Skip to main content

Advertisement

SpringerLink
Log in

In vivo Magnetic Resonance Spectroscopy of cerebral glycogen metabolism in animals and humans

  • Review Article
  • Published:
Metabolic Brain Disease Aims and scope Submit manuscript

Abstract

Glycogen serves as an important energy reservoir in the human body. Despite the abundance of glycogen in the liver and skeletal muscles, its concentration in the brain is relatively low, hence its significance has been questioned. A major challenge in studying brain glycogen metabolism has been the lack of availability of non-invasive techniques for quantification of brain glycogen in vivo. Invasive methods for brain glycogen quantification such as post mortem extraction following high energy microwave irradiation are not applicable in the human brain. With the advent of 13C Magnetic Resonance Spectroscopy (MRS), it has been possible to measure brain glycogen concentrations and turnover in physiological conditions, as well as under the influence of stressors such as hypoglycemia and visual stimulation. This review presents an overview of the principles of the 13C MRS methodology and its applications in both animals and humans to further our understanding of glycogen metabolism under normal physiological and pathophysiological conditions such as hypoglycemia unawareness.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Alquier T, Kawashima J, Tsuji Y, Kahn BB (2007) Role of hypothalamic adenosine 5′-monophosphate-activated protein kinase in the impaired counterregulatory response induced by repetitive neuroglucopenia. Endocrinology 148(3):1367–1375

    Article  CAS  PubMed  Google Scholar 

  • Belanger M, Allaman I, Magistretti PJ (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 14(6):724–738

    Article  CAS  PubMed  Google Scholar 

  • Benarroch EE (2010) Glycogen metabolism: metabolic coupling between astrocytes and neurons. Neurology 74(11):919–923

    Article  CAS  PubMed  Google Scholar 

  • Benington JH, Heller HC (1995) Restoration of brain energy metabolism as the function of sleep. Prog Neurobiol 45(4):347–360

    Article  CAS  PubMed  Google Scholar 

  • Bergström J, Hermansen L, Hultman E, Saltin B (1967) Diet, muscle glycogen and physical performance. Acta Physiol Scand 71(2):140–150

    Article  PubMed  Google Scholar 

  • Brown AM (2004) Brain glycogen re-awakened. J Neurochem 89(3):537–552

    Article  CAS  PubMed  Google Scholar 

  • Brown AM, Ransom BR (2007) Astrocyte glycogen and brain energy metabolism. Glia 55(12):1263–1271

    Article  PubMed  Google Scholar 

  • Brown AM, Baltan Tekkök S, Ransom BR (2004) Energy transfer from astrocytes to axons: the role of CNS glycogen. Neurochem Int 45(4):529–536

    Article  CAS  PubMed  Google Scholar 

  • Brucklacher RM, Vannucci RC, Vannucci SJ (2002) Hypoxic preconditioning increases brain glycogen and delays energy depletion from hypoxia-ischemia in the immature rat. Dev Neurosci 24(5):411–417

    Article  CAS  PubMed  Google Scholar 

  • Canada SE, Weaver SA, Sharpe SN, Pederson BA (2011) Brain glycogen supercompensation in the mouse after recovery from insulin-induced hypoglycemia. J Neurosci Res 89(4):585–591

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cao J, Feng XX, Yao L, Ning B, Yang ZX, Fang DL, Shen W (2013) Saturated free fatty acid sodium Palmitate-Induced lipoapoptosis by targeting glycogen synthase kinase-3beta activation in human liver cells. Dig Dis Sci 59(2):346–357

    Article  PubMed  Google Scholar 

  • Castejon OJ, Diaz M, Castejon HV, Castellano A (2002) Glycogen-rich and glycogen-depleted astrocytes in the oedematous human cerebral cortex associated with brain trauma, tumours and congenital malformations: an electron microscopy study. Brain Inj 16(2):109–132

    Article  PubMed  Google Scholar 

  • Chee NP, Geddes R, Wills PR (1983) Metabolic heterogeneity in rabbit brain glycogen. Biochim Biophys Acta 756(1):9–12

    Article  CAS  PubMed  Google Scholar 

  • Choi IY, Gruetter R (2003) In vivo 13C NMR assessment of brain glycogen concentration and turnover in the awake rat. Neurochem Int 43(4–5):317–322

    Article  CAS  PubMed  Google Scholar 

  • Choi IY, Tkáč I, Ugurbil K, Gruetter R (1999) Noninvasive measurements of [1-13C] glycogen concentrations and metabolism in rat brain in vivo. J Neurochem 73(3):1300–1308

    Article  CAS  PubMed  Google Scholar 

  • Choi IY, Lee SP, Kim SG, Gruetter R (2001) In vivo measurements of brain glucose transport using the reversible Michaelis-Menten model and simultaneous measurements of cerebral blood flow changes during hypoglycemia. J Cereb Blood Flow Metab 21(6):653–663

    Article  CAS  PubMed  Google Scholar 

  • Choi IY, Seaquist ER, Gruetter R (2003) Effect of hypoglycemia on brain glycogen metabolism in vivo. J Neurosci Res 72(1):25–32

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cori GT, Cori CF (1940) The kinetics of the enzymatic synthesis of glycogen from glucose-1-phosphate. J Biol Chem 135:733–756

    CAS  Google Scholar 

  • Cruz NF, Dienel GA (2002) High glycogen levels in brains of rats with minimal environmental stimuli: implications for metabolic contributions of working astrocytes. J Cereb Blood Flow Metab 22(12):1476–1489

    Article  CAS  PubMed  Google Scholar 

  • Dienel GA, Cruz NF (2003) Neighborly interactions of metabolically-activated astrocytes in vivo. Neurochem Int 43(4–5):339–354

    Article  CAS  PubMed  Google Scholar 

  • Dienel GA, Ball KK, Cruz NF (2007) A glycogen phosphorylase inhibitor selectively enhances local rates of glucose utilization in brain during sensory stimulation of conscious rats: implications for glycogen turnover. J Neurochem 102:466–478

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Folbergrova J, Katsura KI, Siesjo BK (1996) Glycogen accumulated in the brain following insults is not degraded during a subsequent period of ischemia. J Neurol Sci 137(1):7–13

    Article  CAS  PubMed  Google Scholar 

  • Franken P, Gip P, Hagiwara G, Ruby NF, Heller HC (2003) Changes in brain glycogen after sleep deprivation vary with genotype. Am J Physiol Regul Integr Comp Physio 285(2):R413–R419

    CAS  Google Scholar 

  • Garriga J, Cusso R (1992) Effect of starvation on glycogen and glucose metabolism in different areas of the rat brain. Brain Res 591(2):277–282

    Article  CAS  PubMed  Google Scholar 

  • Gertz HJ, Cervos-Navarro J, Frydl V, Schultz F (1985) Glycogen accumulation of the aging human brain. Mech Ageing Dev 31(1):25–35

    Article  CAS  PubMed  Google Scholar 

  • Ghosh A, Cheung YY, Mansfield BC, Chou JY (2005) Brain contains a functional glucose-6-phosphatase complex capable of endogenous glucose production. J Biol Chem 280(12):11114–11119

    Article  CAS  PubMed  Google Scholar 

  • Gip P, Hagiwara G, Ruby NF, Heller HC (2002) Sleep deprivation decreases glycogen in the cerebellum but not in the cortex of young rats. Am J Physiol Regul Integr Comp Physiol 283(1):R54–R59

    CAS  PubMed  Google Scholar 

  • Gip P, Hagiwara G, Sapolsky RM, Cao VH, Heller HC, Ruby NF (2004) Glucocorticoids influence brain glycogen levels during sleep deprivation. Am J Physiol Regul Integr Comp Physiol 286(6):R1057–R1062

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Merino D, Bequet F, Berthelot M, Chennaoui M, Guezennec CY (2001) Site-dependent effects of an acute intensive exercise on extracellular 5-HT and 5-HIAA levels in rat brain. Neurosci Lett 301(2):143–146

    Article  CAS  PubMed  Google Scholar 

  • Hamprecht B, Dringen R, Pfeiffer B, Kurz G (1993) The possible roles of astrocytes in energy metabolism of the brain. In: Fedoroff S, Juurlink BHJ, Doucette R (eds) Biology and pathology of astrocyte-neuron interactions. Plenum, New York, pp 83–91

    Chapter  Google Scholar 

  • Herzog RI, Chan O, Yu S, Dziura J, McNay EC, Sherwin RS (2008) Effect of acute and recurrent hypoglycemia on changes in brain glycogen concentration. Endocrinology 149(4):1499–1504

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Horinaka N, Artz N, Jehle J, Takahashi S, Kennedy C, Sokoloff L (1997) Examination of potential mechanisms in the enhancement of cerebral blood flow by hypoglycemia and pharmacological doses of deoxyglucose. J Cereb Blood Flow Metab 17(1):54–63

    Article  CAS  PubMed  Google Scholar 

  • Howe FA (1993) An assessment of artefacts in localized and non-localized 31P MRS studies of phosphate metabolites and pH in rat tumours. NMR Biomed 6(1):43–52

    Article  CAS  PubMed  Google Scholar 

  • Hutchins DA, Rogers KJ (1970) Physiological and drug-induced changes in the glycogen content of mouse brain. Br J Pharmacol 39(1):9–25

    Article  CAS  PubMed Central  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(7):865–877

    Article  CAS  PubMed  Google Scholar 

  • Karadzic V, Mrsulja B (1969a) Deprivation of paradoxical sleep and brain glycogen. J Neurochem 16(1):29–34

    Article  CAS  PubMed  Google Scholar 

  • Karadzic V, Mrsulja B (1969b) Glycogenic response of CNS to paradoxical sleep deprivation in cats and rats. Electroencephalogr Clin Neurophysiol 27(5):552

    Article  CAS  PubMed  Google Scholar 

  • Karnovsky ML, Reich P, Anchors JM, Burrows BL (1983) Changes in brain glycogen during slow-wave sleep in the rat. J Neurochem 41(5):1498–1501

    Article  CAS  PubMed  Google Scholar 

  • Kong J, Shepel PN, Holden CP, Mackiewicz M, Pack AI, Geiger JD (2002) Brain glycogen decreases with increased periods of wakefulness: implications for homeostatic drive to sleep. J Neurosci 22(13):5581–5587

    CAS  PubMed  Google Scholar 

  • Lei H, Gruetter R (2006) Effect of chronic hypoglycaemia on glucose concentration and glycogen content in rat brain: a localized 13C NMR study. J Neurochem 99(1):260–268

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lowry OH, Berger SJ, Carter JG, Chi MM, Manchester JK, Knor J, Pusateri ME (1983) Diversity of metabolic patterns in human brain tumors: enzymes of energy metabolism and related metabolites and cofactors. J Neurochem 41(4):994–1010

    Article  CAS  PubMed  Google Scholar 

  • Madden A, Leach MO, Collins DJ, Payne GS (1991) The water resonance as an alternative pH reference: relevance to in vivo 31P NMR localized spectroscopy studies. Magn Reson Med 19(2):416–421

    Article  CAS  PubMed  Google Scholar 

  • Magistretti PJ, Sorg O (1993) Neurotransmitters regulate energy metabolism in astrocytes: implications for the metabolic trafficking between neural cells. Dev Neurosci 15(3–5):306–312

    Article  CAS  PubMed  Google Scholar 

  • Magistretti PJ, Hof PR, Martin JL (1986) Adenosine stimulates glycogenolysis in mouse cerebral cortex: a possible coupling mechanism between neuronal activity and energy metabolism. J Neurosci 6(9):2558–2562

    CAS  PubMed  Google Scholar 

  • Magnusson I, Rothman DL, Katz LD, Shulman RG, Shulman GI (1992) Increased rate of gluconeogenesis in type II diabetes mellitus. A 13C nuclear magnetic resonance study. J Clin Invest 90(4):1323–1327

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matsui T, Soya S, Okamoto M, Ichitani Y, Kawanaka K, Soya H (2011) Brain glycogen decreases during prolonged exercise. J Physiol 589(Pt 13):3383–3393

    CAS  PubMed Central  PubMed  Google Scholar 

  • Morgenthaler FD, van Heeswijk RB, Xin L, Laus S, Frenkel H, Lei H, Gruetter R (2008) Non-invasive quantification of brain glycogen absolute concentration. J Neurochem 107(5):1414–1423

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Morgenthaler FD, Lanz BR, Petit JM, Frenkel H, Magistretti PJ, Gruetter R (2009) Alteration of brain glycogen turnover in the conscious rat after 5h of prolonged wakefulness. Neurochem Int 55(1–3):45–51

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nelson SR, Schulz DW, Passonneau JV, Lowry OH (1968) Control of glycogen levels in brain. J Neurochem 15(11):1271–1279

    Article  CAS  PubMed  Google Scholar 

  • Obel LF, Muller MS, Walls AB, Sickmann HM, Bak LK, Waagepetersen HS, Schousboe A (2012) Brain glycogen-new perspectives on its metabolic function and regulation at the subcellular level. Front Neuroenerg 4:3. doi:10.3389/fnene.2012.00003

    Article  CAS  Google Scholar 

  • Ohiwa N, Saito T, Chang H, Nakamura T, Soya H (2006) Differential responsiveness of c-Fos expression in the rat brainstem to different treadmill running speeds. Neurosci Res 54(2):124–132

    Article  CAS  PubMed  Google Scholar 

  • Olsen NS, Klein JR (1947) Effect of insulin hypoglycemia on brain glucose, glycogen, lactate and phosphates. Arch Biochem 13(3):343–347

    CAS  PubMed  Google Scholar 

  • Öz G, Henry PG, Seaquist ER, Gruetter R (2002) Direct, noninvasive measurement of brain glycogen metabolism in humans. Neurochem Int 43(4–5):323–329

    Google Scholar 

  • Öz G, Henry PG, Tkáč I, Gruetter R (2005) A localization method for the measurement of fast relaxing 13C NMR signals in humans at high magnetic field. Appl Magn Reson 29(1):159–169

    Article  Google Scholar 

  • Öz G, Seaquist ER, Kumar A, Criego AB, Benedict LE, Rao JP, Henry PG, Van De Moortele PF, Gruetter R (2007) Human brain glycogen content and metabolism: implications on its role in brain energy metabolism. Am J Physiol Endocrinol Metab 292(3):E946–E951

    Article  PubMed  Google Scholar 

  • Öz G, Kumar A, Rao JP, Kodl CT, Chow L, Eberly LE, Seaquist ER (2009) Human brain glycogen metabolism during and after hypoglycemia. Diabetes 58(9):1978–1985

    Article  PubMed Central  PubMed  Google Scholar 

  • Öz G, Tesfaye N, Kumar A, Deelchand DK, Eberly LE, Seaquist ER (2012) Brain glycogen content and metabolism in subjects with type 1 diabetes and hypoglycemia unawareness. J Cereb Blood Flow Metab 32(2):256–263

    Article  PubMed Central  PubMed  Google Scholar 

  • Pagliari R, Peyrin L (1995) Norepinephrine release in the rat frontal cortex under treadmill exercise: a study with microdialysis. J Appl Physiol 78(6):2121–2130

    CAS  PubMed  Google Scholar 

  • Passonneau JV, Gatfield PD, Schulz DW, Lowry OH (1967) An enzymic method for measurement of glycogen. Anal Biochem 19(2):315–326

    Article  CAS  PubMed  Google Scholar 

  • Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci 91(22):10625–10629

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Petit JM, Tobler I, Allaman I, Borbely AA, Magistretti PJ (2005) Sleep deprivation modulates brain mRNAs encoding genes of glycogen metabolism. Eur J Neurosci 16(6):1163–1167

    Article  Google Scholar 

  • Petroff OA, Prichard JW, Behar KL, Alger JR, den Hollander JA, Shulman RG (1985) Cerebral intracellular pH by 31P nuclear magnetic resonance spectroscopy. Neurology 35(6):781–788

    Article  CAS  PubMed  Google Scholar 

  • Pfeuffer J, Tkáč I, Choi IY, Merkle H, Ugurbil 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(6):1077–1083

    Article  CAS  PubMed  Google Scholar 

  • Philip A, Hargreaves M, Baar K (2012) More than a store: regulatory roles for glycogen in skeletal muscle adaptation to exercise. Am J Physiol Endocrinol Metab 302(11):E1343–E1351

    Article  Google Scholar 

  • Radziuk J, Pye S (2001) Hepatic glucose uptake, gluconeogenesis and the regulation of glycogen synthesis. Diabetes Metab Res Rev 17(4):250–272

    Article  CAS  PubMed  Google Scholar 

  • Roberts JK, Wade-Jardetzky N, Jardetzky O (1981) Intracellular pH measurements by 31P nuclear magnetic resonance. Influence of factors other than pH on 31P chemical shifts. Biochemistry 20(19):5389–5394

    Article  CAS  PubMed  Google Scholar 

  • Roden M, Petersen KF, Shulman GI (2001) Nuclear magnetic resonance studies of hepatic glucose metabolism in humans. Recent Prog Horm Res 56:219–237

    Article  CAS  PubMed  Google Scholar 

  • Sagar SM, Sharp FR, Swanson RA (1987) The regional distribution of glycogen in rat brain fixed by microwave irradiation. Brain Res 417(1):172–174

    Article  CAS  PubMed  Google Scholar 

  • Salvan AM, Vion-Dury J, Confort-Gouny S, Dano P, Cozzone PJ (1997) Increased cerebral glycogen detected by localized 1H-magnetic resonance spectroscopy in a patient with suspected McArdle’s disease. Eur Neurol 37(4):251–253

    Article  CAS  PubMed  Google Scholar 

  • Shimizu N, Hamuro Y (1958) Deposition of glycogen and changes in some enzymes in brain wounds. Nature 181(4611):781–782

    Article  CAS  PubMed  Google Scholar 

  • Sickmann HM, Walls AB, Schousboe A, Bouman SD, Waagepetersen HS (2009) Functional significance of brain glycogen in sustaining glutamatergic neurotransmission. J Neurochem 109:80–86

    Article  CAS  PubMed  Google Scholar 

  • Smythe C, Cohen P (1991) The discovery of glycogenin and the priming mechanism for glycogen biogenesis. Eur J Biochem 200(3):625–631

    Article  CAS  PubMed  Google Scholar 

  • Sorg O, Pellerin L, Stolz M, Beggah S, Magistretti PJ (1995) Adenosine triphosphate and arachidonic acid stimulate glycogenolysis in primary cultures of mouse cerebral cortical astrocytes. Neurosci Lett 188(2):109–112

    Article  CAS  PubMed  Google Scholar 

  • Soya H, Mukai A, Deocaris CC, Ohiwa N, Chang H, Nishijima T, Fujikawa T, Togashi K, Saito T (2007) Threshold-like pattern of neuronal activation in the hypothalamus during treadmill running: establishment of a minimum running stress (MRS) rat model. Neurosci Res 58(4):341–348

    Article  CAS  PubMed  Google Scholar 

  • Strang RH, Bachelard HS (1971) Extraction, purification and turnover of rat brain glycogen. J Neurochem 18(6):1067–1076

    Article  CAS  PubMed  Google Scholar 

  • Subbarao KV, Stolzenburg JU, Hertz L (1995) Pharmacological characteristics of potassium-induced, glycogenolysis in astrocytes. Neurosci Lett 196(1–2):45–48

    Article  CAS  PubMed  Google Scholar 

  • Suh SW, Bergher JP, Anderson CM, Treadway JL, Fosgerau K, Swanson RA (2007) Astrocyte glycogen sustains neuronal activity during hypoglycemia: studies with the glycogen phosphorylase inhibitor CP-316,819 ([R-R*, S*]-5-chloro-N-[2-hydroxy-3-(methoxymethylamino)-3-oxo-1-(phenylmethyl)propyl]-1H-indole-2-carboxamide). J Pharmacol Exp Ther 321(1):45–50

    Article  CAS  PubMed  Google Scholar 

  • Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, Magistretti PJ, Alberini CM (2011) Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144(5):810–823

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Swanson RA (1992) Physiologic coupling of glial glycogen metabolism to neuronal activity in brain. Can J Physiol Pharmacol 70(Suppl):S138–S144

    Article  CAS  PubMed  Google Scholar 

  • Swanson RA, Morton MM, Sagar SM, Sharp FR (1992) Sensory stimulation induces local cerebral glycogenolysis: demonstration by autoradiography. Neuroscience 51(2):451–461

    Article  CAS  PubMed  Google Scholar 

  • Tekkök SB, Brown AM, Westenbroek R, Pellerin L, Ransom BR (2005) Transfer of glycogen-derived lactate from astrocytes to axons via specific monocarboxylate transporters supports mouse optic nerve activity. Neurosci Res 81(5):644–652

    Article  Google Scholar 

  • Tkáč I, Starcuk Z, Choi IY, Gruetter R (1999) In vivo 1H NMR spectroscopy of rat brain at 1 ms echo time. Magn Reson Med 41(4):649–656

    Article  PubMed  Google Scholar 

  • van Heeswijk RB, Morgenthaler FD, Xin L, Gruetter R (2010) Quantification of brain glycogen concentration and turnover through localized 13C NMR of both the C1 and C6 resonances. NMR Biomed 23(3):270–276

    PubMed  Google Scholar 

  • van Heeswijk RB, Pilloud Y, Morgenthaler FD, Gruetter R (2012) A comparison of in vivo 13C MR brain glycogen quantification at 9.4 and 14.1 T. Magn Reson Med 67(6):1523–1527

    Article  PubMed  Google Scholar 

  • Vilchez D, Ros S, Cifuentes D, Pujadas L, Valles J, Garcia-Fojeda B, Criado-Garcia O, Fernandez-Sanchez E, Medrano-Fernandez I, Dominguez J, Garcia-Rocha M, Soriano E, Rodriguez de Cordoba S, Guinovart JJ (2007) Mechanism suppressing glycogen synthesis in neurons and its demise in progressive myoclonus epilepsy. Nat Neurosci 10(11):1407–1413

    Article  CAS  PubMed  Google Scholar 

  • Vissing J, Andersen M, Diemer NH (1996) Exercise-induced changes in local cerebral glucose utilization in the rat. J Cereb Blood Flow Metab 16(4):729–736

    Article  CAS  PubMed  Google Scholar 

  • Walls AB, Heimbürger CM, Bouman SD, Schousboe A, Waagepetersen HS (2009) Robust glycogen shunt activity in astrocytes: effects of glutamatergic and adrenergic agents. Neuroscience 158(1):284–292

    Article  CAS  PubMed  Google Scholar 

  • Wiesinger H, Hamprecht B, Dringen R (1997) Metabolic pathways for glucose in astrocytes. Glia 21(1):22–34

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The preparation of this manuscript was supported by the National Institute of Neurological Disorders and Stroke (NINDS) grant R01 NS035192 (ERS, GÖ). The Center for Magnetic Resonance Research is supported by National Center for Research Resources (NCRR) biotechnology research resource grant P41 RR008079, National Institute of Biomedical Imaging and Bioengineering (NIBIB) grant P41 EB015894 and the Institutional Center Cores for Advanced Neuroimaging award P30 NS076408.

Author information

Authors and Affiliations

  1. Division of Diabetes, Endocrinology and Metabolism, Department of Medicine, University of Minnesota, 420 Delaware Street, SE, Minneapolis, MN, 55455, USA

    Ameer Khowaja & Elizabeth R. Seaquist

  2. Hoglund Brain Imaging Center, Department of Neurology, Department of Molecular & Integrative Physiology, University of Kansas Medical Center, Kansas City, KS, 66160, USA

    In-Young Choi

  3. Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, Minneapolis, MN, 55455, USA

    Gülin Öz

Authors
  1. Ameer Khowaja
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. In-Young Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elizabeth R. Seaquist
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gülin Öz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ameer Khowaja.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Khowaja, A., Choi, IY., Seaquist, E.R. et al. In vivo Magnetic Resonance Spectroscopy of cerebral glycogen metabolism in animals and humans. Metab Brain Dis 30, 255–261 (2015). https://doi.org/10.1007/s11011-014-9530-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11011-014-9530-7

Keywords

Search

Navigation