  • First Online:
fMRI: From Nuclear Spins to Brain Functions

Part of the book series: Biological Magnetic Resonance ((BIMR,volume 30))

Abstract

Energy metabolism in the brain relies predominantly on glucose consumption and oxidative metabolism to generate adenosine triphosphate (ATP), which is subsequently utilized to maintain basal electrophysiological activities in the “resting” brain as well as during increased neuronal activity induced by stimulation and/or task performance. Investigating these complex bioenergetic processes in the human brain requires the development of a set of noninvasive neuroimaging techniques capable of providing noninvasive and quantitative measures of the cerebral metabolic rates of glucose and oxygen consumption, and ATP turnover. Multinuclear in vivo magnetic resonance spectroscopy (MRS) and magnetic resonance spectroscopic imaging (MRSI) techniques, especially when performed at ultrahigh magnetic fields (7 T and higher), provide this capability. This chapter provides a brief review of the new developments in these in vivo MRS techniques employed in the quest to understand neuroenergetics.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abragam A (1961) The principles of nuclear magnetism. Oxford University Press, London

    Google Scholar 

  • Ackerman JJH, Grove TH, Wong GG, Gadian DG, Radda GK (1980) Mapping of metabolites in whole animals by 31P NMR using surface coils. Nature 283:167–170

    Article  CAS  PubMed  Google Scholar 

  • Alger JR, Shulman RG (1984) NMR studies of enzymatic rates In Vitro and In Vivo by magnetization transfer. Quart Rev Biophys 17:83–124

    Article  CAS  Google Scholar 

  • Altura BM, Altura BT (1994) Role of magnesium and calcium in alcohol-induced hypertension and strokes as probed by in vivo television microscopy, digital image microscopy, optical spectroscopy, 31P-NMR, spectroscopy and a unique magnesium ion-selective electrode. Alcohol Clin Exp Res 18:1057–1068

    Article  CAS  PubMed  Google Scholar 

  • Arai T, Nakao S, Mori K, Ishimori K, Morishima I, Miyazawa T, Fritz-Zieroth B (1990) Cerebral oxygen utilization analyzed by the use of oxygen-17 and its nuclear magnetic resonance. Biochem Biophys Res Commun 169:153–158

    Article  CAS  PubMed  Google Scholar 

  • Arai T, Mori K, Nakao S, Watanabe K, Kito K, Aoki M, Mori H, Morikawa S, Inubushi T (1991) In vivo oxygen-17 nuclear magnetic resonance for the estimation of cerebral blood flow and oxygen consumption. Biochem Biophys Res Commun 179:954–961

    Article  CAS  PubMed  Google Scholar 

  • Arai T, Nakao S, Morikawa S, Inubushi T, Yokoi T, Shimizu K, Mori K (1998) Measurement of local cerebral blood flow by magnetic resonance imaging: in vivo autoradiographic strategy using 17O-labeled water. Brain Res Bull 45:451–456

    Article  CAS  PubMed  Google Scholar 

  • Atkinson IC, Thulborn KR (2010) Feasibility of mapping the tissue mass corrected bioscale of cerebral metabolic rate of oxygen consumption using 17-oxygen and 23-sodium MR imaging in a human brain at 9.4 T. Neuroimage 51:723–733

    Article  CAS  PubMed  Google Scholar 

  • Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133–1145

    Article  CAS  PubMed  Google Scholar 

  • Balaban RS, Kantor HL, Ferretti JA (1983) In vivo flux between phosphocreatine and adenosine triphosphate determined by two-dimensional phosphorous NMR. J Biol Chem 258:12787–12789

    CAS  PubMed  Google Scholar 

  • Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS (1992) Time course EPI of human brain function during task activation. Magn Reson Med 25:390–397

    Article  CAS  PubMed  Google Scholar 

  • Beal MF (1992) Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann Neurol 31:119–130

    Article  CAS  PubMed  Google Scholar 

  • Beckmann N, Turkalj I, Seelig J, Keller U (1991) 13C NMR for the assessment of human brain glucose metabolism in vivo. Biochemistry 30:6362–6366

    Article  CAS  PubMed  Google Scholar 

  • Bittl JA, DeLayre J, Ingwall JS (1987) Rate equation for creatine kinase predicts the in vivo reaction velocity:31P NMR surface coil studies in brain, heart, and skeletal muscle of the living rat. Biochemistry 26:6083–6090

    Article  CAS  PubMed  Google Scholar 

  • Blackband SJ, Thelwall PE, Chen W (2003) Field dependence of 17O T1, T2 and SNR—in vitro and in vivo studies at 4. 7, 11 and 17.6 Tesla. In: Proceedings of the International Society for Magnetic Resonance in Medicine, Toronto, p 504

    Google Scholar 

  • Blamire AM, Ogawa S, Uğurbil K, Rothman D, McCarthy G, Ellermann JM, Hyder F, Rattner Z, Shulman RG (1992) Dynamic mapping of the human visual cortex by high-speed magnetic resonance imaging. Proc Natl Acad Sci U S A 89:11069–11073

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Boska MD, Hubesch B, Meyerhoff DJ, Twieg DB, Karczmar GS, Matson GB, Weiner MW (1990) Comparison of 31P MRS and 1H MRI at 1.5 and 2.0 T. Magn Reson Med 13:228–238

    Article  CAS  PubMed  Google Scholar 

  • Bottomley PA, Hardy CJ (1992) Mapping creatine kinase reaction rates in human brain and heart with 4 Tesla saturation transfer 31P NMR. J Magn Reson 99:443–448

    CAS  Google Scholar 

  • Braunova Z, Kasparova S, Mlynarik V, Mierisova S, Liptaj T, Tkac I, Gvozdjakova A (2000) Metabolic changes in rat brain after prolonged ethanol consumption measured by 1H and 31P MRS experiments. Cell Mol Neurobiol 20:703–715

    Article  CAS  PubMed  Google Scholar 

  • Brown GG, Levine SR, Gorell JM, Pettegrew JW, Gdowski JW, Bueri JA, Helpern JA, Welch KM (1989) In vivo 31P NMR profiles of Alzheimer’s disease and multiple subcortical infarct dementia. Neurology 39:1423–1427

    Article  CAS  PubMed  Google Scholar 

  • Bruhn J, Lehmann LE, Ropcke H, Bouillon TW, Hoeft A (2001) Shannon entropy applied to the measurement of the electroencephalographic effects of desflurane. Anesthesiology 95:30–35

    Article  CAS  PubMed  Google Scholar 

  • Burt CT, Ribolow H (1994) Glycerol phosphorylcholine (GPC) and serine ethanolamine phosphodiester (SEP):evolutionary mirrored metabolites and their potential metabolic roles. Comp Biochem Physiol Biochem Mol Biol 108:11–20

    Article  CAS  PubMed  Google Scholar 

  • Campbell SL, Jones KA, Shulman RG (1987) 31P NMR saturation-transfer measurements in Saccharomyces cerevisiae:characterization of phosphate exchange reactions by iodoacetate and antimycin A inhibition. Biochemistry 26:7483–7492

    Article  Google Scholar 

  • Chance B, Leigh JS Jr, Nioka S, Sinwell T, Younkin D, Smith DS (1987) An approach to the problem of metabolic heterogeneity in brain:ischemia and reflow after ischemia. Ann N Y Acad Sci 508:309–320

    Article  CAS  PubMed  Google Scholar 

  • Chaumeil MM, Valette J, Guillermier M, Brouillet E, Boumezbeur F, Herard AS, Bloch G, Hantraye P, Lebon V (2009) Multimodal neuroimaging provides a highly consistent picture of energy metabolism, validating 31P MRS for measuring brain ATP synthesis. Proc Natl Acad Sci U S A 106:3988–3993

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen W, Zhu XH (2005) Dynamic study of cerebral bioenergetics and brain function using in vivo multinuclear MRS approaches. Concept Magn Reson A 27A:84–121

    Article  CAS  Google Scholar 

  • Chen W, Novotny E, Zhu XH, Rothman D, Shulman RG (1993) Localized 1H NMR measurement of glucose consumption in human brain during visual stimulation. Proc Natl Acad Sci U S A 90:9896–9900

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen W, Novotny EJ, Boulware SD, Rothman DL, Mason GF, Zhu XH, Blamire AM, Prichard JW, Shulman RG (1994) Quantitative measurements of regional TCA cycle flux in visual cortex of human brain using 1H-{13C} NMR spectroscopy. In: The 2nd annual meeting of SMR, San Francisco, p 63

    Google Scholar 

  • Chen W, Zhu X-H, Adriany G, Uğurbil K (1997) Increase of creatine kinase activity in the visual cortex of human brain during visual stimulation:a 31P NMR magnetization transfer study. Magn Reson Med 38:551–557

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Adriany G, Zhu XH, Gruetter R, Uğurbil K (1998) Detecting natural abundance carbon signal of NAA metabolite within 12 cm3 localized volume of human brain using 1H-{13C} NMR spectroscopy. Magn Reson Med 40:180–184

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Zhu XH, Gruetter R, Seaquist ER, Uğurbil K (2001) Study of oxygen utilization changes of human visual cortex during hemifield stimulation using 1H-{13C} MRS and fMRI. Magn Reson Med 45:349–355

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Zhu XH, Uğurbil K (2004) Imaging cerebral metabolic rate of oxygen consumption (CMRO2) using 17O NMR approach at ultra-high field. In: Shulman RG, Rothman DL (eds) Brain energetics and neuronal activity. Wiley, New York, pp 125–146

    Google Scholar 

  • Choi IY, Lei H, Gruetter R (2002) Effect of deep pentobarbital anesthesia on neurotransmitter metabolism in vivo: on the correlation of total glucose consumption with glutamatergic action. J Cereb Blood Flow Metab 22:1343–1351

    Article  CAS  PubMed  Google Scholar 

  • Clarke DD, Sokoloff L (1999) Circulation and energy metabolism of the brain. In: Siegel GJ et al (eds) Basic neruochemistry: molecular, cellular and medical aspects. Lippincott-Raven, Philadephia, pp 633–669

    Google Scholar 

  • Davis TL, Kwong KK, Weisskoff RM, Rosen BR (1998) Calibrated functional MRI: mapping the dynamic of oxidative metabolism. Proc Natl Acad Sci U S A 95:1834–1839

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Degani H, Laughlin M, Campbell S, Shulman RG (1985) Kinetics of creatine kinase in heart: a 31P NMR saturation- and inversion-transfer study. Biochemistry 24:5510–5516

    Article  CAS  PubMed  Google Scholar 

  • Degani H, Alger JR, Shulman RG, Petroff OA, Prichard JW (1987) 31P magnetization transfer studies of creatine kinase kinetics in living rabbit brain. Magn Reson Med 5:1–12

    Article  CAS  PubMed  Google Scholar 

  • Detre JA, Zhang W, Roberts DA, Silva AC, Williams DS, Grandis DJ, Koretsky AP, Leigh JS (1994) Tissue specific perfusion imaging using arterial spin labeling. NMR in Biomed 7:75–82

    Article  CAS  Google Scholar 

  • Du F, Zhu XH, Qiao H, Zhang X, Chen W (2007) Efficient in vivo 31P magnetization transfer approach for noninvasively determining multiple kinetic parameters and metabolic fluxes of ATP metabolism in the human brain. Magn Reson Med 57:103–114

    Article  CAS  PubMed  Google Scholar 

  • Du F, Zhu XH, Zhang Y, Friedman M, Zhang N, Uğurbil K, Chen W (2008) Tightly coupled brain activity and cerebral ATP metabolic rate. Proc Natl Acad Sci U S A 105:6409–6414

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Du F, Zhang Y, Iltis I, Marjanska M, Zhu XH, Henry PG, Chen W (2009) In vivo proton MRS to quantify anesthetic effects of pentobarbital on cerebral metabolism and brain activity in rat. Magn Reson Med 62:1385–1393

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Du F, Zhang Y, Zhu XH, Chen W (2012) Simultaneous measurement of glucose blood-brain transport constants and metabolic rate in rat brain using in-vivo 1H MRS. J Cereb Blood Flow Metab 32:1778–1787

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Duncan JS (1997) Imaging and epilepsy. Brain 120(Pt 2):339–377

    Article  PubMed  Google Scholar 

  • Fiat D, Kang S (1992) Determination of the rate of cerebral oxygen consumption and regional cerebral blood flow by non-invasive 17O in vivo NMR spectroscopy and magnetic resonance imaging: part 1. Theory and data analysis methods. Neurol Res 14:303–311

    CAS  PubMed  Google Scholar 

  • Fiat D, Kang S (1993) Determination of the rate of cerebral oxygen consumption and regional cerebral blood flow by non-invasive 17O in vivo NMR spectroscopy and magnetic resonance imaging. Part 2. Determination of CMRO2 for the rat by 17O NMR, and CMRO2, rCBF and the partition coefficient for the cat by 17O MRI. Neurol Res 15:7–22

    CAS  PubMed  Google Scholar 

  • Fiat D, Ligeti L, Lyon RC, Ruttner Z, Pekar J, Moonen CT, McLaughlin AC (1992) In vivo 17O NMR study of rat brain during 17O2 inhalation. Magn Reson Med 24:370–374

    Article  CAS  PubMed  Google Scholar 

  • Fiat D, Dolinsek J, Hankiewicz J, Dujovny M, Ausman J (1993) Determination of regional cerebral oxygen consumption in the human: 17O natural abundance cerebral magnetic resonance imaging and spectroscopy in a whole body system. Neurol Res 15:237–248

    CAS  PubMed  Google Scholar 

  • Fox PT, Raichle ME, Mintun MA, Dence C (1988) Nonoxidative glucose consumption during focal physiologic neural activity. Science 241:462–464

    Article  CAS  PubMed  Google Scholar 

  • Frackowiak RS, Herold S, Petty RK, Morgan-Hughes JA (1988) The cerebral metabolism of glucose and oxygen measured with positron tomography in patients with mitochondrial diseases. Brain 111(Pt 5):1009–1024

    Article  PubMed  Google Scholar 

  • From AH, Uğurbil K (2011) Standard magnetic resonance-based measurements of the Pi– > ATP rate do not index the rate of oxidative phosphorylation in cardiac and skeletal muscles. Am J Physiol Cell Physiol 301:C1–11

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frosen S, Hoffman RA (1963) Study of moderately rapid chemical exchange by means of nuclear magnetic double resonance. J Chem Phys 39:2892–2901

    Article  Google Scholar 

  • Gadian DG, Williams SR, Bates TE, Kauppinen RA (1993) NMR spectroscopy: current status and future possibilities. Acta Neurochir Suppl (Wien) 57:1–8

    CAS  Google Scholar 

  • Gruetter R, Novotny EJ, Boulware SD, Rothman DL, Mason GF, Shulman GI, Shulman RG, Tamborlane WV (1992) Direct measurement of brain glucose concentrations in humans by 13C NMR spectroscopy. Proc Natl Acad Sci U S A 89:1109–1112

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gruetter R, Novotny EJ, Boulware SD, Mason GF, Rothman DL, Prichard JW, Shulman RG (1994) Localized 13C NMR spectroscopy of amino acid labeling from {1–13C} D-glucose in the human brain. J Neurochem 63:1377–1385

    Article  CAS  PubMed  Google Scholar 

  • Gruetter R, Garwood M, Uğurbil K, Seaquist ER (1996) Observation of resolved glucose signals in 1H NMR spectra of the human brain at 4 Tesla. Magn Reson Med 36:1–6

    Article  CAS  PubMed  Google Scholar 

  • Gruetter R, Seaquist ER, Kim S, Uğurbil K (1998a) Localized in vivo 13C-NMR of glutamate metabolism in the human brain: initial results at 4 T. Dev Neurosci 20:380–388

    Article  CAS  PubMed  Google Scholar 

  • Gruetter R, Uğurbil K, Seaquist ER (1998b) Steady-state cerebral glucose concentrations and transport in the human brain. J Neurochem 70:397–408

    Article  CAS  PubMed  Google Scholar 

  • Gruetter R, Seaquist ER, Uğurbil K (2001) A mathematical model of compartmentalized neurotransmitter metabolism in the human brain. Am J Physiol Endocrinol Metabol 281:100–112

    Google Scholar 

  • Hardy CJ, Bottomley PA, Roemer PB, Redington RW (1988) Rapid 31P spectroscopy on a 4-T whole-body system. Magn Reson Med 8:104–109

    Article  CAS  PubMed  Google Scholar 

  • Harel N, Lee SP, Nagaoka T, Kim DS, Kim SG (2002) Origin of negative blood oxygenation level-dependent fMRI signals. J Cereb Blood Flow Metab 22:908–917

    Article  PubMed  Google Scholar 

  • Herscovitch A, Raichle ME (1985) What is the correct value for the brain-blood partition coefficient for water? J Cereb Blood Flow Metab 5:65–69

    Article  CAS  PubMed  Google Scholar 

  • Hetherington HP, Spencer DD, Vaughan JT, Pan JW (2001) Quantitative 31P spectroscopic imaging of human brain at 4 Tesla: assessment of gray and white matter differences of phosphocreatine and ATP. Magn Reson Med 45:46–52

    Article  CAS  PubMed  Google Scholar 

  • Hetherington HP, Pan JW, Spencer DD (2002) 1H and 31P spectroscopy and bioenergetics in the lateralization of seizures in temporal lobe epilepsy. J Magn Reson Imaging 16:477–483

    Article  PubMed  Google Scholar 

  • Hinkle PC (2005) P/O ratios of mitochondrial oxidative phosphorylation. Biochim Biophys Acta 1706:1–11

    Article  CAS  PubMed  Google Scholar 

  • Hoge RD, Atkinson J, Gill B, Crelier GR, Marrett S, Pike GB (1999) Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. Proc Natl Acad Sci U S A 96:9403–9408

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hopkins AL, Barr RG (1987) Oxygen-17 compounds as potential NMR T2 contrast agents: enrichment effects of H2 17O on protein solutions and living tissues. Magn Reson Med 4:399–403

    Article  CAS  PubMed  Google Scholar 

  • Hossmann KA (1991) Studies of experimental cerebral ischemia with NMR spectroscopy. Arzneimittelforschung 41:292–298

    CAS  PubMed  Google Scholar 

  • Hyder F, Chase JR, Behar KL, Mason GF, Siddeek M, Rothman DL, Shulman RG (1996) Increase tricarboxylic acid cycle flux in rat brain during forepaw stimulation detected with 1H-{13C} NMR. Proc Natl Acad Sci U S A 93:7612–7617

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hyder F, Rothman DL, Mason GF, Rangarajan A, Behar KL, Shulman RG (1997) Oxidative glucose metabolism in rat brain during single forepaw stimulation: a spatially localized 1H[13C] nuclear magnetic resonance study. J Cereb Bllod Flow Metab 17:1040–1047

    Article  CAS  Google Scholar 

  • Hyder F, Kennan RP, Kida I, Mason GF, Behar KL, Rothman D (2000) Dependence of oxygen delivery on blood flow in rat brain: a 7 T nuclear magnetic resonance study. J Cereb Blood Flow Metab 20:485–498

    Article  CAS  PubMed  Google Scholar 

  • Hyder F, Patel AB, Gjedde A, Rothman DL, Behar KL, Shulman RG (2006) Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J Cereb Blood Flow Metab 26:865–877

    Article  CAS  PubMed  Google Scholar 

  • Iltis I, Marjanska M, Du F, Koski DM, Zhu XH, Uğurbil K, Chen W, Henry PG (2008) 1H MRS in the rat brain under pentobarbital anesthesia: accurate quantification of in vivo spectra in the presence of propylene glycol. Magn Reson Med 59:631–635

    Article  CAS  PubMed  Google Scholar 

  • Jensen JE, Al-Semaan YM, Williamson PC, Neufeld RW, Menon RS, Schaeffer B, Densmore M, Drost DJ (2002) Region-specific changes in phospholipid metabolism in chronic, medicated schizophrenia: 31P-MRS study at 4.0 Tesla. Br J Psychiatry 180:39–44

    Article  PubMed  Google Scholar 

  • Joubert F, Mateo P, Gillet B, Beloeil JC, Mazet JL, Hoerter JA (2004) CK flux or direct ATP transfer: versatility of energy transfer pathways evidenced by NMR in the perfused heart. Mol Cell Biochem 256–257:43–58

    Article  PubMed  Google Scholar 

  • Kemp GJ (2000) Non-invasive methods for studying brain energy metabolism: what they show and what it means. Dev Neurosci 22:418–428

    Article  CAS  PubMed  Google Scholar 

  • Kim S-G (1995) Quantification of relative cerebral blood flow change by flow-sensitive alternating inversion recovery (FAIR) technique: application to functional mapping. Magn Reson Med 34:293–301

    Article  CAS  PubMed  Google Scholar 

  • Kim SG, Uğurbil K (1997) Comparison of blood oxygenation and cerebral blood flow effects in fMRI: estimation of relative oxygen consumption change. Magn Reson Med 38:59–65

    Article  CAS  PubMed  Google Scholar 

  • Kim SG, Rostrup E, Larsson HB, Ogawa S, Paulson OB (1999) Determination of relative CMRO2 from CBF and BOLD changes: significant increase of oxygen consumption rate during visual stimulation. Magn Reson Med 41:1152–1161

    Article  CAS  PubMed  Google Scholar 

  • Kingsley-Hickman PB, Sako EY, Mohanakrishnan P, Robitaille PM, From AH, Foker JE, Uğurbil K (1987) 31P NMR studies of ATP synthesis and hydrolysis kinetics in the intact myocardium. Biochemistry 26:7501–7510

    Article  CAS  PubMed  Google Scholar 

  • Kwong KK, Hopkins AL, Belliveau JW, Chesler DA, Porkka LM, McKinstry RC, Finelli DA, Hunter GJ, Moore JB, Barr RG, Rosen BR (1991) Proton NMR imaging of cerebral blood flow using H2 17O. Magn Reson Med 22:154–158

    Article  CAS  PubMed  Google Scholar 

  • Kwong KK, Belliveau JW, Chesler DA, Goldberg IE, Weisskoff RM, Poncelet BP, Kennedy DN, Hoppel BE, Cohen MS, Turner R, Cheng HM, Brady TJ, Rosen BR (1992) Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci U S A 89:5675–5679

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kwong KK, Chesler DA, Weisskoff RM, Donahue KM, Davis TL, Stergaard L, Campbell TA, Rosen BR (1995) MR perfusion studies with T1-weighted echo planar imaging. Magn Reson Med 34:878–887

    Article  CAS  PubMed  Google Scholar 

  • Lei H, Uğurbil K, Chen W (2003a) Measurement of unidirectional Pi to ATP flux in human visual cortex at 7 Tesla using in vivo 31P magnetic resonance spectroscopy. Proc Natl Acad Sci U S A 100:14409–14414

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lei H, Zhu XH, Zhang XL, Uğurbil K, Chen W (2003b) In vivo 31P magnetic resonance spectroscopy of human brain at 7 T: an initial experience. Magn Reson Med 49:199–205

    Article  CAS  PubMed  Google Scholar 

  • Lenzi GL, Jones T, Frackowiak RS (1981) Positron emission tomography: state of the art in neurology. Prog Nucl Med 7:118–137

    CAS  PubMed  Google Scholar 

  • Lu M, Zhang Y, Uğurbil K, Chen W, Zhu XH (2013) In vitro and in vivo studies of 17O NMR sensitivity at 9.4 and 16.4 T. Magn Reson Med 69:1523–1527

    Article  CAS  PubMed  Google Scholar 

  • Lu M, Chen W, Zhu XH (2014a) Field dependence study of in vivo brain 31P MRS up to 16.4 T. NMR Biomed 27:1135–1141

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lu M, Zhu XH, Zhang Y, Chen W (2014b) Intracellular redox state revealed by in vivo 31P MRS measurement of NAD+ and NADH contents in brains. Magn Reson Med 71:1959–1972

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lund-Andersen H (1979) Tansport of glucose from blood to brain. Physiol Rev 59:305–352

    CAS  PubMed  Google Scholar 

  • Mangia S, Tkac I, Gruetter R, Van De Moortele PF, Giove F, Maraviglia B, Uğurbil K (2006) Sensitivity of single-voxel 1H-MRS in investigating the metabolism of the activated human visual cortex at 7 T. Magnetic Reson Imaging 24:343–348

    Article  Google Scholar 

  • Mangia S, Tkac I, Gruetter R, Van de Moortele PF, Maraviglia B, Uğurbil K (2007) Sustained neuronal activation raises oxidative metabolism to a new steady-state level: evidence from 1H NMR spectroscopy in the human visual cortex. J Cereb Blood Flow Metab 27:1055–1063

    CAS  PubMed  Google Scholar 

  • Mason GF, Gruetter R, Rothman DL, Behar KL, Shulman RG, Novotny EJ (1995) Simultaneous determination of the rates of the TCA cycle, glucose utilization, and a-ketoglutarate/glutamate exchange, and glutamate synthesis in human brain by NMR. J Cereb Blood Flow Metab 15:12–25

    Article  CAS  PubMed  Google Scholar 

  • Mason GF, Pan JW, Chu WJ, Zhang YT, Khazaeli MB, Williams R, Newcomer BD, Orr R, Conger K, Pohost GM, Hetherington HP (1996) TCA cycle rate measurement in human brain by indirect 13C detection with a volume coil. In: 4th scientific meeting of the International Society of Magnetic Resonance in Medicine, New York, p 407

    Google Scholar 

  • Mateescu GD, Yvars G, Pazara DI, Alldridge NA, LaManna JC, Lust DW, Mattingly M, Kuhn W (1989) 17O-1H magnetic resonance imaging in plants, animals, and materials. In: Baillie TA, Jones JR (eds) Synthesis and application of isotopically labeled compounds. Elsevier, Amsterdam, pp 499–508

    Google Scholar 

  • Mateescu GD, LaManna JC, Lust WD, Mars LM, Tseng J (1991) Oxygen-17 magnetic resonance: in vivo detection of nascent mitochondrial water in animals breathing 17O2 enriched air. In: Society of Magnetic Resonance in Medicine, San Francisco, p 1031

    Google Scholar 

  • Matthews PM, Bland JL, Gadian DG, Radda GK (1982) A 31P-NMR saturation transfer study of the regulation of creatine kinase in the rat heart. Biochim Biophys Acta 721:312–320

    Article  CAS  PubMed  Google Scholar 

  • Maurer I, Zierz S, Moller HJ (2000) A selective defect of cytochrome c oxidase is present in brain of Alzheimer disease patients. Neurobiol Aging 21:455–462

    Article  CAS  PubMed  Google Scholar 

  • Maurer I, Zierz S, Moller H (2001) Evidence for a mitochondrial oxidative phosphorylation defect in brains from patients with schizophrenia. Schizophr Res 48:125–136

    Article  CAS  PubMed  Google Scholar 

  • Merboldt KD, Bruhn H, Hanicke W, Michaelis T, Frahm J (1992) Decrease of glucose in the human visual cortex during photic stimulation. Magn Reson Med 25:187–194

    Article  CAS  PubMed  Google Scholar 

  • Mintun MA, Raichle ME, Martin WR, Herscovitch P (1984) Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography. J Nucl Med 25:177–187

    CAS  PubMed  Google Scholar 

  • Mitsumori F, Rees D, Brindle KM, Radda GK, Campbell ID (1988) 31P-NMR saturation transfer studies of aerobic Escherichia coli cells. Biochimica et Biophysica Acta 969:185–193

    Article  CAS  PubMed  Google Scholar 

  • Mlynarik V, Zbyn S, Brehm A, Bischof M, Roden M (2005) An optimized protocol for measuring rate constant of creatine kinase reaction in human brain by 31P NMR saturation transfer. 13th Proceedings of the International Society for Magnetic Resonance in Medicine, Miami, p 2767

    Google Scholar 

  • Mora BN, Narasimhan PT, Ross BD (1992) 31P magnetization transfer studies in the monkey brain. Magn Reson Med 26:100–115

    Article  CAS  PubMed  Google Scholar 

  • Nakao Y, Itoh Y, Kuang TY, Cook M, Jehle J, Sokoloff L (2001) Effects of anesthesia on functional activation of cerebral blood flow and metabolism. Proc Natl Acad Sci U S A 98:7593–7598

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nioka S, Smith DS, Mayevsky A, Dobson GP, Veech RL, Subramanian H, Chance B (1991a) Age dependence of steady state mitochondrial oxidative metabolism in the in vivo hypoxic dog brain. Neurol Res 13:25–32

    CAS  PubMed  Google Scholar 

  • Nioka S, Zaman A, Yoshioka H, Masumura M, Miyake H, Lockard S, Chance B (1991b) 31P magnetic resonance spectroscopy study of cerebral metabolism in developing dog brain and its relationship to neuronal function. Dev Neurosci 13:61–68

    Article  CAS  PubMed  Google Scholar 

  • Novotny EJ, Ogino T, Rothman DL, Petroff OC, Prichard JW, Shulman RG (1990) Direct carbon versus proton heteronuclear editing of 2–13C ethanol in rabbit brain in vivo: a sensitivity comparison. Magn Reson Med 16:431–443

    Article  CAS  PubMed  Google Scholar 

  • Ogawa S, Lee T-M, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A 87:9868–9872

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ogawa S, Tank DW, Menon R, Ellermann JM, Kim S-G, Merkle H, Uğurbil K (1992) Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci U S A 89:5951–5955

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pekar J, Ligeti L, Ruttner Z, Lyon RC, Sinnwell TM, van Gelderen P, Fiat D, Moonen CT, McLaughlin AC (1991) In vivo measurement of cerebral oxygen consumption and blood flow using 17O magnetic resonance imaging. Magn Reson Med 21:313–319

    Article  CAS  PubMed  Google Scholar 

  • Pekar J, Sinnwell T, Ligeti L, Chesnick AS, Frank JA, McLaughlin AC (1995) Simultaneous measurement of cerebral oxygen consumption and blood flow using 17O and 19F magnetic resonance imaging. J Cereb Blood Flow Metab 15:312–320

    Article  CAS  PubMed  Google Scholar 

  • Pettegrew JW, Klunk WE, Panchalingam K, McClure RJ, Stanley JA (1997) Magnetic resonance spectroscopic changes in Alzheimer’s disease. Ann N Y Acad Sci 826:282–306

    Article  CAS  PubMed  Google Scholar 

  • Pfeuffer J, Tkac I, Choi IY, Merkle H, Uğurbil K, Garwood M, Gruetter R (1999) Localized in vivo 1H NMR detection of neurotransmitter labeling in rat brain during infusion of [1–13C] D-glucose. Magn Reson Med 41:1077–1083

    Article  CAS  PubMed  Google Scholar 

  • Provencher SW (2001) Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 14:260–264

    Article  CAS  PubMed  Google Scholar 

  • Qiao H, Zhang X, Zhu XH, Du F, Chen W (2006) In vivo 31P MRS of human brain at high/ultrahigh fields: a quantitative comparison of NMR detection sensitivity and spectral resolution between 4 T and 7 T. Magn Reson Imaging 24:1281–1286

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raichle ME (1987) Circulatory and metabolic correlates of brain function in normal humans. In: Mountcastle VB, Plum F, Geiger SR (eds) Handbook of physiology-the nervous system. American Physiological Society, Bethesda, pp 643–674

    Google Scholar 

  • Raichle ME (2006) Neuroscience. The brain’s dark energy. Science 314:1249–1250

    Article  CAS  PubMed  Google Scholar 

  • Raichle ME, Mintun MA (2006) Brain work and brain imaging. Annu Rev Neurosci 29:449–476

    Article  CAS  PubMed  Google Scholar 

  • Ramadan NM, Halvorson H, Vande-Linde A, Levine SR, Helpern JA, Welch KM (1989) Low brain magnesium in migraine. Headache 29:590–593

    Article  CAS  PubMed  Google Scholar 

  • Reddy R, Stolpen AH, Leigh JS (1995) Detection of 17O by proton T1 rho dispersion imaging. J Magn Reson B 108:276–279

    Article  CAS  PubMed  Google Scholar 

  • Reddy R, Stolpen AH, Charagundla SR, Insko EK, Leigh JS (1996) 17O-decoupled 1H detection using a double-tuned coil. Magn Reson Imaging 14:1073–1078

    Article  CAS  PubMed  Google Scholar 

  • Riehemann S, Volz HP, Smesny S, Hubner G, Wenda B, Rossger G, Sauer H (2000) Phosphorus 31 magnetic resonance spectroscopy in schizophrenia research. Pathophysiology of cerebral metabolism of high-energy phosphate and membrane phospholipids. Nervenarzt 71:354–363

    Article  CAS  PubMed  Google Scholar 

  • Rolfe DF, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758

    CAS  PubMed  Google Scholar 

  • Ronen I, Navon G (1994) A new method for proton detection of H2 17O with potential applications for functional MRI. Magn Reson Med 32:789–793

    Article  CAS  PubMed  Google Scholar 

  • Ronen I, Merkle H, Uğurbil K, Navon G (1998) Imaging of H2 17O distribution in the brain of a live rat by using proton-detected 17O MRI. Proc Natl Acad Sci U S A 95:12934–12939

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ross BM, Moszczynska A, Blusztajn JK, Sherwin A, Lozano A, Kish SJ (1997) Phospholipid biosynthetic enzymes in human brain. Lipids 32:351–358

    Article  CAS  PubMed  Google Scholar 

  • Rothman DL, Novotny EJ, Shulman GI, Howseman AM, Petroff OA, Mason G, Nixon T, Hanstock CC, Prichard JW, Shulman RG (1992) 1H-{13C} NMR measurements of [4–13C] glutamate turnover in human brain. Proc Natl Acad Sci U S A 89:9603–9606

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rothman DL, Sibson NR, Hyder F, Shen J, Behar KL, Shulman RG (1999) In vivo nuclear magnetic resonance spectroscopy studies of the relationship between the glutamate-glutamine neurotransmitter cycle and functional neuroenergetics. Philos Trans R Soc Lond B Biol Sci 354:1165–1177

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saks VA, Ventura-Clapier R, Aliev MK (1996) Metabolic control and metabolic capacity: two aspects of creatine kinase functioning in the cells. Biochim Biophys Acta 1274:81–88

    Article  PubMed  Google Scholar 

  • Sauter A, Rudin M (1993) Determination of creatine kinase parameters in rat brain by NMR magnetization transfer. J Biological Chem 268:13166–13171

    CAS  Google Scholar 

  • Shen J, Petersen KF, Behar KL, Brown P, Nixon TW, Mason GF, Petroff OA, Shulman GI, Shulman RG, Rothman DL (1999) Determination of the rate of the glutamate/glutamine cycle in the human brain by in vivo 13C NMR. Proc Natl Acad Sci U S A 96:8235–8240

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shestov AA, Emir UE, Kumar A, Henry PG, Seaquist ER, Oz G (2011) Simultaneous measurement of glucose transport and utilization in the human brain. Am J Physiol Endocrinol Metabol 301:E1040–E1049

    Article  CAS  Google Scholar 

  • Shestov AA, Valette J, Deelchand DK, Uğurbil K, Henry PG (2012) Metabolic modeling of dynamic brain 13C NMR multiplet data: concepts and simulations with a two-compartment neuronal-glial model. Neurochem Res 37:2388–2401

    Article  CAS  PubMed  Google Scholar 

  • Shmuel A, Yacoub E, Pfeuffer J, Van de Moortele PF, Adriany G, Hu X, Uğurbil K (2002) Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron 36:1195–1210

    Article  CAS  PubMed  Google Scholar 

  • Shmuel A, Augath M, Oeltermann A, Logothetis NK (2006) Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 9:569–577

    Article  CAS  PubMed  Google Scholar 

  • Shoubridge EA, Briggs RW, Radda GK (1982) 31P NMR saturation transfer measurements of the steady state rates of creatine kinase and ATP synthetase in the rat brain. FEBS Lett 140:289–292

    Article  CAS  PubMed  Google Scholar 

  • Shulman RG, Brown TR, Uğurbil K, Ogawa S, Cohen SM, den Hollander JA (1979) Cellular applications of 31P and 13C nuclear magnetic resonance. Science 205:160–166

    Article  CAS  PubMed  Google Scholar 

  • Shulman RG, Rothman DL, Hyder F (1999) Stimulated changes in localized cerebral energy consumption under anesthesia. Proc Natl Acad Sci U S A 96:3245–3250

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shulman RG, Rothman DL, Behar KL, Hyder F (2004) Energetic basis of brain activity: implications for neuroimaging. Trends Neurosci 27:489–495

    Article  CAS  PubMed  Google Scholar 

  • Shulman RG, Rothman DL, Hyder F (2007) A BOLD search for baseline. Neuroimage 36:277–281

    Article  PubMed Central  PubMed  Google Scholar 

  • Sibson NR, Dhankhar A, Mason GF, Behar KL, Rothman DL, Shulman RG (1997) In vivo 13C NMR measurements of cerebral glutamine synthesis as evidence for glutamate-glutamine cycling. Proc Natl Acad Sci U S A 94:2699–2704

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, Shulman RG (1998) Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci U S A 95:316–321

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Siesjo BK (1978) Brain energy metabolism. Wiley, New York, pp 101–110

    Google Scholar 

  • Spencer RG, Balschi JA, Leigh JS Jr, Ingwall JS (1988) ATP synthesis and degradation rates in the perfused rat heart. 31P-nuclear magnetic resonance double saturation transfer measurements. Biophys J 54:921–929

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stolpen AH, Reddy R, Leigh JS (1997) 17O-decoupled proton MR spectroscopy and imaging in a tissue model. J Magn Reson 125:1–7

    Article  CAS  PubMed  Google Scholar 

  • Ter-Pogossian MM, Eichling JO, Davis DO, Welch MJ (1970) The measure in vivo of regional cerebral oxygen utilization by means of oxyhemoglobin labeled with radioactive oxygen-15. J Clin Invest 49:381–391

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thoma WJ, Uğurbil K (1987) Saturation-transfer studies of ATP-Pi exchange in isolated perfused rat liver. Biochimica et Biophysica Acta 893:225–231

    Article  CAS  PubMed  Google Scholar 

  • Uğurbil K (1985a) Magnetization transfer measurements of creatine kinase and ATPase rates in intact hearts. Circulation 72:IV94–IV96

    PubMed  Google Scholar 

  • Uğurbil K (1985b) Magnetization transfer measurements of individual rate constants in the presence of multiple reactions. J Magn Reson 64:207–219

    Google Scholar 

  • Uğurbil K, Brown TR, den Hollander JA, Glynn P, Shulman RG (1978) High resolution 31P and 13C magnetic resonance studies of glucose metabolism in E. coli. Proc Natl Acad Sci U S A 75:3742–3746

    Article  PubMed Central  PubMed  Google Scholar 

  • Uğurbil K, Petein M, Maiden R, Michurski S, From A (1986) Measurement of an individual rate constant in the presence of multiple exchanges: application to myocardial creatine kinase rates. Biochemistry 25:100–108

    Article  PubMed  Google Scholar 

  • Uğurbil K, Adriany G, Andersen P, Chen W, Garwood M, Gruetter R, Henry PG, Kim SG, Lieu H, Tkac I, Vaughan T, Van De Moortele PF, Yacoub E, Zhu XH (2003) Ultrahigh field magnetic resonance imaging and spectroscopy. Magn Reson Imaging 21:1263–1281

    Article  PubMed  Google Scholar 

  • Vlassenko AG, Rundle MM, Mintun MA (2006) Human brain glucose metabolism may evolve during activation: findings from a modified FDG PET paradigm. Neuroimage 33:1036–1041

    Article  PubMed  Google Scholar 

  • Wallace DC (1992) Mitochondrial genetics: a paradigm for aging and degenerative diseases? Science 256:628–632

    Article  CAS  PubMed  Google Scholar 

  • Wallace DC (1999) Mitochondrial diseases in man and mouse. Science 283:1482–1488

    Article  CAS  PubMed  Google Scholar 

  • Wallimann T, Hemmer W (1994) Creatine kinase in non-muscle tissues and cells. Mol Cell Biochem 133–134:193–220

    Article  PubMed  Google Scholar 

  • Weiner MW (1987) NMR spectroscopy for clinical medicine. Animal models and clinical examples. Ann N Y Acad Sci 508:287–299

    Article  CAS  PubMed  Google Scholar 

  • Weiss RG, Gerstenblith G, Bottomley PA (2005) ATP flux through creatine kinase in the normal, stressed, and failing human heart. Proc Natl Acad Sci U S A 102:808–813

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Welch KM, Levine SR, Martin G, Ordidge R, Vande Linde AM, Helpern JA (1992) Magnetic resonance spectroscopy in cerebral ischemia. Neurol Clin 10:1–29

    CAS  PubMed  Google Scholar 

  • Wong-Riley M, Antuono P, Ho KC, Egan R, Hevner R, Liebl W, Huang Z, Rachel R, Jones J (1997) Cytochrome oxidase in Alzheimer’s disease: biochemical, histochemical, and immunohistochemical analyses of the visual and other systems. Vision Res 37:3593–3608

    Article  CAS  PubMed  Google Scholar 

  • Xiong Q, Du F, Zhu XH, Zhang P, Suntharalingam P, Ippolito J, Kamdar FD, Chen W, Zhang J (2011) ATP production rate via creatine kinase or ATP synthase in vivo: a novel superfast magnetization saturation transfer method. Circ Res 108:653–663

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yee SH, Lee K, Jerabek PA, Fox PT (2006) Quantitative measurement of oxygen metabolic rate in the rat brain using microPET imaging of briefly inhaled 15O-labelled oxygen gas. Nucl Med Commun 27:573–581

    Article  CAS  PubMed  Google Scholar 

  • Young RS, Chen B, Petroff OA, Gore JC, Cowan BE, Novotny EJ Jr, Wong M, Zuckerman K (1989) The effect of diazepam on neonatal seizure: in vivo 31P and 1H NMR study. Pediatr Res 25:27–31

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Zhu XH, Tian R, Zhang Y, Merkle H, Chen W (2003) Measurement of arterial input function of 17O water tracer in rat carotid artery by using a region-defined (REDE) implanted vascular RF coil. Magma 16:77–85

    Article  PubMed  Google Scholar 

  • Zhang N, Zhu XH, Lei H, Uğurbil K, Chen W (2004) Simplified methods for calculating cerebral metabolic rate of oxygen based on 17O magnetic resonance spectroscopic imaging measurement during a short 17O2 inhalation. J Cereb Blood Flow Metab 24:840–848

    Article  CAS  PubMed  Google Scholar 

  • Zhu XH, Chen W (2011) In vivo oxygen-17 NMR for imaging brain oxygen metabolism at high field. Prog Nucl Magn Reson Spectrosc 59:319–335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu XH, Kim SG, Andersen P, Ogawa S, Uğurbil K, Chen W (1998) Simultaneous oxygenation and perfusion imaging study of functional activity in primary visual cortex at different visual stimulus frequency: quantitative correlation between dynamic BOLD and CBF changes. Magn Reson Med 40:703–711

    Article  CAS  PubMed  Google Scholar 

  • Zhu XH, Merkle H, Kwag JH, Uğurbil K, Chen W (2001) 17O relaxation time and NMR sensitivity of cerebral water and their field dependence. Magn Reson Med 45:543–549

    Article  CAS  PubMed  Google Scholar 

  • Zhu XH, Lei H, Zhang Y, Zhang XL, Zhang N, Uğurbil K, Chen W (2002a) Evidence of limited permeation of metabolic water in rat brain observed by 17O magnetic resonance spectroscopic imaging and its implications. In: Proceedings of the International Society for Magnetic Resonance in Medicine, Hawaii, p 1094

    Google Scholar 

  • Zhu XH, Zhang Y, Tian RX, Lei H, Zhang N, Zhang X, Merkle H, Uğurbil K, Chen W (2002b) Development of 17O NMR approach for fast imaging of cerebral metabolic rate of oxygen in rat brain at high field. Proc Natl Acad Sci U S A 99:13194–13199

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu XH, Zhang XL, Chen W (2003) Study of 17O NMR sensitivity and relaxation times of cerebral water in human at 7 Tesla. In: Proceedings of the International Society for Magnetic Resonance in Medicine, Toronto, p 868

    Google Scholar 

  • Zhu XH, Zhang N, Zhang Y, Zhang X, Uğurbil K, Chen W (2005) In vivo 17O NMR approaches for brain study at high field. NMR Biomed 18:83–103

    Article  CAS  PubMed  Google Scholar 

  • Zhu XH, Zhang Y, Zhang N, Uğurbil K, Chen W (2007) Noninvasive and three-dimensional imaging of CMRO2 in rats at 9.4 T: reproducibility test and normothermia/hypothermia comparison study. J Cereb Blood Flow Metab 27:1225–1234

    Article  PubMed  Google Scholar 

  • Zhu XH, Zhang Y, Chen W (2008) Functional mapping of CK and ATPase metabolic rate changes elevated by visual stimulation in cat brain. In: Proceedings of the International Society for Magnetic Resonance in Medicine, Toronto, p 408

    Google Scholar 

  • Zhu XH, Zhang N, Zhang Y, Uğurbil K, Chen W (2009) New insights into central roles of cerebral oxygen metabolism in the resting and stimulus-evoked brain. J Cereb Blood Flow Metab 29:10–18

    Article  CAS  PubMed  Google Scholar 

  • Zhu XH, Qiao H, Du F, Xiong Q, Liu X, Zhang X, Uğurbil K, Chen W (2012) Quantitative imaging of energy expenditure in human brain. Neuroimage 60:2107–2117

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhu XH, Chen JM, Tu TW, Chen W, Song SK (2013) Simultaneous and noninvasive imaging of cerebral oxygen metabolic rate, blood flow and oxygen extraction fraction in stroke mice. Neuroimage 64:437–447

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Drs. Peter Andersen, Gregor Adriany, Robert Shulman, Douglas Rothman, Seiji Ogawa, Keith Thulborn, Hellmut Merkle, and Mr. John Strupp for their support, technical assistance, and insightful discussion. The part of the reviewed work in this chapter was supported by the National Institutes of Health (NIH) grants of NS041262, NS057560, NS070839, P30 NS057091/P30 NS076408, and P41 RR08079 (NCRR)/P41 EB015894 (NIBIB); and the W. M. Keck Foundation.

Author information

Authors and Affiliations

  1. Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, School of Medicine, 2021 6th St. SE, 55455, Minneapolis, MN, USA

    Xiao-Hong Zhu, Min Lu, Yi Zhang, Kâmil Uğurbil & Wei Chen PhD

  2. McLean Hospital, Department of Psychiatry, Harvard Medical School, Belmont, MA, USA

    Fei Du

  3. Department of Bioengineering, Center for Neural Engineering, The Pennsylvania State University, University Park, PA, USA

    Nanyin Zhang

  4. Laboratory of Functional and Molecular Imaging, NINDS, National Institute of Health, Bethesda, MD, USA

    Xiao Liu

  5. Wuhan Institute of Physics and Mathematics, Chinese Academy of Sciences, Wuhan, China

    Hao Lei

  6. Department of Radiology, University of California San Francisco, San Francisco, CA, USA

    Xiaoliang Zhang

Authors
  1. Xiao-Hong Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fei Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nanyin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Min Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hao Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiaoliang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kâmil Uğurbil
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Wei Chen PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wei Chen PhD .

Editor information

Editors and Affiliations

  1. Maastricht Brain Imaging Centre, Maastricht University, Maastricht, The Netherlands

    Kamil Uludag

  2. University of Minnesota Medical School, Minneapolis, Minnesota, USA

    Kamil Ugurbil

  3. Department of Chemistry and Biochemistry, University of Denver, Denver, Colorado, USA

    Lawrence Berliner

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer New York

About this chapter

Cite this chapter

Zhu, XH. et al. (2015). Study of Brain Bioenergetics and Function Using In Vivo MRS. In: Uludag, K., Ugurbil, K., Berliner, L. (eds) fMRI: From Nuclear Spins to Brain Functions. Biological Magnetic Resonance, vol 30. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-7591-1_28

Download citation

Publish with us

Policies and ethics

Search

Navigation