Brain lactate metabolism: The discoveries and the controversies

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 7, 2012, Pages 1107-1138

  Dienel, Gerald A ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Astrocyte; brain activation; glucose; lactate shuttling; metabolism; neuron

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 3; GLUTAMIC ACID; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 2;

AEROBIC METABOLISM; AMINO ACID TRANSPORT; ASTROCYTE; BRAIN BLOOD FLOW; BRAIN METABOLISM; BRAIN OXYGEN CONSUMPTION; CELL RESPIRATION; DENDRITIC SPINE; GLUCOSE TRANSPORT; GLYCOGENOLYSIS; GLYCOLYSIS; HUMAN; NERVE CELL CULTURE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPTOSOME;

ANIMALS; BRAIN; ENERGY METABOLISM; HUMANS; LACTIC ACID;

EID: 84863464112     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2011.175     Document Type: Review

References (240)

1. Ackermann RF, Lear JL (1989) Glycolysis-induced discordance between glucose metabolic rates measured with radiolabeled fluorodeoxyglucose and glucose. J Cereb Blood Flow Metab 9:774-85 (Pubitemid 20006897)
2. Adachi K, Cruz NF, Sokoloff L, Dienel GA (1995) Labeling of metabolic pools by [6-14C]glucose during K+-induced stimulation of glucose utilization in rat brain. J Cereb Blood Flow Metab 15:97-110
3. Alano CC, Tran A, Tao R, Ying W, Karliner JS, Swanson RA (2007) Differences among cell types in NAD(+) compartmentalization: a comparison of neurons, astrocytes, and cardiac myocytes. J Neurosci Res 85:3378-85 (Pubitemid 350058526)
4. Allen NJ, Káradó ttir R, Attwell D (2005) A preferential role for glycolysis in preventing the anoxic depolarization of rat hippocampal area CA1 pyramidal cells. J Neurosci 25:848-59 (Pubitemid 40171000)
5. Almeida A, Almeida J, Bolañ os JP, Moncada S (2001) Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc Natl Acad Sci USA 98: 15294-9 (Pubitemid 34014008)
6. Almeida A, Moncada S, Bolañ os JP (2004) Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway. Nat Cell Biol 6:45-51 (Pubitemid 38425729)
7. Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133-45 (Pubitemid 32947479)
8. Aubert A, Costalat R (2007) Compartmentalization of brain energy metabolism between glia and neurons: insights from mathematical modeling. Glia 55:1272-9 (Pubitemid 47235368)
9. Aubert A, Costalat R, Magistretti PJ, Pellerin L (2005) Brain lactate kinetics: modeling evidence for neuronal lactate uptake upon activation. Proc Natl Acad Sci USA 102:16448-53
10. Aubert A, Pellerin L, Magistretti PJ, Costalat R (2007) A coherent neurobiological framework for functional neuroimaging provided by a model integrating compartmentalized energy metabolism. Proc Natl Acad Sci USA 104:4188-93 (Pubitemid 47181600)
11. Bak LK, Walls AB, Schousboe A, Ring A, Sonnewald U, Waagepetersen HS (2009) Neuronal glucose but not lactate utilization is positively correlated with NMDAinduced neurotransmission and fluctuations in cytosolic Ca2+ levels. J Neurochem 109(Suppl 1):87-93
12. Balázs R, Cremer JE (1972) Metabolic Compartmentation in the Brain (eds) New York: John Wiley & Sons
13. Ball KK, Cruz NF, Mrak RE, Dienel GA (2010) Trafficking of glucose, lactate, and amyloid-beta from the inferior colliculus through perivascular routes. J Cereb Blood Flow Metab 30:162-76
14. Ball KK, Gandhi GK, Thrash J, Cruz NF, Dienel GA (2007) Astrocytic connexin distributions and rapid, extensive dye transfer via gap junctions in the inferior colliculus: Implications for [14C]glucose metabolite trafficking. J Neurosci Res 85:3267-83 (Pubitemid 350058515)
15. Baquer NZ, McLean P, Greenbaum AL (1975) Systems relationships and control of metabolic pathways in developing brain. In: Normal and pathological development of energy metabolism. (Hommes FA, van den Berg CJ, eds), London: Academic Press, 109-31
16. Barros LF, Deitmer JW (2010) Glucose and lactate supply to the synapse. Brain Res Rev 63:149-59
17. Bergersen L, Rafiki A, Ottersen OP (2002) Immunogold cytochemistry identifies specialized membrane domains for monocarboxylate transport in the central nervous system. Neurochem Res 27:89-96 (Pubitemid 34242435)
18. Bergersen L, Waerhaug O, Helm J, Thomas M, Laake P, Davies AJ,Wilson MC, Halestrap AP, Ottersen OP (2001) A novel postsynaptic density protein: the monocarboxylate transporter MCT2 is co-localized with delta-glutamate receptors in postsynaptic densities of parallel fiber-Purkinje cell synapses. Exp Brain Res 136:523-34 (Pubitemid 32193853)
19. Bergersen LH (2007) Is lactate food for neurons? Comparison of monocarboxylate transporter subtypes in brain and muscle. Neuroscience 145:11-9 (Pubitemid 46237686)
20. Bergersen LH, Magistretti PJ, Pellerin L (2005) Selective postsynaptic co-localization of MCT2 with AMPA receptor GluR2/3 subunits at excitatory synapses exhibiting AMPA receptor trafficking. Cereb Cortex 15:361-70 (Pubitemid 40388236)
21. Bittner CX, Valdebenito R, Ruminot I, Loaiza A, Larenas V, Sotelo-Hitschfeld T, Moldenhauer H, San Martín A, Gutiérrez R, Zambrano M, Barros LF (2011) Fast and reversible stimulation of astrocytic glycolysis by K+ and a delayed and persistent effect of glutamate. J Neurosci 31:4709-13
22. Blomqvist G, Stone-Elander S, Halldin C, Roland PE, Widén L, Lindqvist M, Swahn CG, La°ngström B, Wiesel FA (1990) Positron emission tomographic measurements of cerebral glucose utilization using [1-11C]Dglucose. J Cereb Blood Flow Metab 10:467-83 (Pubitemid 20209193)
23. Bolañ os JP, Almeida A (2010) The pentose-phosphate pathway in neuronal survival against nitrosative stress. IUBMB Life 62:14-8
24. Bonavita V, Guarneri R, Amore G (1970) Nicotinamide adenine dinucleotides in the convulsant rat brain. J Neurochem 17:1613-4
25. Borgström L, Chapman AG, SiesjöBK (1976) Glucose consumption in the cerebral cortex of rat during bicuculline-induced status epilipticus. J Neurochem 27:971-3
26. Boumezbeur F, Petersen KF, Cline GW, Mason GF, Behar KL, Shulman GI, Rothman DL (2010) The contribution of blood lactate to brain energy metabolism in humans measured by dynamic 13C nuclear magnetic resonance spectroscopy. J Neurosci 30:13983-91
27. Bourne JN, Harris KM (2008) Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47-67
28. Bouzier-Sore AK, Voisin P, Bouchaud V, Bezancon E, Franconi JM, Pellerin L (2006) Competition between glucose and lactate as oxidative energy substrates in both neurons and astrocytes: a comparative NMR study. Eur J Neurosci 24:1687-94 (Pubitemid 44427537)
29. Bouzier-Sore AK, Voisin P, Canioni P, Magistretti PJ, Pellerin L (2003) Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J Cereb Blood Flow Metab 23:1298-306 (Pubitemid 37409793)
30. Bradford HF (1975) Isolated nerve terminals as an in vitro preparation for the study of dynamic aspects of transmitter metabolism and release. In: Handbook of Psychopharmacology. Vol. 1, Biochemical Principles and Techniques in Neuropharmacology (Iversen LL, Iverseh SD, Snyder SH, eds), New York, NY: Plenum Press, 191-252
31. Bradford HF, Ward HK, Thomas AJ (1978) Glutamine-a major substrate for nerve endings. J Neurochem 30: 1453-9 (Pubitemid 8377490)
32. Brennan AM, Connor JA, Shuttleworth CW (2006) NAD(P)H fluorescence transients after synaptic activity in brain slices: predominant role of mitochondrial function. J Cereb Blood Flow Metab 26:1389-406 (Pubitemid 44629887)
33. Bröer S, Bröer A, Schneider HP, Stegen C, Halestrap AP, Deitmer JW (1999) Characterization of the high-affinity monocarboxylate transporter MCT2 in Xenopus laevis oocytes. Biochem J 341:529-35 (Pubitemid 29389181)
34. Caesar K, Hashemi P, Douhou A, Bonvento G, Boutelle MG, Walls AB, Lauritzen M (2008) Glutamate receptordependent increments in lactate, glucose and oxygen metabolism evoked in rat cerebellum in vivo. J Physiol 586:1337-49 (Pubitemid 351321272)
35. Calvetti D, Somersalo E (2011) Dynamic activation model for a glutamatergic neurovascular unit. J Theor Biol 274:12-29
36. Cerdán S, Rodrigues TB, Sierra A, Benito M, Fonseca LL, Fonseca CP, García-Martín ML (2006) The redox switch/redox coupling hypothesis. Neurochem Int 48:523-30
37. Chatton JY, Pellerin L, Magistretti PJ (2003) GABA uptake into astrocytes is not associated with significant metabolic cost: implications for brain imaging of inhibitory transmission. Proc Natl Acad Sci USA 100: 12456-61
38. Chih CP, Lipton P, Roberts Jr EL (2001) Do active cerebral neurons really use lactate rather than glucose? Trends Neurosci 24:573-8 (Pubitemid 32913386)
39. Chih CP, Roberts Jr EL (2003) Energy substrates for neurons during neural activity: a critical review of the astrocyteneuron lactate shuttle hypothesis. J Cereb Blood Flow Metab 23:1263-81 (Pubitemid 37409789)
40. Choi SW, Gerencser AA, Lee DW, Rajagopalan S, Nicholls DG, Andersen JK, Brand MD (2011) Intrinsic bioenergetic properties and stress sensitivity of dopaminergic synaptosomes. J Neurosci 31:4524-34
41. Choi SW, Gerencser AA, Nicholls DG (2009) Bioenergetic analysis of isolated cerebrocortical nerve terminals on a microgram scale: spare respiratory capacity and stochastic mitochondrial failure. J Neurochem 109: 1179-91
42. Collins RC, McCandless DW, Wagman IL (1987) Cerebral glucose utilization: comparison of [14C]deoxyglucose and [6-14C]glucose quantitative autoradiography. J Neurochem 49:1564-70 (Pubitemid 17161380)
43. Contreras L, Satrú stegui J (2009) Calcium signaling in brain mitochondria: interplay of malate aspartate NADH shuttle and calcium uniporter/mitochondrial dehydrogenase pathways. J Biol Chem 284:7091-9
44. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990a) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247:470-3
45. Cornell-Bell AH, Thomas PG, Smith SJ (1990b) The excitatory neurotransmitter glutamate causes filopodia formation in cultured hippocampal astrocytes. Glia 3:322-34
46. Costa Leite T, Da Silva D, Guimarães Coelho R, Zancan P, Sola-Penna M (2007) Lactate favours the dissociation of skeletal muscle 6-phosphofructo-1-kinase tetramers down-regulating the enzyme and muscle glycolysis. Biochem J 408:123-30 (Pubitemid 350158410)
47. Cremer JE (1964) Amino acid metabolism in rat brain studied with 14C-labelled glucose. J Neurochem 11: 165-85
48. Cremer JE (1982) Substrate utilization and brain development. J Cereb Blood Flow Metab 2:394-407 (Pubitemid 13168816)
49. Cremer JE, Cunningham VJ, Seville MP (1983) Relationships between extraction and metabolism of glucose, blood flow, and tissue blood volume in regions of rat brain. J Cereb Blood Flow Metab 3:291-302 (Pubitemid 13017777)
50. Cruz F, Villalba M, García-Espinosa MA, Ballesteros P, Bogónez E, Satrú stegui J, Cerdán S (2001) Intracellular compartmentation of pyruvate in primary cultures of cortical neurons as detected by (13)C NMR spectroscopy with multiple (13)C labels. J Neurosci Res 66:771-81
51. Cruz NF, Adachi K, Dienel GA (1999) Metabolite trafficking during K+-induced spreading cortical depression: rapid efflux of lactate from cerebral cortex. J Cereb Blood Flow Metab 19:380-92 (Pubitemid 30161226)
52. Cruz NF, Ball KK, Dienel GA (2007) Imaging focal brain activation in conscious rats: metabolite spreading and release contribute to underestimation of glucose utilization with [14C]glucose. J Neurosci Res 85:3254-66 (Pubitemid 350058514)
53. Cruz NF, Dienel GA (2002) High brain glycogen levels in brains of rats with minimal environmental stimuli: Implications for metabolic contributions of working astrocytes. J Cereb Blood Flow Metab 22:1476-89 (Pubitemid 35424932)
54. Cruz NF, Lasater A, Zielke HR, Dienel GA (2005) Activation of astrocytes in brain of conscious rats during acoustic stimulation: acetate utilization in working brain. J Neurochem 92:934-47 (Pubitemid 40229566)
55. Dalsgaard MK (2006) Fuelling cerebral activity in exercising man. J Cereb Blood Flow Metab 26:731-50
56. Debernardi R, Magistretti PJ, Pellerin L (1999) Transinhibition of glutamate transport prevents excitatory amino acid-induced glycolysis in astrocytes. Brain Res 850:39-46
57. Diamond I, Fishman RA (1973) Development of Na+-stimulated glucose oxidation in synaptosomes. J Neurochem 21:1043-50
58. Dienel GA, Ball KK, Cruz NF (2007a) 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 102:466-78 (Pubitemid 47000604)
59. Dienel GA, Cruz NF (2003) Neighborly interactions of metabolically- activated astrocytes in vivo. Neurochem Int 43:339-54 (Pubitemid 36561287)
60. Dienel GA, Cruz NF (2004) Nutrition during brain activation: does cell-to-cell lactate shuttling contribute significantly to sweet and sour food for thought? Neurochem Int 45:321-51 (Pubitemid 38625624)
61. Dienel GA, Cruz NF (2006) Astrocyte activation in working brain: energy supplied by minor substrates. Neurochem Int 48:586-95
62. Dienel GA, Cruz NF (2008) Imaging brain activation: simple pictures of complex biology. Ann NY Acad Sci 1147:139-70
63. Dienel GA, Cruz NF (2009) Exchange-mediated dilution of brain lactate specific activity: implications for the origin of glutamate dilution and the contributions of glutamine dilution and other pathways. J Neurochem 109(Suppl 1):30-7
64. Dienel GA, Cruz NF, Ball K, Popp D, Gokden M, Baron S, Wright D, Wenger GR (2003) Behavioral training increases local astrocytic metabolic activity but does not alter outcome of mild transient ischemia. Brain Res 961:201-12 (Pubitemid 36071581)
65. Dienel GA, Hertz L (2001) Glucose and lactate metabolism during brain activation. J Neuroscience Res 66:824-38
66. Dienel GA, Hertz L (2005) Astrocytic contributions to bioenergetics of cerebral ischemia. Glia 50:362-88 (Pubitemid 40780841)
67. Dienel GA, Liu K, Cruz NF (2001) Local uptake of (14)Clabeled acetate and butyrate in rat brain in vivo during spreading cortical depression. J Neurosci Res 66:812-20
68. Dienel GA, Schmidt KC, Cruz NF (2007b) Astrocyte activation in vivo during graded photic stimulation. J Neurochem 103:1506-22 (Pubitemid 47631813)
69. Dienel GA, Wang RY, Cruz NF (2002) Generalized sensory stimulation of conscious rats increases labeling of oxidative pathways of glucose metabolism when the brain glucose-oxygen uptake ratio rises. J Cereb Blood Flow Metab 22:1490-502 (Pubitemid 35424933)
70. DiNuzzo M, Mangia S, Maraviglia B, Giove F (2010a) Changes in glucose uptake rather than lactate shuttle take center stage in subserving neuroenergetics: evidence from mathematical modeling. J Cereb Blood Flow Metab 30:586-602
71. DiNuzzo M, Mangia S, Maraviglia B, Giove F (2010b) Glycogenolysis in astrocytes supports blood-borne glucose channeling not glycogen-derived lactate shuttling to neurons: evidence from mathematical modeling. J Cereb Blood Flow Metab 30:1895-904
72. Dringen R, Gebhardt R, Hamprecht B (1993) Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res 623:208-14 (Pubitemid 23275402)
73. Duarte JM, Lanz B, Gruetter R (2011) Compartmentalized cerebral metabolism of [1,6-C]glucose determined by in vivo 13C NMR spectroscopy at 14.1 T. Front Neuroenergetics 3:3
74. Duffy TE, Howse DC, Plum F (1975) Cerebral energy metabolism during experimental status epilepticus. J Neurochem 24:925-34
75. Ereciń ska M, Nelson D, Chance B (1991) Depolarizationinduced changes in cellular energy production. Proc Natl Acad Sci USA 88:7600-4 (Pubitemid 21915201)
76. Ereciń ska M, Nelson D, Silver IA (1996) Metabolic and energetic properties of isolated nerve ending particles (synaptosomes). Biochim Biophys Acta 1277:13-34 (Pubitemid 26388873)
77. Ereciń ska M, Nelson D, Vanderkooi JM (1995) Effects of NO-generating compounds on synaptosomal energy metabolism. J Neurochem 65:2699-705
78. Eriksson G, Peterson A, Iverfeldt K, Walum E (1995) Sodium-dependent glutamate uptake as an activator of oxidative metabolism in primary astrocyte cultures from newborn rat. Glia 15:152-6
79. Erlichman JS, Hewitt A, Damon TL, Hart M, Kurascz J, Li A, Leiter JC (2008) Inhibition of monocarboxylate transporter 2 in the retrotrapezoid nucleus in rats: a test of the astrocyte-neuron lactate-shuttle hypothesis. J Neurosci 28:4888-96
80. Ferreira JM, Burnett AL, Rameau GA (2011) Activitydependent regulation of surface glucose transporter-3. J Neurosci 31:1991-9
81. Fox PT, Raichle ME (1986) Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc Natl Acad Sci USA 83:1140-4 (Pubitemid 16086428)
82. Fox PT, Raichle ME, Mintun MA, Dence C (1988) Nonoxidative glucose consumption during focal physiologic neural activation. Science 241:462-4
83. Galeffi F, Foster KA, Sadgrove MP, Beaver CJ, Turner DA (2007) Lactate uptake contributes to the NAD(P)H biphasic response and tissue oxygen response during synaptic stimulation in area CA1 of rat hippocampal slices. J Neurochem 103:2449-61 (Pubitemid 350173574)
84. Gandhi GK, Ball KK, Cruz NF, Dienel GA (2010) Hyperglycaemia and diabetes impair gap junctional communication among astrocytes. ASN Neuro 2:e00030
85. Gandhi GK, Cruz NF, Ball KK, Dienel GA (2009) Astrocytes are poised for lactate trafficking and release from activated brain and for supply of glucose to neurons. J Neurochem 111:522-36
86. Garofalo O, Cox DW, Bachelard HS (1988) Brain levels of NADH and NAD+ under hypoxic and hypoglycaemic conditions in vitro. J Neurochem 51:172-6
87. Gleichmann M, Collis LP, Smith PJ, Mattson MP (2009) Simultaneous single neuron recording of O2 consumption, [Ca2+]i and mitochondrial membrane potential in glutamate toxicity. J Neurochem 109:644-55
88. Gleitz J, Beile A, Khan S, Wilffert B, Tegtmeier F (1993) Anaerobic glycolysis and postanoxic recovery of respiration of rat cortical synaptosomes are reduced by synaptosomal sodium load. Brain Res 611:286-94 (Pubitemid 23159697)
89. Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456:745-9
90. Gramsbergen JB, Leegsma-Vogt G, Venema K, Noraberg J, Korf J (2003) Quantitative on-line monitoring of hippocampus glucose and lactate metabolism in organotypic cultures using biosensor technology. J Neurochem 85:399-408 (Pubitemid 36438335)
91. Halestrap AP (1975) The mitochondrial pyruvate carrier. Kinetics and specificity for substrates and inhibitors. Biochem J 148:85-96
92. Halestrap AP, Denton RM (1974) Specific inhibition of pyruvate transport in rat liver mitochondria and human erythrocytes by alpha-cyano-4- hydroxycinnamate. Biochem J 138:313-6
93. Halestrap AP, Denton RM (1975) The specificity and metabolic implications of the inhibition of pyruvate transport in isolated mitochondria and intact tissue preparations by alpha-cyano-4-hydroxycinnamate and related compounds. Biochem J 148:97-106
94. Hargreaves RJ, Planas AM, Cremer JE, Cunningham VJ (1986) Studies on the relationship between cerebral glucose transport and phosphorylation using 2-deoxyglucose. J Cereb Blood Flow Metab 6:708-16 (Pubitemid 17226448)
95. Harvey SA, Booth RF, Clark JB (1982) The effects in vitro of hypoglycaemia and recovery from anoxia on synaptosomal metabolism. Biochem J 206:433-9 (Pubitemid 13199515)
96. Hawkins RA, Miller AL, Nielsen RC, Veech RL (1973) The acute action of ammonia on rat brain metabolism in vivo. Biochem J 134:1001-8
97. Hawkins RA, Williamson DH, Krebs HA (1971) Ketonebody utilization by adult and suckling rat brain in vivo. Biochem J 122:13-8
98. Hein TW, Xu W, Kuo L (2006) Dilation of retinal arterioles in response to lactate: role of nitric oxide, guanylyl cyclase, and ATP-sensitive potassium channels. Invest Ophthalmol Vis Sci 47:693-9 (Pubitemid 46768399)
99. Herrero-Mendez A, Almeida A, Fernández E, Maestre C, Moncada S, Bolañ os JP (2009) The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/CCdh1. Nat Cell Biol 11:747-52
100. Hertz L (2004) The astrocyte-neuron lactate shuttle: a challenge of a challenge. J Cereb Blood Flow Metab 24:1241-8 (Pubitemid 39482486)
101. Hertz L (2011) Astrocytic energy metabolism and glutamate formation-relevance for (13)C-NMR spectroscopy and importance of cytosolic/mitochondrial trafficking. Magn Reson Imaging Epub [ahead of print]
102. Hertz L, Drejer J, Schousboe A (1988) Energy metabolism in glutamatergic neurons, GABAergic neurons and astrocytes in primary cultures. Neurochem Res 13:605-10
103. Hertz L, Swanson RA, Newman GC, Marrif H, Juurlink BH, Peng L (1998) Can experimental conditions explain the discrepancy over glutamate stimulation of aerobic glycolysis? Dev Neurosci 20:339-47 (Pubitemid 28495528)
104. Hertz L, Peng L, Dienel GA (2007) Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J Cereb Blood Flow Metab 27:219-49 (Pubitemid 46148451)
105. Howse DC, Duffy TE (1975) Control of the redox state of the pyridine nucleotides in the rat cerebral cortex. Effect of electroshock-induced seizures. J Neurochem 24:935-40
106. Hu Y, Wilson GS (1997a) Rapid changes in local extracellular rat brain glucose observed with an in vivo glucose sensor. J Neurochem 68:1745-52 (Pubitemid 27133086)
107. Hu Y, Wilson GS (1997b) A temporary local energy pool coupled to neuronal activity: fluctuations of extracellular lactate levels in rat brain monitored with rapid-response enzyme-based sensor. J Neurochem 69:1484-90 (Pubitemid 27406949)
108. 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 26:865-77 (Pubitemid 43980402)
109. Ide K, Horn A, Secher NH (1999) Cerebral metabolic response to submaximal exercise. J Appl Physiol 87: 1604-8
110. Ide K, Schmalbruch IK, Quistorff B, Horn A, Secher NH (2000) Lactate, glucose and O2 uptake in human brain during recovery from maximal exercise. J Physiol 522: 159-64 (Pubitemid 30052778)
111. Ide T, Steinke J, Cahill Jr GF (1969) Metabolic interactions of glucose, lactate, and beta-hydroxybutyrate in rat brain slices. Am J Physiol 217:784-92
112. Ikemoto A, Bole DG, Ueda T (2003) Glycolysis and glutamate accumulation into synaptic vesicles. Role of glyceraldehyde phosphate dehydrogenase and 3-phosphoglycerate kinase. J Biol Chem 278:5929-40 (Pubitemid 36800840)
113. Ivannikov MV, Sugimori M, Llinás RR (2010) Calcium clearance and its energy requirements in cerebellar neurons. Cell Calcium 47:507-13
114. Jameson N, Olson J, Nguyen H, Holtzman D (1984) Respiration in primary cultured cerebellar granule neurons and cerebral cortical neurons. J Neurochem 42:470-4 (Pubitemid 14185598)
115. Jekabsons MB, Nicholls DG (2004) In situ respiration and bioenergetic status of mitochondria in primary cerebellar granule neuronal cultures exposed continuously to glutamate. J Biol Chem 279:32989-3000 (Pubitemid 39014759)
116. Jolivet R, Allaman I, Pellerin L, Magistretti PJ, Weber B (2010) Comment on recent modeling studies of astrocyte-neuron metabolic interactions. J Cereb Blood Flow Metab 30:1982-6
117. Joyce OJ, Farmer MK, Tipton KF, Porter RK (2003) Oxidative phosphorylation by in situ synaptosomal mitochondria from whole brain of young and old rats. J Neurochem 86:1032-41 (Pubitemid 36992217)
118. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305:99-103 (Pubitemid 38869381)
119. Kauppinen RA, Nicholls DG (1986a) Failure to maintain glycolysis in anoxic nerve terminals. J Neurochem 47:1864-9 (Pubitemid 17191503)
120. Kauppinen RA, Nicholls DG (1986b) Synaptosomal bioenergetics. The role of glycolysis, pyruvate oxidation and responses to hypoglycaemia. Eur J Biochem 158: 159-65 (Pubitemid 16066517)
121. Kauppinen RA, Taipale HT, Komulainen H (1989) Interrelationships between glucose metabolism, energy state, and the cytosolic free calcium concentration in cortical synaptosomes from the guinea pig. J Neurochem 53:766-71 (Pubitemid 19207371)
122. Kemppainen J, Aalto S, Fujimoto T, Kalliokoski KK, La°ngsjöJ, Oikonen V, Rinne J, Nuutila P, Knuuti J (2005) High intensity exercise decreases global brain glucose uptake in humans. J Physiol 568:323-32 (Pubitemid 41448641)
123. Korf J, de Boer J (1990) Lactography as an approach to monitor glucose metabolism on-line in brain and muscle. Int J Biochem 22:1371-8 (Pubitemid 20370317)
124. Krebs HA (1972) The Pasteur effect and the relations between respiration and fermentation. Essays Biochem 8:1-34
125. Krivanek J (1958) Changes of brain glycogen in the spreading EEG-depression of Leao. J Neurochem 2:337-43
126. Krzanowski J, Matschinsky FM (1969) Regulation of phosphofructokinase by phosphocreatine and phosphorylated glycolytic intermediates. Biochem Biophys Res Commun 34:816-23
127. Ksiezak HJ, Gibson GE (1981a) Acetylcholine synthesis and CO2 production from variously labeled glucose in rat brain slices and synaptosomes. J Neurochem 37: 88-94 (Pubitemid 11003479)
128. Ksiezak HJ, Gibson GE (1981b) Oxygen dependence of glucose and acetylcholine metabolism in slices and synaptosomes from rat brain. J Neurochem 37:305-14 (Pubitemid 11059442)
129. LaManna JC, Salem N, Puchowicz M, Erokwu B, Koppaka S, Flask C, Lee Z (2009) Ketones suppress brain glucose consumption. Adv Exp Med Biol 645:301-6
130. Lavialle M, Aumann G, Anlauf E, Pröls F, Arpin M, Derouiche A (2011) Structural plasticity of perisynaptic astrocyte processes involves ezrin and metabotropic glutamate receptors. Proc Natl Acad Sci USA 108: 12915-9
131. Lear J (1990) Glycolysis: link between PET and proton MR spectroscopic studies of the brain. Radiology 174:328-30 (Pubitemid 20038582)
132. Lear J, Ackermann RF (1989) Why the deoxyglucose method has proven so useful in cerebral activation studies: the unappreciated prevalence of stimulationinduced glycolysis. J Cereb Blood Flow Metab 9:911-3 (Pubitemid 20006914)
133. Lee DH, Chung MY, Lee JU, Kang DG, Paek YW (2000) Changes of glucose transporters in the cerebral adaptation to hypoglycemia. Diabetes Res Clin Pract 47:15-23
134. Leino RL, Gerhart DZ, van Bueren AM, McCall AL, Drewes LR (1997) Ultrastructural localization of GLUT 1 and GLUT 3 glucose transporters in rat brain. J Neurosci Res 49:617-26 (Pubitemid 27381249)
135. Li Z, Okamoto K, Hayashi Y, Sheng M (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119: 873-87 (Pubitemid 40017692)
136. Liao SL, Chen CJ (2003) L-glutamate decreases glucose utilization by rat cortical astrocytes. Neurosci Lett 348: 81-4
137. Linde R, Schmalbruch IK, Paulson OB, Madsen PL (1999) The Kety-Schmidt technique for repeated measurements of global cerebral blood flow and metabolism in the conscious rat. Acta Physiol Scand 165:395-401 (Pubitemid 29224646)
138. Loaiza A, Porras OH, Barros LF (2003) Glutamate triggers rapid glucose transport stimulation in astrocytes as evidenced by real-time confocal microscopy. J Neurosci 23:7337-42 (Pubitemid 36999523)
139. Lovatt D, Sonnewald U, Waagepetersen HS, Schousboe A, He W, Lin JH, Han X, Takano T, Wang S, Sim FJ, Goldman SA, Nedergaard M (2007) The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J Neurosci 27:12255-66
140. Lowry OH, Passonneau JV (1966) Kinetic evidence for multiple binding sites on phosphofructokinase. J Biol Chem 241:2268-79
141. Lowry OH, Passonneau JV, Hasselberger FX, Schulz DW (1964) Effect of ischemia on known substrates and cofactors of the glycolytic pathway in brain. J Biol Chem 239:18-30
142. Madsen PL, Cruz NF, Sokoloff L, Dienel GA (1999) Cerebral oxygen/glucose ratio is low during sensory stimulation and rises above normal during recovery: excess glucose consumption during stimulation is not accounted for by lactate efflux from or accumulation in brain tissue. J Cereb Blood Flow Metab 19:393-400 (Pubitemid 30161227)
143. Madsen PL, Hasselbalch SG, Hagemann LP, Olsen KS, Bülow J, Holm S, Wildschiødtz G, Paulson OB, Lassen NA (1995) Persistent resetting of the cerebral oxygen/glucose uptake ratio by brain activation: evidence obtained with the Kety-Schmidt technique. J Cereb Blood Flow Metab 15:485-91
144. Madsen PL, Linde R, Hasselbalch SG, Paulson OB, Lassen NA (1998) Activation-induced resetting of cerebral oxygen and glucose uptake in the rat. J Cereb Blood Flow Metab 18:742-8 (Pubitemid 28307629)
145. Magistretti PJ (2009) Role of glutamate in neuron-glia metabolic coupling. Am J Clin Nutr 90:875S-80S
146. Maher F, Simpson IA (1994) Modulation of expression of glucose transporters GLUT3 and GLUT1 by potassium and N-methyl-D-aspartate in cultured cerebellar granule neurons. Mol Cell Neurosci 5:369-75 (Pubitemid 24264577)
147. Malthankar-Phatak GH, Patel AB, Xia Y, Hong S, Chowdhury GM, Behar KL, Orina IA, Lai JC (2008) Effects of continuous hypoxia on energy metabolism in cultured cerebro-cortical neurons. Brain Res 1229:147-54
148. Mangia S, DiNuzzo M, Giove F, Carruthers A, Simpson IA, Vannucci SJ (2011) Response to 'comment on recent modeling studies of astrocyte-neuron metabolic interactions': much ado about nothing. J Cereb Blood Flow Metab 31:1346-53
149. Mangia S, Giove F, Tkác I, Logothetis NK, Henry PG, Olman CA, Maraviglia B, Di Salle F, Uǧurbil K (2009a) Metabolic and hemodynamic events after changes in neuronal activity: current hypotheses, theoretical predictions and in vivo NMR experimental findings. J Cereb Blood Flow Metab 29:441-63
150. Mangia S, Simpson IA, Vannucci SJ, Carruthers A (2009b) The in vivo neuron-to-astrocyte lactate shuttle in human brain: evidence from modeling of measured lactate levels during visual stimulation. J Neurochem 109(Suppl 1):55-62
151. Mangia S, Tkác I, Logothetis NK, Gruetter R, Van de Moortele PF, Uǧurbil K (2007) Dynamics of lactate concentration and blood oxygen level-dependent effect in the human visual cortex during repeated identical stimuli. J Neurosci Res 85:3340-6 (Pubitemid 350058522)
152. Mason GF, Rothman DL (2004) Basic principles of metabolic modeling of NMR (13)C isotopic turnover to determine rates of brain metabolism in vivo. Metab Eng 6:75-84 (Pubitemid 38157797)
153. McKenna MC, Hopkins IB, Carey A (2001) Alpha-cyano-4-hydroxycinnamate decreases both glucose and lactate metabolism in neurons and astrocytes: implications for lactate as an energy substrate for neurons. J Neurosci Res 66:747-54
154. McKenna MC, Sonnewald U, Huang X, Stevenson J, Zielke HR (1996) Exogenous glutamate concentration regulates the metabolic fate of glutamate in astrocytes. J Neurochem 66:386-93 (Pubitemid 26010804)
155. Medina MA, Deam AP, Stavinoha WB (1980) Inactivation of brain tissue by microwave irradiation. In: Cerebral metabolism and neural function (Passonneau JV, Hawkins RA, Lust WD, Welsh FA, eds), Baltimore: Williams & Wilkins, 56-69
156. Meldrum BS, Nilsson B (1976) Cerebral blood flow and metabolic rate early and late in prolonged epileptic seizures induced in rats by bicuculline. Brain 99:523-42
157. Miller AL, Hawkins RA, Veech RL (1973) The mitochondrial redox state of rat brain. J Neurochem 20:1393-400
158. Minervini M, Atlante A, Gagliardi S, Ciotti MT, Marra E, Calissano P (1997) Glutamate stimulates 2-deoxyglucose uptake in rat cerebellar granule cells. Brain Res 768: 57-62 (Pubitemid 27433477)
159. Nicholls DG (2003) Bioenergetics and transmitter release in the isolated nerve terminal. Neurochem Res 28: 1433-41 (Pubitemid 37193525)
160. Nicholls DG (2009) Spare respiratory capacity, oxidative stress and excitotoxicity. Biochem Soc Trans 37:1385-8
161. Nicholls DG (2010) Mitochondrial ion circuits. Essays Biochem 47:25-35
162. Occhipinti R, Somersalo E, Calvetti D (2010) Energetics of inhibition: insights with a computational model of the human GABAergic neuron-astrocyte cellular complex. J Cereb Blood Flow Metab 30:1834-46
163. Okada Y, Lipton P (2007) Glucose, oxidative energy metabolism and neural function in brain slices-glycolysis plays a key role in neural activity. In: Brain energetics. Integration of molecular and cellular processes (Gibson GE, Dienel GA, eds), Berlin: Springer-Verlag, 17-39
164. O'Neal RM, Koeppe RE (1966) Precursors in vivo of glutamate, aspartate and their derivatives of rat brain. J Neurochem 13:835-47
165. Orzi F, Lucignani G, Dow-Edwards D, Namba H, Nehlig A, Patlak CS, Pettigrew K, Schuier F, Sokoloff L (1988) Local cerebral glucose utilization in controlled graded levels of hyperglycemia in the conscious rat. J Cereb Blood Flow Metab 8:346-56
166. Owen OE, Morgan AP, Kemp HG, Sullivan JM, Herrera MG, Cahill Jr GF (1967) Brain metabolism during fasting. J Clin Invest 46:1589-95
167. Öz G, Berkich DA, Henry PG, Xu Y, LaNoue K, Hutson SM, Gruetter R (2004) Neuroglial metabolism in the awake rat brain: CO2 fixation increases with brain activity. J Neurosci 24:11273-9 (Pubitemid 39658262)
168. Pardo B, Contreras L, Serrano A, Ramos M, Kobayashi K, Iijima M, Saheki T, Satrú stegui J (2006) Essential role of aralar in the transduction of small Ca2+ signals to neuronal mitochondria. J Biol Chem 281:1039-47
169. Pardo B, Rodrigues TB, Contreras L, Garzón M, Llorente-Folch I, Kobayashi K, Saheki T, Cerdan S, Satrú stegui J (2011) Brain glutamine synthesis requires neuronalborn aspartate as amino donor for glial glutamate formation. J Cereb Blood Flow Metab 31:90-101
170. Passonneau JV, Lowry OH (1963) P-Fructokinase and the control of the citric acid cycle. Biochem Biophys Res Commun 13:372-9
171. Patel JR, Brewer GJ (2003) Age-related changes in neuronal glucose uptake in response to glutamate and betaamyloid. J Neurosci Res 72:527-36 (Pubitemid 36523427)
172. Pellerin L (2008) Brain energetics (thought needs food). Curr Opin Clin Nutr Metab Care 11:701-5
173. Pellerin L, Bouzier-Sore AK, Aubert A, Serre S, Merle M, Costalat R, Magistretti PJ (2007) Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55:1251-62 (Pubitemid 47235366)
174. Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci 91:10625-9 (Pubitemid 24329051)
175. Peng L, Hertz L (2002) Amobarbital inhibits K(+)-stimulated glucose oxidation in cerebellar granule neurons by two mechanisms. Eur J Pharmacol 446:53-61 (Pubitemid 34722557)
176. Peng L, Swanson RA, Hertz L (2001) Effects of L-glutamate, D-aspartate, and monensin on glycolytic and oxidative glucose metabolism in mouse astrocyte cultures: further evidence that glutamate uptake is metabolically driven by oxidative metabolism. Neurochem Int 38:437-43 (Pubitemid 32166901)
177. Peng L, Zhang X, Hertz L (1994) High extracellular potassium concentrations stimulate oxidative metabolism in a glutamatergic neuronal culture and glycolysis in cultured astrocytes but have no stimulatory effect in a GABAergic neuronal culture. Brain Res 663:168-72 (Pubitemid 24329678)
178. Pieper AA, Blackshaw S, Clements EE, Brat DJ, Krug DK, White AJ, Pinto-Garcia P, Favit A, Conover JR, Snyder SH, Verma A (2000) Poly(ADP-ribosyl)ation basally activated by DNA strand breaks reflects glutamate-nitric oxide neurotransmission. Proc Natl Acad Sci USA 97:1845-50 (Pubitemid 30118531)
179. Pierre K, Chatton JY, Parent A, Repond C, Gardoni F, Di Luca M, Pellerin L (2009) Linking supply to demand: the neuronal monocarboxylate transporter MCT2 and the alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionic acid receptor GluR2/3 subunit are associated in a common trafficking process. Eur J Neurosci 29:1951-63
180. Porras OH, Loaiza A, Barros LF (2004) Glutamate mediates acute glucose transport inhibition in hippocampal neurons. J Neurosci 24:9669-73 (Pubitemid 39441521)
181. Prebil M, Vardjan N, Jensen J, Zorec R, Kreft M (2011) Dynamic monitoring of cytosolic glucose in single astrocytes. Glia 59:903-13
182. Qu H, Eloqayli H, Unsgard G, Sonnewald U (2001) Glutamate decreases pyruvate carboxylase activity and spares glucose as energy substrate in cultured cerebellar astrocytes. J Neurosci Res 66:1127-32 (Pubitemid 33135598)
183. Quistorff B, Grunnet N (2011a) High brain lactate is not caused by a shift in the lactate dehydrogenase A/B ratio. Proc Natl Acad Sci USA 108:E21
184. Quistorff B, Grunnet N (2011b) The isoenzyme pattern of LDH does not play a physiological role; except perhaps during fast transitions in energy metabolism. Aging (Albany NY) 3:457-60
185. Quistorff B, Secher NH, Van Lieshout JJ (2008) Lactate fuels the human brain during exercise. FASEB J 22:3443-9
186. Reagan LP, Magariñ os AM, Lucas LR, van Bueren A, McCall AL, McEwen BS (1999) Regulation of GLUT-3 glucose transporter in the hippocampus of diabetic rats subjected to stress. Am J Physiol 276:E879-86 (Pubitemid 29249607)
187. Reichenbach A, Derouiche A, Kirchhoff F (2010) Morphology and dynamics of perisynaptic glia. Brain Res Rev 63:11-25
188. Robinson AM,Williamson DH (1980) Physiological roles of ketone bodies as substrates and signals in mammalian tissues. Physiol Rev 60:143-87 (Pubitemid 10104513)
189. Rodrigues TB, López-Larrubia P, Cerdán S (2009) Redox dependence and compartmentation of [13C]pyruvate in the brain of deuterated rats bearing implanted C6 gliomas. J Neurochem 109(Suppl 1):237-45
190. Rolleston FS, Newsholme EA (1967) Effects of fatty acids, ketone bodies, lactate and pyruvate on glucose utilization by guinea-pig cerebral cortex slices. Biochem J 104:519-23
191. Ruderman NB, Ross PS, Berger M, Goodman MN (1974) Regulation of glucose and ketone-body metabolism in brain of anaesthetized rats. Biochem J 138:1-10
192. Schaffer WT, Olson MS (1980) The regulation of pyruvate oxidation during membrane depolarization of rat brain synaptosomes. Biochem J 192:741-51 (Pubitemid 11206844)
193. Schmalbruch IK, Linde R, Paulson OB, Madsen PL (2002) Activation-induced resetting of cerebral metabolism and flow is abolished by beta-adrenergic blockade with propranolol. Stroke 33:251-5 (Pubitemid 34052220)
194. Schousboe A, Drejer J, Hansen GH, Meier E (1985) Cultured neurons as model systems for biochemical and pharmacological studies on receptors for neurotransmitter amino acids. Dev Neurosci 7:252-62 (Pubitemid 16120573)
195. Schurr A (2006) Lactate: the ultimate cerebral oxidative energy substrate? J Cereb Blood Flow Metab 26:142-52
196. Schurr A, West CA, Rigor BM (1988) Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 240:1326-8
197. Scott ID, Nicholls DG (1980) Energy transduction in intact synaptosomes. Influence of plasma-membrane depolarization on the respiration and membrane potential of internal mitochondria determined in situ. Biochem J 186:21-33 (Pubitemid 10152072)
198. Sher PK (1990) Chronic hypoxia in neuronal cell culture: metabolic consequences. Brain Dev 12:293-300 (Pubitemid 20227954)
199. 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 Metab 301:E1040-9
200. Shuttleworth CW (2010) Use of NAD(P)H and flavoprotein autofluorescence transients to probe neuron and astrocyte responses to synaptic activation. Neurochem Int 56:379-86
201. Shuttleworth CW, Brennan AM, Connor JA (2003) NAD(P)H fluorescence imaging of postsynaptic neuronal activation in murine hippocampal slices. J Neurosci 23:3196-208 (Pubitemid 36531961)
202. SiesjöBK (1978) Brain Energy Metabolism. Chichester: John Wiley & Sons
203. Simpson IA, Carruthers A, Vannucci SJ (2007) Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 27:1766-91 (Pubitemid 47624552)
204. Smith D, Pernet A, Hallett WA, Bingham E, Marsden PK, Amiel SA (2003) Lactate: a preferred fuel for human brain metabolism in vivo. J Cereb Blood Flow Metab 23:658-64 (Pubitemid 36713670)
205. Sokoloff L, Reivich M, Kennedy C, Des Rosiers MH, Patlak CS, Pettigrew KD, Sakurada O, Shinohara M (1977) The [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 28:897-916 (Pubitemid 8098854)
206. Sonnewald U, Müller TB, Westergaard N, Unsga°rd G, Petersen SB, Schousboe A (1994) NMR spectroscopic study of cell cultures of astrocytes and neurons exposed to hypoxia: compartmentation of astrocyte metabolism. Neurochem Int 24:473-83 (Pubitemid 24169906)
207. Soucek T, Cumming R, Dargusch R, Maher P, Schubert D (2003) The regulation of glucose metabolism by HIF-1 mediates a neuroprotective response to amyloid beta peptide. Neuron 39:43-56 (Pubitemid 36830947)
208. Swanson RA, Benington JH (1996) Astrocyte glucose metabolism under normal and pathological conditions in vitro. Dev Neurosci 18:515-21 (Pubitemid 26371596)
209. Swanson RA, Yu AC, Chan PH, Sharp FR (1990) Glutamate increases glycogen content and reduces glucose utilization in primary astrocyte culture. J Neurochem 54:490-6
210. Takahashi S, Driscoll BF, Law MJ, Sokoloff L (1995) Role of sodium and potassium ions in regulation of glucose metabolism in cultured astroglia. Proc Natl Acad Sci USA 92:4616-20
211. Terrian DM, Johnston D, Claiborne BJ, Ansah-Yiadom R, Strittmatter WJ, Rea MA (1988) Glutamate and dynorphin release from a subcellular fraction enriched in hippocampal mossy fiber synaptosomes. Brain Res Bull 21:343-51 (Pubitemid 19269149)
212. Vaishnavi SN, Vlassenko AG, Rundle MM, Snyder AZ, Mintun MA, Raichle ME (2010) Regional aerobic glycolysis in the human brain. Proc Natl Acad Sci USA 107:17757-62
213. van Hall G, Strømstad M, Rasmussen P, Jans O, Zaar M, Gam C, Quistorff B, Secher NH, Nielsen HB (2009) Blood lactate is an important energy source for the human brain. J Cereb Blood Flow Metab 29:1121-9
214. Vannucci SJ, Maher F, Koehler E, Simpson IA (1994) Altered expression of GLUT-1 and GLUT-3 glucose transporters in neurohypophysis of water-deprived or diabetic rats. Am J Physiol 267:E605-11
215. Vannucci SJ, Simpson IA (2003) Developmental switch in brain nutrient transporter expression in the rat. Am J Physio Endocrinol Metab 285:E1127-34 (Pubitemid 37296336)
216. Veech RL (1991) The metabolism of lactate. NMR Biomed 4:53-8
217. Veech RL, Harris RL, Veloso D, Veech EH (1973) Freezeblowing: a new technique for the study of brain in vivo. J Neurochem 20:183-8
218. Vissing J, Andersen M, Diemer NH (1996) Exercise-induced changes in local cerebral glucose utilization in the rat. J Cereb Blood Flow Metab 16:729-36 (Pubitemid 26227084)
219. Waagepetersen HS, Sonnewald U, Larsson OM, Schousboe A (2000) Compartmentation of TCA cycle metabolism in cultured neocortical neurons revealed by 13C MR spectroscopy. Neurochem Int 36:349-58 (Pubitemid 30101576)
220. Walz W, Mukerji S (1988) Lactate release from cultured astrocytes and neurons: a comparison. Glia 1: 366-70
221. Wang L, Bill A (1997) Effects of constant and flickering light on retinal metabolism in rabbits. Acta Ophthalmol Scand 75:227-31 (Pubitemid 27315581)
222. Wang L, Kondo M, Bill A (1997a) Glucose metabolism in cat outer retina. Effects of light and hyperoxia. Invest Ophthalmol Vis Sci 38:48-55 (Pubitemid 27051523)
223. Wang L, Tornquist P, Bill A (1997b) Glucose metabolism of the inner retina in pigs in darkness and light. Acta Physiol Scand 160:71-4 (Pubitemid 27223430)
224. Wang L, Tornquist P, Bill A (1997c) Glucose metabolism in pig outer retina in light and darkness. Acta Physiol Scand 160:75-81 (Pubitemid 27223431)
225. Ward MW, Huber HJ, Weisová P, Düssmann H, Nicholls DG, Prehn JH (2007) Mitochondrial and plasma membrane potential of cultured cerebellar neurons during glutamate-induced necrosis, apoptosis, and tolerance. J Neurosci 27:8238-49 (Pubitemid 47219629)
226. Weisová P, Concannon CG, Devocelle M, Prehn JH, Ward MW (2009) Regulation of glucose transporter 3 surface expression by the AMP-activated protein kinase mediates tolerance to glutamate excitation in neurons. J Neurosci 29:2997-3008
227. Welsh FA (1980) In situ freezing of cat brain. In: Cerebral metabolism and neural function (Passonneau JV, Hawkins RA, Lust WD, Welsh FA, eds), Baltimore: Williams & Wilkins, 28-33
228. White EJ, Juchniewicz HJ, Clark JB (1989) Effects of lactic acidosis on the function of cerebral cortical synaptosomes. J Neurochem 52:154-61 (Pubitemid 19023362)
229. Wree A, Erselius R, Tønder N, Beck T (1993) Time course of hippocampal glucose utilization and persistence of parvalbumin immunoreactive neurons after ibotenic acid-induced lesions of the rat dentate area. J Cereb Blood Flow Metab 13:998-1005 (Pubitemid 23312649)
230. Wu K, Aoki C, Elste A, Rogalski-Wilk AA, Siekevitz P (1997) The synthesis of ATP by glycolytic enzymes in the postsynaptic density and the effect of endogenously generated nitric oxide. Proc Natl Acad Sci USA 94:13273-8 (Pubitemid 27518512)
231. Wyss MT, Jolivet R, Buck A, Magistretti PJ, Weber B (2011) In vivo evidence for lactate as a neuronal energy source. J Neurosci 31:7477-85
232. Wyss MT, Weber B, Treyer V, Heer S, Pellerin L, Magistretti PJ, Buck A (2009) Stimulation-induced increases of astrocytic oxidative metabolism in rats and humans investigated with 1-11C-acetate. J Cereb Blood Flow Metab 29:44-56
233. Yadava N, Nicholls DG (2007) Spare respiratory capacity rather than oxidative stress regulates glutamate excitotoxicity after partial respiratory inhibition of mitochondrial complex I with rotenone. J Neurosci 27: 7310-7 (Pubitemid 47037569)
234. Yamanishi S, Katsumura K, Kobayashi T, Puro DG (2006) Extracellular lactate as a dynamic vasoactive signal in the rat retinal microvasculature. Am J Physiol Heart Circ Physiol 290:H925-34
235. Yu AC, Hertz E, Hertz L (1984) Alterations in uptake and release rates for GABA, glutamate, and glutamine during biochemical maturation of highly purified cultures of cerebral cortical neurons, a GABAergic preparation. J Neurochem 42:951-60 (Pubitemid 14173544)
236. Yu S, Zhao T, Guo M, Fang H, Ma J, Ding A, Wang F, Chan P, Fan M (2008) Hypoxic preconditioning up-regulates glucose transport activity and glucose transporter (GLUT1 and GLUT3) gene expression after acute anoxic exposure in the cultured rat hippocampal neurons and astrocytes. Brain Res 1211:22-9 (Pubitemid 351636093)
237. Zeng J, Yang GY, Ying W, Kelly M, Hirai K, James TL, Swanson RA, Litt L (2007) Pyruvate improves recovery after PARP-1-associated energy failure induced by oxidative stress in neonatal rat cerebrocortical slices. J Cereb Blood Flow Metab 27:304-15 (Pubitemid 46148457)
238. Zhao Y, Fung C, Shin D, Shin BC, Thamotharan S, Sankar R, Ehninger D, Silva A, Devaskar SU (2010) Neuronal glucose transporter isoform 3 deficient mice demonstrate features of autism spectrum disorders. Mol Psychiatry 15:286-99
239. Zielke HR, Zielke CL, Baab PJ, Tildon JT (2007) Effect of fluorocitrate on cerebral oxidation of lactate and glucose in freely moving rats. J Neurochem 101:9-16 (Pubitemid 46426464)
240. Zielke HR, Zielke CL, Baab PJ (2009) Direct measurement of oxidative metabolism in the living brain by microdialysis: a review. J Neurochem 109(Suppl 1):24-9