A Cellular Perspective on Brain Energy Metabolism and Functional Imaging

Neuron

Volumn 86, Issue 4, 2015, Pages 883-901

  Magistretti, Pierre J ^a,b,c   Allaman, Igor ^b  

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^b EPFL   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); GLUCOSE TRANSPORTER 3; HYDROXYACYLGLUTATHIONE HYDROLASE; LACTATE DEHYDROGENASE; LACTOYLGLUTATHIONE LYASE; MONOCARBOXYLATE TRANSPORTER; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE KINASE 4; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; GLUCOSE;

AEROBIC METABOLISM; ANAEROBIC GLYCOLYSIS; ASTROCYTE; BIOENERGY; BOLD SIGNAL; BRAIN BLOOD FLOW; CELL INTERACTION; CEREBELLUM; COGNITION; DORSOLATERAL PREFRONTAL CORTEX; ENERGY CONSUMPTION; ENERGY METABOLISM; ENZYME PHOSPHORYLATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GLUCOSE METABOLISM; GLUCOSE UTILIZATION; GLYCOGENOLYSIS; HUMAN; MICROGLIA; MIDDLE FRONTAL GYRUS; NERVE CELL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGODENDROGLIA; POSITRON EMISSION TOMOGRAPHY; POSTERIOR CINGULATE; PRECUNEUS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVIEW; SYNAPSE; UPREGULATION; ANIMAL; BRAIN; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES;

ANIMALS; ASTROCYTES; BRAIN; ENERGY METABOLISM; GLUCOSE; HUMANS; MAGNETIC RESONANCE IMAGING; NEURONS;

EID: 84930259783     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.03.035     Document Type: Review

References (204)

1. Aiello L.C., Wheeler P. The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr. Anthropol. 1995, 36:199-221.
2. Allaman I., Magistretti P.J. Brain energy metabolism. Fundamental Neuroscience 2013, 261-284. Academic Press, San Diego. L.R. Squire, D. Berg, F.E. Bloom, S. du Lac, A. Ghosh, N.C. Spitzer (Eds.).
3. Alle H., Roth A., Geiger J.R. Energy-efficient action potentials in hippocampal mossy fibers. Science 2009, 325:1405-1408.
4. Andriezen W.L. On a system of fibre-like cells surrounding the blood vessels of the brain of man and mammals, and its physiological significance. Int. Monatsschr. Anat. Physiol. 1893, 10:532-540.
5. Attwell D., Laughlin S.B. An energy budget for signaling in the grey matter of the brain. J.Cereb. Blood Flow Metab. 2001, 21:1133-1145.
6. Attwell D., Buchan A.M., Charpak S., Lauritzen M., Macvicar B.A., Newman E.A. Glial and neuronal control of brain blood flow. Nature 2010, 468:232-243.
7. Aubert A., Pellerin L., Magistretti P.J., Costalat R. A coherent neurobiological framework for functional neuroimaging provided by a model integrating compartmentalized energy metabolism. Proc. Natl. Acad. Sci. USA 2007, 104:4188-4193.
8. Azarias G., Perreten H., Lengacher S., Poburko D., Demaurex N., Magistretti P.J., Chatton J.Y. Glutamate transport decreases mitochondrial pH and modulates oxidative metabolism in astrocytes. J.Neurosci. 2011, 31:3550-3559.
9. Bak L.K., Schousboe A., Waagepetersen H.S. The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J.Neurochem. 2006, 98:641-653.
10. Barros L.F. Metabolic signaling by lactate in the brain. Trends Neurosci. 2013, 36:396-404.
11. Barros L.F., Bittner C.X., Loaiza A., Porras O.H. A quantitative overview of glucose dynamics in the gliovascular unit. Glia 2007, 55:1222-1237.
12. Barros L.F., San Martín A., Sotelo-Hitschfeld T., Lerchundi R., Fernández-Moncada I., Ruminot I., Gutiérrez R., Valdebenito R., Ceballo S., Alegría K., et al. Small is fast: astrocytic glucose and lactate metabolism at cellular resolution. Front. Cell. Neurosci. 2013, 7:27.
13. Bauernfeind A.L., Barks S.K., Duka T., Grossman L.I., Hof P.R., Sherwood C.C. Aerobic glycolysis in the primate brain: reconsidering theimplications for growth and maintenance. Brain Struct. Funct. 2014, 219:1149-1167.
14. Bélanger M., Allaman I., Magistretti P.J. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 2011, 14:724-738.
15. Bélanger M., Yang J., Petit J.M., Laroche T., Magistretti P.J., Allaman I. Role of the glyoxalase system in astrocyte-mediated neuroprotection. J.Neurosci. 2011, 31:18338-18352.
16. Bergersen L.H., Gjedde A. Is lactate a volume transmitter of metabolic states of the brain?. Front. Neuroenergetics 2012, 4:5.
17. +-mediated metabolic waves. Proc. Natl. Acad. Sci. USA 2004, 101:14937-14942.
18. Berthet C., Lei H., Thevenet J., Gruetter R., Magistretti P.J., Hirt L. Neuroprotective role of lactate after cerebral ischemia. J.Cereb. Blood Flow Metab. 2009, 29:1780-1789.
19. Berthet C., Castillo X., Magistretti P.J., Hirt L. New evidence of neuroprotection by lactate after transient focal cerebral ischaemia: extended benefit after intracerebroventricular injection and efficacy of intravenous administration. Cerebrovasc. Dis. 2012, 34:329-335.
20. Bittar P.G., Charnay Y., Pellerin L., Bouras C., Magistretti P.J. Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J.Cereb. Blood Flow Metab. 1996, 16:1079-1089.
21. + and a delayed and persistent effect of glutamate. J.Neurosci. 2011, 31:4709-4713.
22. Bliss T.M., Ip M., Cheng E., Minami M., Pellerin L., Magistretti P., Sapolsky R.M. Dual-gene, dual-cell type therapy against an excitotoxic insult by bolstering neuroenergetics. J.Neurosci. 2004, 24:6202-6208.
23. Bolaños J.P., Almeida A., Moncada S. Glycolysis: a bioenergetic or a survival pathway?. Trends Biochem. Sci. 2010, 35:145-149.
24. 13C nuclear magnetic resonance spectroscopy. J.Neurosci. 2010, 30:13983-13991.
25. Bouzat P., Oddo M. Lactate and the injured brain: friend or foe?. Curr. Opin. Crit. Care 2014, 20:133-140.
26. Bouzat P., Sala N., Suys T., Zerlauth J.B., Marques-Vidal P., Feihl F., Bloch J., Messerer M., Levivier M., Meuli R., et al. Cerebral metabolic effects of exogenous lactate supplementation on the injured human brain. Intensive Care Med. 2014, 40:412-421.
27. Bouzier A.K., Thiaudiere E., Biran M., Rouland R., Canioni P., Merle M. The metabolism of [3-(13)C]lactate in the rat brain is specific of a pyruvate carboxylase-deprived compartment. J.Neurochem. 2000, 75:480-486.
28. Bouzier-Sore A.K., Pellerin L. Unraveling the complex metabolic nature of astrocytes. Front. Cell. Neurosci. 2013, 7:179.
29. Bouzier-Sore A.K., Voisin P., Canioni P., Magistretti P.J., Pellerin L. Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J.Cereb. Blood Flow Metab. 2003, 23:1298-1306.
30. Bouzier-Sore A.K., Voisin P., Bouchaud V., Bezancon E., Franconi J.M., Pellerin L. Competition between glucose and lactate as oxidative energy substrates in both neurons and astrocytes: a comparative NMR study. Eur. J. Neurosci. 2006, 24:1687-1694.
31. Bozek K., Wei Y., Yan Z., Liu X., Xiong J., Sugimoto M., Tomita M., Pääbo S., Pieszek R., Sherwood C.C., et al. Exceptional evolutionary divergence of human muscle and brain metabolomes parallels human cognitive and physical uniqueness. PLoS Biol. 2014, 12:e1001871.
32. Bozzo L., Puyal J., Chatton J.Y. Lactate modulates the activity of primary cortical neurons through a receptor-mediated pathway. PLoS ONE 2013, 8:e71721.
33. Brown A.M., Sickmann H.M., Fosgerau K., Lund T.M., Schousboe A., Waagepetersen H.S., Ransom B.R. Astrocyte glycogen metabolism is required for neural activity during aglycemia or intense stimulation in mouse white matter. J.Neurosci. Res. 2005, 79:74-80.
34. Brunet J.F., Grollimund L., Chatton J.Y., Lengacher S., Magistretti P.J., Villemure J.G., Pellerin L. Early acquisition of typical metabolic features upon differentiation of mouse neural stem cells into astrocytes. Glia 2004, 46:8-17.
35. Bushong E.A., Martone M.E., Jones Y.Z., Ellisman M.H. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J.Neurosci. 2002, 22:183-192.
36. Buxton R.B. Interpreting oxygenation-based neuroimaging signals: the importance and the challenge of understanding brain oxygen metabolism. Front. Neuroenergetics 2010, 2:8.
37. Cáceres M., Lachuer J., Zapala M.A., Redmond J.C., Kudo L., Geschwind D.H., Lockhart D.J., Preuss T.M., Barlow C. Elevated gene expression levels distinguish human from non-human primate brains. Proc. Natl. Acad. Sci. USA 2003, 100:13030-13035.
38. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: anew resource for understanding brain development and function. J.Neurosci. 2008, 28:264-278.
39. Cauli B., Hamel E. Revisiting the role of neurons in neurovascular coupling. Front. Neuroenergetics 2010, 2:9.
40. Cerdán S., Rodrigues T.B., Sierra A., Benito M., Fonseca L.L., Fonseca C.P., García-Martín M.L. The redox switch/redox coupling hypothesis. Neurochem. Int. 2006, 48:523-530.
41. Choi H.B., Gordon G.R., Zhou N., Tai C., Rungta R.L., Martinez J., Milner T.A., Ryu J.K., McLarnon J.G., Tresguerres M., et al. Metabolic communication between astrocytes and neurons via bicarbonate-responsive soluble adenylyl cyclase. Neuron 2012, 75:1094-1104.
42. Cholet N., Pellerin L., Welker E., Lacombe P., Seylaz J., Magistretti P., Bonvento G. Local injection of antisense oligonucleotides targeted to the glial glutamate transporter GLAST decreases the metabolic response to somatosensory activation. J.Cereb. Blood Flow Metab. 2001, 21:404-412.
43. Chuquet J., Quilichini P., Nimchinsky E.A., Buzsáki G. Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex. J.Neurosci. 2010, 30:15298-15303.
44. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 2001, 65:1-105.
45. Dienel G.A. Brain lactate metabolism: the discoveries and the controversies. J.Cereb. Blood Flow Metab. 2012, 32:1107-1138.
46. DiNuzzo M., Mangia S., Maraviglia B., Giove F. Changes in glucose uptake rather than lactate shuttle take center stage in subserving neuroenergetics: evidence from mathematical modeling. J.Cereb. Blood Flow Metab. 2010, 30:586-602.
47. 1H NMR spectroscopy. Neuroimage 2012, 61:342-362.
48. Duka T., Anderson S.M., Collins Z., Raghanti M.A., Ely J.J., Hof P.R., Wildman D.E., Goodman M., Grossman L.I., Sherwood C.C. Synaptosomal lactate dehydrogenase isoenzyme composition is shifted toward aerobic forms in primate brain evolution. Brain Behav. Evol. 2014, 83:216-230.
49. Elston G.N., Benavides-Piccione R., Elston A., Zietsch B., Defelipe J., Manger P., Casagrande V., Kaas J.H. Specializations of the granular prefrontal cortex of primates: implications for cognitive processing. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 2006, 288:26-35.
50. Erlichman J.S., Hewitt A., Damon T.L., Hart M., Kurascz J., Li A., Leiter J.C. Inhibition of monocarboxylate transporter 2 in the retrotrapezoid nucleus in rats: a test of the astrocyte-neuron lactate-shuttle hypothesis. J.Neurosci. 2008, 28:4888-4896.
51. Evans R.D., Brown A.M., Ransom B.R. Glycogen function in adult central and peripheral nerves. J.Neurosci. Res. 2013, 91:1044-1049.
52. Figley C.R., Stroman P.W. The role(s) of astrocytes and astrocyte activity in neurometabolism, neurovascular coupling, and the production of functional neuroimaging signals. Eur. J. Neurosci. 2011, 33:577-588.
53. Filosa J.A., Iddings J.A. Astrocyte regulation of cerebral vascular tone. Am. J. Physiol. Heart Circ. Physiol. 2013, 305:H609-H619.
54. Fox P.T., Raichle M.E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl. Acad. Sci. USA 1986, 83:1140-1144.
55. Fox P.T., Raichle M.E., Mintun M.A., Dence C. Nonoxidative glucose consumption during focal physiologic neural activity. Science 1988, 241:462-464.
56. Friede R.L., van Houten W.H. Neuronal extension and glial supply: functional significance of glia. Proc. Natl. Acad. Sci. USA 1962, 48:817-821.
57. Fu X., Giavalisco P., Liu X., Catchpole G., Fu N., Ning Z.B., Guo S., Yan Z., Somel M., Pääbo S., et al. Rapid metabolic evolution in human prefrontal cortex. Proc. Natl. Acad. Sci. USA 2011, 108:6181-6186.
58. Fünfschilling U., Supplie L.M., Mahad D., Boretius S., Saab A.S., Edgar J., Brinkmann B.G., Kassmann C.M., Tzvetanova I.D., Möbius W., et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 2012, 485:517-521.
59. 13C-labelled microdialysis and high-resolution nuclear magnetic resonance study. Brain 2009, 132:2839-2849.
60. Genoud C., Quairiaux C., Steiner P., Hirling H., Welker E., Knott G.W. Plasticity of astrocytic coverage and glutamate transporter expression in adult mouse cortex. PLoS Biol. 2006, 4:e343.
61. Giaume C., Koulakoff A., Roux L., Holcman D., Rouach N. Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat. Rev. Neurosci. 2010, 11:87-99.
62. Giaume C., Leybaert L., Naus C.C., Sáez J.C. Connexin and pannexin hemichannels in brain glial cells: properties, pharmacology, and roles. Front. Pharmacol. 2013, 4:88.
63. Golgi C. Sulla fine anatomia degli organi centrali del sisterna nervoso 1886, Hoepli, Milano.
64. Goodman M., Sterner K.N. Phylogenomic evidence of adaptive evolution in the ancestry of humans. Proc. Natl. Acad. Sci. USA 2010, 107(Suppl 2):8918-8923.
65. Goyal M.S., Hawrylycz M., Miller J.A., Snyder A.Z., Raichle M.E. Aerobic glycolysis in the human brain is associated with development and neotenous gene expression. Cell Metab. 2014, 19:49-57.
66. Grossman L.I., Wildman D.E., Schmidt T.R., Goodman M. Accelerated evolution of the electron transport chain in anthropoid primates. Trends Genet. 2004, 20:578-585.
67. Halestrap A.P. Monocarboxylic acid transport. Compr. Physiol. 2013, 3:1611-1643.
68. Halim N.D., Mcfate T., Mohyeldin A., Okagaki P., Korotchkina L.G., Patel M.S., Jeoung N.H., Harris R.A., Schell M.J., Verma A. Phosphorylation status of pyruvate dehydrogenase distinguishes metabolic phenotypes of cultured rat brain astrocytes and neurons. Glia 2010, 58:1168-1176.
69. Hall C.N., Klein-Flügge M.C., Howarth C., Attwell D. Oxidative phosphorylation, not glycolysis, powers presynaptic and postsynaptic mechanisms underlying brain information processing. J.Neurosci. 2012, 32:8940-8951.
70. Hamberger A., Hyden H. Inverse enzymatic changes in neurons and glia during increased function and hypoxia. J.Cell Biol. 1963, 16:521-525.
71. Harris J.J., Jolivet R., Attwell D. Synaptic energy use and supply. Neuron 2012, 75:762-777.
72. Harrison K.H., Hof P.R., Wang S.S. Scaling laws in the mammalian neocortex: does form provide clues to function?. J.Neurocytol. 2002, 31:289-298.
73. Herculano-Houzel S. Scaling of brain metabolism with a fixed energy budget per neuron: implications for neuronal activity, plasticity and evolution. PLoS ONE 2011, 6:e17514.
74. Herrero-Mendez A., Almeida A., Fernández E., Maestre C., Moncada S., Bolaños J.P. The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat. Cell Biol. 2009, 11:747-752.
75. Hertz L., Peng L., Dienel G.A. Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J.Cereb. Blood Flow Metab. 2007, 27:219-249.
76. Hillman E.M. Coupling mechanism and significance of the BOLD signal: a status report. Annu. Rev. Neurosci. 2014, 37:161-181.
77. 2+-dependent glycogen hydrolysis in mouse cerebral cortex. J.Neurosci. 1988, 8:1922-1928.
78. Hu Y., Wilson G.S. A temporary local energy pool coupled toneuronal activity: fluctuations of extracellular lactate levels in rat brain monitored with rapid-response enzyme-based sensor. J.Neurochem. 1997, 69:1484-1490.
79. Hu X., Yacoub E. The story of the initial dip in fMRI. Neuroimage 2012, 62:1103-1108.
80. Hu Y., Mitchell K.M., Albahadily F.N., Michaelis E.K., Wilson G.S. Direct measurement of glutamate release in the brain using a dual enzyme-based electrochemical sensor. Brain Res. 1994, 659:117-125.
81. Hutchinson D.S., Summers R.J., Gibbs M.E. Beta2- and beta3-adrenoceptors activate glucose uptake in chick astrocytes by distinct mechanisms: a mechanism for memory enhancement?. J.Neurochem. 2007, 103:997-1008.
82. Hyden H., Lange P.W. A kinetic study of the neuronglia relationship. J.Cell Biol. 1962, 13:233-237.
83. Hyder F., Patel A.B., Gjedde A., Rothman D.L., Behar K.L., Shulman R.G. Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J.Cereb. Blood Flow Metab. 2006, 26:865-877.
84. Hyder F., Rothman D.L., Bennett M.R. Cortical energy demands of signaling and nonsignaling components in brain are conserved across mammalian species and activity levels. Proc. Natl. Acad. Sci. USA 2013, 110:3549-3554.
85. Iadecola C., Nedergaard M. Glial regulation of the cerebral microvasculature. Nat. Neurosci. 2007, 10:1369-1376.
86. Iliff J.J., Wang M., Liao Y., Plogg B.A., Peng W., Gundersen G.A., Benveniste H., Vates G.E., Deane R., Goldman S.A., et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci. Transl. Med. 2012, 4:147ra111.
87. Itoh Y., Esaki T., Shimoji K., Cook M., Law M.J., Kaufman E., Sokoloff L. Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia invitro and on glucose utilization by brain invivo. Proc. Natl. Acad. Sci. USA 2003, 100:4879-4884.
88. Ivanov A., Mukhtarov M., Bregestovski P., Zilberter Y. Lactate effectively covers energy demands during neuronal network activity in neonatal hippocampal slices. Front. Neuroenergetics 2011, 3:2.
89. Izumi Y., Benz A.M., Zorumski C.F., Olney J.W. Effects of lactate and pyruvate on glucose deprivation in rat hippocampal slices. Neuroreport 1994, 5:617-620.
90. Izumi Y., Benz A.M., Katsuki H., Zorumski C.F. Endogenous monocarboxylates sustain hippocampal synaptic function and morphological integrity during energy deprivation. J.Neurosci. 1997, 17:9448-9457.
91. Jakoby P., Schmidt E., Ruminot I., Gutiérrez R., Barros L.F., Deitmer J.W. Higher transport and metabolism of glucose in astrocytes compared with neurons: a multiphoton study of hippocampal and cerebellar tissue slices. Cereb. Cortex 2014, 24:222-231.
92. Jerison H.J. Evolution of the Brain and Intelligence 1973, Academic Press, New York.
93. Jolivet R., Magistretti P.J., Weber B. Deciphering neuron-gliacompartmentalization in cortical energy metabolism. Front. Neuroenergetics 2009, 1:4.
94. Jolivet R., Allaman I., Pellerin L., Magistretti P.J., Weber B. Comment on recent modeling studies of astrocyte-neuron metabolic interactions. J.Cereb. Blood Flow Metab. 2010, 30:1982-1986.
95. Jolivet R., Coggan J.S., Allaman I., Magistretti P.J. Multi-timescale modeling of activity-dependent metabolic coupling in the neuron-glia-vasculature ensemble. PLoS Comput. Biol. 2015, 11:e1004036.
96. Just N., Xin L., Frenkel H., Gruetter R. Characterization of sustained BOLD activation in the rat barrel cortex and neurochemical consequences. Neuroimage 2013, 74:343-351.
97. Kacem K., Lacombe P., Seylaz J., Bonvento G. Structural organization of the perivascular astrocyte endfeet and their relationship withthe endothelial glucose transporter: a confocal microscopy study. Glia 1998, 23:1-10.
98. Kadekaro M., Crane A.M., Sokoloff L. Differential effects of electrical stimulation of sciatic nerve on metabolic activity in spinal cord and dorsal root ganglion in the rat. Proc. Natl. Acad. Sci. USA 1985, 82:6010-6013.
99. Karbowski J. Global and regional brain metabolic scaling and its functional consequences. BMC Biol. 2007, 5:18.
100. Kasischke K.A., Vishwasrao H.D., Fisher P.J., Zipfel W.R., Webb W.W. Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 2004, 305:99-103.
101. Kettenmann H., Verkhratsky A. Neuroglia: the 150 years after. Trends Neurosci. 2008, 31:653-659.
102. Khaitovich P., Tang K., Franz H., Kelso J., Hellmann I., Enard W., Lachmann M., Pääbo S. Positive selection on gene expression in the human brain. Curr. Biol. 2006, 16:R356-R358.
103. Kleinfeld D., Blinder P., Drew P.J., Driscoll J.D., Muller A., Tsai P.S., Shih A.Y. A guide to delineate the logic of neurovascular signaling in the brain. Front. Neuroenergetics 2011, 3:1.
104. Kuzawa C.W., Chugani H.T., Grossman L.I., Lipovich L., Muzik O., Hof P.R., Wildman D.E., Sherwood C.C., Leonard W.R., Lange N. Metabolic costs and evolutionary implications of human brain development. Proc. Natl. Acad. Sci. USA 2014, 111:13010-13015.
105. Lee Y., Morrison B.M., Li Y., Lengacher S., Farah M.H., Hoffman P.N., Liu Y., Tsingalia A., Jin L., Zhang P.W., et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012, 487:443-448.
106. Lennie P. The cost of cortical computation. Curr. Biol. 2003, 13:493-497.
107. Lin A.L., Fox P.T., Hardies J., Duong T.Q., Gao J.H. Nonlinear coupling between cerebral blood flow, oxygen consumption, and ATP production in human visual cortex. Proc. Natl. Acad. Sci. USA 2010, 107:8446-8451.
108. Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
109. Lovatt D., Sonnewald U., Waagepetersen H.S., Schousboe A., He W., Lin J.H., Han X., Takano T., Wang S., Sim F.J., et al. The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J.Neurosci. 2007, 27:12255-12266.
110. Magistretti P.J. Brain energy metabolism. Fundamental Neuroscience 1999, 389-413. Academic Press, San Diego. M.J. Zigmond, F.E. Bloom, S.C. Landis, J.L. Roberts, L.R. Squire (Eds.).
111. Magistretti P.J. Cellular bases of functional brain imaging: insights from neuron-glia metabolic coupling. Brain Res. 2000, 886:108-112.
112. Magistretti P.J. Neuron-glia metabolic coupling and plasticity. J.Exp. Biol. 2006, 209:2304-2311.
113. Magistretti P.J. Neuroscience. Low-cost travel in neurons. Science 2009, 325:1349-1351.
114. Magistretti P.J., Morrison J.H. Noradrenaline- and vasoactive intestinal peptide-containing neuronal systems in neocortex: functional convergence with contrasting morphology. Neuroscience 1988, 24:367-378.
115. Magistretti P.J., Pellerin L. Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1999, 354:1155-1163.
116. + dynamics and ATP hydrolysis in astrocytes. J.Neural Transm. 2005, 112:77-85.
117. Magistretti P.J., Morrison J.H., Shoemaker W.J., Sapin V., Bloom F.E. Vasoactive intestinal polypeptide induces glycogenolysis in mouse cortical slices: a possible regulatory mechanism for the local control of energy metabolism. Proc. Natl. Acad. Sci. USA 1981, 78:6535-6539.
118. Malonek D., Grinvald A. Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science 1996, 272:551-554.
119. Mamczur P., Borsuk B., Paszko J., Sas Z., Mozrzymas J., Wiśniewski J.R., Gizak A., Rakus D. Astrocyte-neuron crosstalk regulates the expression and subcellular localization of carbohydrate metabolism enzymes. Glia 2015, 63:328-340.
120. Mangia S., Garreffa G., Bianciardi M., Giove F., Di Salle F., Maraviglia B. The aerobic brain: lactate decrease at the onset of neural activity. Neuroscience 2003, 118:7-10.
121. Mangia S., Giove F., Tkác I., Logothetis N.K., Henry P.G., Olman C.A., Maraviglia B., Di Salle F., Uğurbil K. Metabolic and hemodynamic events after changes in neuronal activity: current hypotheses, theoretical predictions and invivo NMR experimental findings. J.Cereb. Blood Flow Metab. 2009, 29:441-463.
122. Mangia S., Simpson I.A., Vannucci S.J., Carruthers A. The invivo neuron-to-astrocyte lactate shuttle in human brain: evidence frommodeling of measured lactate levels during visual stimulation. J.Neurochem. 2009, 109(Suppl 1):55-62.
123. Martin R.D. Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 1981, 293:57-60.
124. Mathiisen T.M., Lehre K.P., Danbolt N.C., Ottersen O.P. The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia 2010, 58:1094-1103.
125. McIlwain H. Substances which support respiration and metabolic response to electrical impulses in human cerebral tissues. J.Neurol. Neurosurg. Psychiatry 1953, 16:257-266.
126. McKenna M.C. The glutamate-glutamine cycle is not stoichiometric: fates of glutamate in brain. J.Neurosci. Res. 2007, 85:3347-3358.
127. Miele M., Boutelle M.G., Fillenz M. The source of physiologically stimulated glutamate efflux from the striatum of conscious rats. J.Physiol. 1996, 497:745-751.
128. Mink J.W., Blumenschine R.J., Adams D.B. Ratio of central nervous system to body metabolism in vertebrates: its constancy and functional basis. Am. J. Physiol. 1981, 241:R203-R212.
129. Mueckler M., Thorens B. The SLC2 (GLUT) family of membrane transporters. Mol. Aspects Med. 2013, 34:121-138.
130. Münch G., Westcott B., Menini T., Gugliucci A. Advanced glycation endproducts and their pathogenic roles in neurological disorders. Amino Acids 2012, 42:1221-1236.
131. Nagase M., Takahashi Y., Watabe A.M., Kubo Y., Kato F. On-site energy supply at synapses through monocarboxylate transporters maintains excitatory synaptic transmission. J.Neurosci. 2014, 34:2605-2617.
132. Nedergaard M., Ransom B., Goldman S.A. New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 2003, 26:523-530.
133. Newman L.A., Korol D.L., Gold P.E. Lactate produced by glycogenolysis in astrocytes regulates memory processing. PLoS ONE 2011, 6:e28427.
134. Obel L.F., Müller M.S., Walls A.B., Sickmann H.M., Bak L.K., Waagepetersen H.S., Schousboe A. Brain glycogen-new perspectives on its metabolic function and regulation at the subcellular level. Front. Neuroenergetics 2012, 4:3.
135. Ogawa S., Lee T.M., Kay A.R., Tank D.W. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. USA 1990, 87:9868-9872.
136. Ogawa S., Lee T.M., Nayak A.S., Glynn P. Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields. Magn. Reson. Med. 1990, 14:68-78.
137. Patel A.B., Lai J.C., Chowdhury G.M., Hyder F., Rothman D.L., Shulman R.G., Behar K.L. Direct evidence for activity-dependent glucose phosphorylation in neurons with implications for the astrocyte-to-neuron lactate shuttle. Proc. Natl. Acad. Sci. USA 2014, 111:5385-5390.
138. Pellerin L., Magistretti P.J. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. USA 1994, 91:10625-10629.
139. +-ATPase activity in astrocytes via activation of a distinct subunit highly sensitive to ouabain. J.Neurochem. 1997, 69:2132-2137.
140. Pellerin L., Magistretti P.J. Sweet sixteen for ANLS. J.Cereb. Blood Flow Metab. 2012, 32:1152-1166.
141. Pellerin L., Bouzier-Sore A.K., Aubert A., Serres S., Merle M., Costalat R., Magistretti P.J. Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 2007, 55:1251-1262.
142. Petzold G.C., Murthy V.N. Role of astrocytes in neurovascular coupling. Neuron 2011, 71:782-797.
143. Pierre K., Pellerin L. Monocarboxylate transporters in the central nervous system: distribution, regulation and function. J.Neurochem. 2005, 94:1-14.
144. Porras O.H., Loaiza A., Barros L.F. Glutamate mediates acute glucose transport inhibition in hippocampal neurons. J.Neurosci. 2004, 24:9669-9673.
145. 1H NMR in human visual cortex during physiologic stimulation. Proc. Natl. Acad. Sci. USA 1991, 88:5829-5831.
146. Pysh J.J., Khan T. Variations in mitochondrial structure and content of neurons and neuroglia in rat brain: an electron microscopic study. Brain Res. 1972, 36:1-18.
147. Qu H., Håberg A., Haraldseth O., Unsgård G., Sonnewald U. (13)C MR spectroscopy study of lactate as substrate for rat brain. Dev. Neurosci. 2000, 22:429-436.
148. Raichle M.E. Positron emission tomography. Annu. Rev. Neurosci. 1983, 6:249-267.
149. Raichle M.E. Behind the scenes of functional brain imaging: a historical and physiological perspective. Proc. Natl. Acad. Sci. USA 1998, 95:765-772.
150. Raichle M.E., Mintun M.A. Brain work and brain imaging. Annu. Rev. Neurosci. 2006, 29:449-476.
151. Rangaraju V., Calloway N., Ryan T.A. Activity-driven local ATP synthesis is required for synaptic function. Cell 2014, 156:825-835.
152. Rouach N., Koulakoff A., Abudara V., Willecke K., Giaume C. Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 2008, 322:1551-1555.
153. Roy C.S., Sherrington C.S. On the regulation of the blood-supply of the brain. J.Physiol. 1890, 11:85-158.
154. +. J.Neurosci. 2011, 31:14264-14271.
155. Saab A.S., Tzvetanova I.D., Nave K.A. The role of myelin and oligodendrocytes in axonal energy metabolism. Curr. Opin. Neurobiol. 2013, 23:1065-1072.
156. Sada N., Lee S., Katsu T., Otsuki T., Inoue T. Targeting LDH enzymes with a stiripentol analog to treat epilepsy. Science 2015, 347:1362-1367.
157. Sampol D., Ostrofet E., Jobin M.L., Raffard G., Sanchez S., Bouchaud V., Franconi J.M., Bonvento G., Bouzier-Sore A.K. Glucose and lactate metabolism in the awake and stimulated rat: a (13)C-NMR study. Front. Neuroenergetics 2013, 5:5.
158. 31P magnetic resonance spectroscopy. J.Cereb. Blood Flow Metab. 1992, 12:584-592.
159. Schaller B., Mekle R., Xin L., Kunz N., Gruetter R. Net increase of lactate and glutamate concentration in activated human visual cortex detected with magnetic resonance spectroscopy at 7 tesla. J.Neurosci. Res. 2013, 91:1076-1083.
160. +/- mice. Am. J. Physiol. Endocrinol. Metab. 2008, 295:E1084-E1094.
161. Schurr A. Cerebral glycolysis: a century of persistent misunderstanding and misconception. Front. Neurosci. 2014, 8:360.
162. Schurr A., Gozal E. Aerobic production and utilization of lactate satisfy increased energy demands upon neuronal activation in hippocampal slices and provide neuroprotection against oxidative stress. Front. Pharmacol. 2011, 2:96.
163. Schurr A., West C.A., Rigor B.M. Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 1988, 240:1326-1328.
164. Schurr A., Payne R.S., Miller J.J., Rigor B.M. Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further invitro validation. J.Neurochem. 1997, 69:423-426.
165. Schurr A., Payne R.S., Miller J.J., Tseng M.T., Rigor B.M. Blockade of lactate transport exacerbates delayed neuronal damage in a rat model of cerebral ischemia. Brain Res. 2001, 895:268-272.
166. Selak I., Skaper S.D., Varon S. Pyruvate participation in the low molecular weight trophic activity for central nervous system neurons in glia-conditioned media. J.Neurosci. 1985, 5:23-28.
167. Serres S., Bezancon E., Franconi J.M., Merle M. Exvivo analysis of lactate and glucose metabolism in the rat brain under different states of depressed activity. J.Biol. Chem. 2004, 279:47881-47889.
168. Serres S., Bezancon E., Franconi J.M., Merle M. Exvivo NMR study of lactate metabolism in rat brain under various depressed states. J.Neurosci. Res. 2005, 79:19-25.
169. Sherwood C.C., Stimpson C.D., Raghanti M.A., Wildman D.E., Uddin M., Grossman L.I., Goodman M., Redmond J.C., Bonar C.J., Erwin J.M., Hof P.R. Evolution of increased glia-neuron ratios in the human frontal cortex. Proc. Natl. Acad. Sci. USA 2006, 103:13606-13611.
170. 13C NMR of intermediary metabolism: implications for systemic physiology. Annu. Rev. Physiol. 2001, 63:15-48.
171. Simard M., Arcuino G., Takano T., Liu Q.S., Nedergaard M. Signaling at the gliovascular interface. J.Neurosci. 2003, 23:9254-9262.
172. Simpson I.A., Carruthers A., Vannucci S.J. Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J.Cereb. Blood Flow Metab. 2007, 27:1766-1791.
173. Smith D., Pernet A., Hallett W.A., Bingham E., Marsden P.K., Amiel S.A. Lactate: a preferred fuel for human brain metabolism invivo. J.Cereb. Blood Flow Metab. 2003, 23:658-664.
174. Sofroniew M.V., Vinters H.V. Astrocytes: biology and pathology. Acta Neuropathol. 2010, 119:7-35.
175. Sokoloff L. Localization of functional activity in the central nervous system by measurement of glucose utilization with radioactive deoxyglucose. J.Cereb. Blood Flow Metab. 1981, 1:7-36.
176. 14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J.Neurochem. 1977, 28:897-916.
177. Sorg O., Magistretti P.J. Characterization of the glycogenolysis elicited by vasoactive intestinal peptide, noradrenaline and adenosine in primary cultures of mouse cerebral cortical astrocytes. Brain Res. 1991, 563:227-233.
178. Sorg O., Pellerin L., Stolz M., Beggah S., Magistretti P.J. Adenosine triphosphate and arachidonic acid stimulate glycogenolysis in primary cultures of mouse cerebral cortical astrocytes. Neurosci. Lett. 1995, 188:109-112.
179. Stephan H., Baron G., Frahm H. Comparative size of brains and brain components. Comparative Primate Biology 1988, 1-38. Alan R. Liss, New York. H.D. Steklis, J. Erwin (Eds.).
180. Stobart J.L., Anderson C.M. Multifunctional role of astrocytes as gatekeepers of neuronal energy supply. Front. Cell. Neurosci. 2013, 7:38.
181. Stuart C.A., Ross I.R., Howell M.E., McCurry M.P., Wood T.G., Ceci J.D., Kennel S.J., Wall J. Brain glucose transporter (Glut3) haploinsufficiency does not impair mouse brain glucose uptake. Brain Res. 2011, 1384:15-22.
182. *]-5-chloro-N-[2-hydroxy-3-(methoxymethylamino)-3-oxo-1-(phenylmethyl)propyl]-1H-indole-2-carboxamide). J.Pharmacol. Exp. Ther. 2007, 321:45-50.
183. Suzuki A., Stern S.A., Bozdagi O., Huntley G.W., Walker R.H., Magistretti P.J., Alberini C.M. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 2011, 144:810-823.
184. Swanson R.A., Choi D.W. Glial glycogen stores affect neuronal survival during glucose deprivation invitro. J.Cereb. Blood Flow Metab. 1993, 13:162-169.
185. Takahashi S., Driscoll B.F., Law M.J., Sokoloff L. Role of sodium and potassium ions in regulation of glucose metabolism in cultured astroglia. Proc. Natl. Acad. Sci. USA 1995, 92:4616-4620.
186. Tang F., Lane S., Korsak A., Paton J.F., Gourine A.V., Kasparov S., Teschemacher A.G. Lactate-mediated glia-neuronal signalling in the mammalian brain. Nat. Commun. 2014, 5:3284.
187. Tekkök S.B., Brown A.M., Westenbroek R., Pellerin L., Ransom B.R. Transfer of glycogen-derived lactate from astrocytes to axons via specific monocarboxylate transporters supports mouse optic nerve activity. J.Neurosci. Res. 2005, 81:644-652.
188. Tomasello M., Call J. Primate Cognition 1997, Oxford University Press, New York.
189. Tsacopoulos M., Magistretti P.J. Metabolic coupling between glia and neurons. J.Neurosci. 1996, 16:877-885.
190. Uddin M., Wildman D.E., Liu G., Xu W., Johnson R.M., Hof P.R., Kapatos G., Grossman L.I., Goodman M. Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. Proc. Natl. Acad. Sci. USA 2004, 101:2957-2962.
191. Vaishnavi S.N., Vlassenko A.G., Rundle M.M., Snyder A.Z., Mintun M.A., Raichle M.E. Regional aerobic glycolysis in the human brain. Proc. Natl. Acad. Sci. USA 2010, 107:17757-17762.
192. van Hall G., Strømstad M., Rasmussen P., Jans O., Zaar M., Gam C., Quistorff B., Secher N.H., Nielsen H.B. Blood lactate is an important energy source for the human brain. J.Cereb. Blood Flow Metab. 2009, 29:1121-1129.
193. Virchow R. Gesammelte Abhandlungen zur Wissenschaftlichen Medizin 1856, Meidinger Sohn, Frankfurt.
194. Virchow R. Die Cellularpathologie in ihrer Begründung auf physiologische and pathologische Gewebelehre 1859, August Hirschwald, Berlin.
195. von Pföstl V., Li J., Zaldivar D., Goense J., Zhang X., Serr N., Logothetis N.K., Rauch A. Effects of lactate on the early visual cortex of non-human primates, investigated by pharmaco-MRI and neurochemical analysis. Neuroimage 2012, 61:98-105.
196. Voutsinos-Porche B., Bonvento G., Tanaka K., Steiner P., Welker E., Chatton J.Y., Magistretti P.J., Pellerin L. Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex. Neuron 2003, 37:275-286.
197. Voutsinos-Porche B., Knott G., Tanaka K., Quairiaux C., Welker E., Bonvento G. Glial glutamate transporters and maturation of the mouse somatosensory cortex. Cereb. Cortex 2003, 13:1110-1121.
198. Wang D., Pascual J.M., Yang H., Engelstad K., Mao X., Cheng J., Yoo J., Noebels J.L., De Vivo D.C. A mouse model for Glut-1 haploinsufficiency. Hum. Mol. Genet. 2006, 15:1169-1179.
199. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
200. Ward P.S., Thompson C.B. Metabolic reprogramming: a cancer hallmark even Warburg did not anticipate. Cancer Cell 2012, 21:297-308.
201. Wyss M.T., Jolivet R., Buck A., Magistretti P.J., Weber B. Invivo evidence for lactate as a neuronal energy source. J.Neurosci. 2011, 31:7477-7485.
202. Yang J., Ruchti E., Petit J.M., Jourdain P., Grenningloh G., Allaman I., Magistretti P.J. Lactate promotes plasticity gene expression by potentiating NMDA signaling in neurons. Proc. Natl. Acad. Sci. USA 2014, 111:12228-12233.
203. Yu N., Martin J.L., Stella N., Magistretti P.J. Arachidonic acid stimulates glucose uptake in cerebral cortical astrocytes. Proc. Natl. Acad. Sci. USA 1993, 90:4042-4046.
204. Zhang Y., Chen K., Sloan S.A., Bennett M.L., Scholze A.R., O'Keeffe S., Phatnani H.P., Guarnieri P., Caneda C., Ruderisch N., et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J.Neurosci. 2014, 34:11929-11947.