An increase in lactate output by brain tissue serves to meet the energy needs of glutamate-activated neurons

Journal of Neuroscience

Volumn 19, Issue 1, 1999, Pages 34-39

  Schurr, Avital ^a   Miller, James J ^a   Payne, Ralphiel S ^a   Rigor, Benjamin M ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Energy metabolism; Glial glycolytic flux; Glutamate excitation; Hippocampal slices; Lactate transport; Neuronal function

Indexed keywords

DEOXYGLUCOSE; GLUTAMIC ACID; LACTIC ACID; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL TISSUE; ARTICLE; BRAIN METABOLISM; BRAIN SLICE; CELL ACTIVATION; ENERGY METABOLISM; GLUCOSE METABOLISM; GLYCOLYSIS; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0032929864     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-01-00034.1999     Document Type: Article

References (49)

1. Brew H, Attwell D (1987) Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327:707-709.
2. Bröer S, Rahman B, Pellegri G, Pellerin L, Martin J-L, Verleysdonk S, Hamprecht B, Magistretti PJ (1997) Comparison of lactate transport in astroglial cells and monocarboxylate transporter 1 (MCT 1) expressing Xenopus laevis oocytes. J Biol Chem 272:30096-30102.
3. Brooks GA (1987) Lactate production under fully aerobic conditions: the lactate shuttle during rest and exercise. Fed Proc 45:2924-2929.
4. Bueno D, Azzolin IR, Perry MLS (1994) Ontogenic study of glucose and lactate utilisation by rat cerebellum slices. Med Sci Res 22:631-632.
5. Buxton RB, Frank LR (1997) A model for the coupling between cerebral blood flow and oxygen metabolism during neural stimulation. J Cereb Blood Flow Metab 17:64-72.
6. Clarke DD, Sokoloff L (1994) Circulation and energy metabolism of the brain. In: Basic neurochemistry (Siegle GJ, Agranoff BW, Albers RW, Molinoff PB, eds), pp 645-680. New York: Raven.
7. Fellows LK, Boutelle MG, Fillenz M (1993) Physiological stimulation increases nonoxidative glucose metabolism in the brain of the freely moving rat. J Neurochem 60:1258-1263.
8. 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 83:1140-1144.
9. Fox PT, Raichle ME, Mintun MA, Dence C (1988) Nonoxidative glucose consumption during focal physiologic neural activity. Science 241:462-464.
10. Fray AE, Forsyth RJ, Boutelle MG, Fillenz M (1996) The mechanisms controlling physiologically stimulated changes in rat brain glucose and lactate: a microdialysis study. J Physiol (Lond) 496:49-57.
11. Friedmann TE, Barborka C (1941) The significance of the ratio of lactic acid to pyruvic acid in blood after exercise. J Biol Chem 141:993-994.
12. Haljamae H (1987) Lactate metabolism. Intens Care World 4:118-121.
13. Henneberry RC (1989) The role of neuronal energy in the neurotoxicity of excitatory amino acids. Neurobiol Aging 10:611-613.
14. Hu Y, Wilson GS (1997) A temporary lacal energy pool coupled to neuronal activity: fluctuations of extracellular lactate levels in rat brain monitored with rapid-response enzyme-based sensor. J Neurochem 69:1484-1490.
15. 13C]NMR. Proc Natl Acad Sci USA 93:7612-7617.
16. Irwin RP, Lin S-Z, Paul SM (1994) N-methyl-D-aspartate induces a rapid, reversible, and calcium-dependent intracellular acidosis in cultured fetal rat hippocampal neurons. J Neurosci 14:1352-1357.
17. Izumi Y, Benz AM, Zorumski CF, Olney JW (1994) Effects of lactate and pyruvate on glucose deprivation in rat hippocampal slices. NeuroReport 5:617-620.
18. Izumi Y, Benz AM, Katsuki H, Zorumski CF (1997) Endogenous monocarboxylates sustain hippocampal synaptic function and morphological integrity during energy deprivation. J Neurosci 17:9448-9457.
19. Kim S-G, Ugurbil K (1997) Comparison of blood oxygenation and cerebral blood flow effects in fMRI: estimation of relative oxygen consumption change. Magn Reson Med 38:59-65.
20. Kim S-G, Hendrich K, Hu X, Merkle H, Ugurbil K (1994) Potential pitfalls of functional MRI using conventional gradient-recalled echo techniques. NMR Biomed 7:69-74.
21. Larrabee MG (1995) Lactate metabolism and its effects on glucose metabolism in an excised neural tissue. J Neurochem 64:1734-1741.
22. 2 production between glucose and lactate in excised sympathetic ganglia, with implications for brain. J Neurochem 67:1726-1734.
23. + uptake require glycolysis. Fed Proc 12:2875-2880.
24. Magistretti PJ, Pellerin L, Martin JL (1995) Brain energy metabolism: an integrated cellular perspective. In: Psychopharmacology: the Fourth Generation of Progress (Bloom FE, Kupfer DJ, eds), pp 657-670. New York: Raven.
25. Malonek D, Grinvald A (1996) Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science 272:551-554.
26. Malonek D, Dirnagl U, Lindauer U, Yamada K, Kanno I, Grinvald A (1997) Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc Natl Acad Sci USA 94:14826-14831.
27. McIlwain H (1953a) Glucose level, metabolism, and response to electrical impulses in cerebral tissues from man and laboratory animals. Biochem J 55:618-624.
28. McIlwain H (1953b) Substances which support respiration and metabolic response to electrical impulses in human cerebral tissues. J Neurol Neurosurg Psychiatry 16:257-266.
29. McIlwain H (1956) Electrical influences and speed of chemical change in the brain. Physiol Rev 36:355-375.
30. Novelli A, Reilly JA, Lysko PG, Henneberry RC (1988) Glutamate becomes neurotoxic via the N-methyl-D-aspartate receptor when intracellular energy levels are reduced. Brain Res 451:205-212.
31. Ogawa S, Tank DW, Menon RS, Ellermann JM, Kim S-G, Merkle H, Ugurbil K (1992) Intrinsic signal changes accompanying sensory stimulation: functional brain mapping using MRI. Proc Natl Acad Sci USA 89:5951-5955.
32. Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci USA 91:10625-10629.
33. +-ATPase activity in astrocytes via activation of a distinct subunit highly sensitive to ouabain. J Neurochem 69:2132-2137.
34. 1H NMR in human visual cortex during physiologic stimulation. Proc Natl Acad Sci USA 88:5829-5831.
35. Raichle ME (1991) The metabolic requirements of functional activity in the human brain: a positron emission tomography study. Adv Exp Med Biol 291:1-4.
36. 15O PET rCBF. J Cereb Blood Flow Metab 16:755-764.
37. Rosenberg PA, Aizenmann E (1989) Hundred-fold increase in neuronal vulnerability to glutamate toxicity in astrocytes-poor cultures of rat cerebral cortex. Neurosci Lett 103:162-168.
38. Rosenberg PA, Amin S, Leitner M (1992) Glutamate uptake disguises neurotoxic potency of glutamate agonists in cerebral cortex in dissociated cell culture. J Neurosci 12:56-61.
39. 31P magnetic resonance spectroscopy. J Cereb Blood Flow Metab 12:584-592.
40. Schurr A, Reid KH, Tseng MT, Edmonds Jr HL, Rigor BM (1985) A dual chamber for comparative studies using the brain slice preparation. Comp Biochem Physiol 82A:701-704.
41. Schurr A, West CA, Rigor BM (1988) Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 240:1326-1328.
42. Schurr A, West CA, Rigor BM (1989) Electrophysiology of energy metabolism and neuronal function in the hippocampal slice preparation. J Neurosci Methods 28:7-13.
43. Schurr A, Payne RS, Miller JJ, Rigor BM (1997a) Brain lactate, not glucose, fuels the recovery of synaptic function from hypoxia upon reoxygenation: an in vitro study. Brain Res 744:105-111.
44. Schurr A, Payne RS, Miller JJ, Rigor BM (1997b) Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation. J Neurochem 69:423-426.
45. Schurr A, Payne RS, Miller JJ, Rigor BM (1997c) Glia are the main source of lactate utilized by neurons for recovery of function posthypoxia. Brain Res 774:221-224.
46. Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, Shulman RG (1998) Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci USA 95:316-321.
47. Siesjö BK (1981) Cell damage in the brain: a speculative synthesis. J Cereb Blood Flow Metab 1:155-185.
48. Stittsworth Jr JD, Lanthorn TH (1993) Lactate mimics only some effects of D-glucose on epileptic depolarization and long-term synaptic failure. Brain Res 630:21-27.
49. Volk C, Kempski B, Kempski OS (1997) Inhibition of lactate export by quercetin acidifies rat glial cells in vitro. Neurosci Lett 223:121-124.