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Functional Activation of Energy Metabolism in Nervous Tissue: Where and Why

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Neurodegenerative Diseases

Abstract

In tissues that do physical work, such as heart, skeletal muscle, and kidney, rates of energy metabolism under physiological conditions vary more or less in proportion to the amount of work being done by the tissue. To demonstrate such a relationship in brain has been difficult because, first of all, the exact nature of the physical work done by brain tissue is not obvious, and, secondly, the brain mediates a variety of functions, each of which is localized in discrete regions specific for the function and not in the tissue as a whole. It is only recently that it has become possible to measure the rates of energy metabolism in such discrete structural and functional components of the nervous system in conscious, behaving animals and man and to relate these rates to the levels of functional activity within them.

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References

  1. D.D. Clarke and L. Sokoloff, Circulation and energy metabolism of the brain; in: Basic Neurochemistry, Fifth Edition, G. Siegel, B.W. Agranoff, R.W. Albers, and P. Molinoff, eds, Raven Press, New York (1994), pp. 645–680.

    Google Scholar 

  2. O.E. Owen, A.P. Morgan, H.G. Kemp, J.M. Sullivan, M.G. Herrera, G.F. Cahill, Jr: Brain metabolism during fasting. J. Clin. Invest 46:1589–1595 (1967).

    Article  PubMed  CAS  Google Scholar 

  3. L. Sokoloff, M. Reivich, C. Kennedy, M.H. Des Rosiers, C.S. Patlak, K.D. Pettigrew, O. Sakurada, M. Shinohara, The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: heory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28:897–916 (1977).

    Article  PubMed  CAS  Google Scholar 

  4. C. B. Smith, Localization of actvity-associated changes in metabolism of the central nervous system with the deoxyglucose method: Prospects for cellular resolution, in: Current Methods in Cellular Neurobiology, Vol. I, Anatomical Techniques, J.L. Barker and J.F. McKelvy, eds, John Wiley, New York (1983), pp. 269–317.

    Google Scholar 

  5. M. Reivich, D. Kuhl, A. Wolf, J. Greenberg, M. Phelps, T. Ido, V. Cassella, J. Fowler, E. Hoffman, A. Alavi, P. Som, and L. Sokoloff, The [18F]fluoro-deoxyglucose method for the measurement of local cerebral glucose utilization in man. Circ.Res. 44:127–137 (1979).

    Article  PubMed  CAS  Google Scholar 

  6. M. E. Phelps, S.C. Huang, E.J. Hoffman, C. Selin, L. Sokoloff, and D.E. Kuhl, Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: validation of method, Ann. Neurol.; 6:371–388 (1979).

    Article  PubMed  CAS  Google Scholar 

  7. C. Kennedy, O. Sakurada, M. Shinohara, J.W. Jehle, and L. Sokoloff, Local cerebral glucose utilization in the normal conscious Macaque monkey. Ann. Neurol. 4: 293–301 (1978).

    Article  PubMed  CAS  Google Scholar 

  8. L. Sokoloff, Localization of functional activity in the central nervous system by measurement of glucose utilization with radioactive deoxyglucose. J. Cereb. Blood Flow Metab. 1:7–36 (1981).

    Article  PubMed  CAS  Google Scholar 

  9. ME. Phelps, J.C. Mazziotta, and S.C. Huang, Study of cerebral function with positron computed tomography. J. Cereb. Blood Flow Metab. 2: 113–162 (1982).

    Article  PubMed  CAS  Google Scholar 

  10. L. Sokoloff, Local cerebral circulation at rest and during altered cerebral activity induced by anesthesia or visual stimulation, in: The Regional Chemistry, Physiology and Pharmacology of the Nervous System, S.S. Kety and J. Elkes, eds., Pergamon Press, Oxford (1961), pp. 107–117.

    Google Scholar 

  11. N.A. Lassen, D. Ingvar, and E. Skinhøj, Brain function and blood flow. Sci. Am. 239: 62–71 (1978).

    Article  PubMed  CAS  Google Scholar 

  12. D.H. Hubel and T.N. Wiesel, Receptive fields and functional architecture of monkey striate cortex. J. Physiol. (London), 195: 215–243, (1968).

    CAS  Google Scholar 

  13. C. Kennedy, M.H. Des Rosiers, O. Sakurada, M. Shinohara, M. Reivich, J.W. Jehle, and L. Sokoloff, Metabolic mapping of the primary visual system of the monkey by means of the autoradiographic [14C]deoxyglucose technique. Proc. Natl. Acad. Sci., U.S.A. 73:4230–4234 (1976).

    Article  PubMed  CAS  Google Scholar 

  14. P.J. Hand, The 2-deoxyglucose method, in: Neuroanatomical Tracing Methods, L. Heimer and M.J. Robards, eds., Plenum Press, New York (1981), pp. 511–538.

    Chapter  Google Scholar 

  15. H.E. Savaki, C. Kennedy., L. Sokoloff, and M. Mishkin, Visually guided reaching with the forelimb contralateral to a’ blind’ hemisphere: a metabolic study in monkeys. J. Neurosci. 13:2772–2789 (1993).

    PubMed  CAS  Google Scholar 

  16. W. Schwartz, C.B. Smith, L. Davidsen, H. Savaki, L. Sokoloff, M. Mata, D. J. Fink, and H. Gainer, Metabolic mapping of functional activity in the hypothalamoneurohypophysial system of the rat. Science 205:723–725 (1979).

    Article  PubMed  CAS  Google Scholar 

  17. M. Miyaoka, M. Shinohara, M. Batipps, K.D. Pettigrew, C. Kennedy, and L. Sokoloff, The relationship between the intensity of the stimulus and the metabolic response in the visual system of the rat. Acta Neurol. Scand. 60 [Suppl 70]): 16–17 (1979).

    Google Scholar 

  18. J.J. Nordmann, Ultrastructural morphometry of the rat neurohypophysis. J. Anat. 123:213–218 (1977).

    PubMed  CAS  Google Scholar 

  19. M. Kadekaro, A.M. Crane, and L. Sokoloff, 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., U.S.A. 82:6010–6013 (1985).

    Article  PubMed  CAS  Google Scholar 

  20. T.G. Smith, Jr., Sites of action potential generation in cultured neurons. Brain Res. 288:381–383 (1983).

    Article  PubMed  Google Scholar 

  21. W.H. Freygang, Jr., An analysis of extracellular potentials from single neurons in the lateral geniculate nucleus of the cat. J. Gen. Physiol. 41:543–564 (1958).

    Article  PubMed  Google Scholar 

  22. W.H. Freygang, Jr. and K. Frank, Extracellular potentials from single spinal motoneurones. J. Gen. Physiol 42:749–760 (1959).

    Article  PubMed  Google Scholar 

  23. P. Yarowsky, M. Kadekaro, and L. Sokoloff, Frequency-dependent activation of glucose utilization in the superior cervical ganglion by electrical stimulation of cervical sympathetic trunk. Proc. Natl. Acad. Sci., U.S.A. 80:4179–4183 (1983).

    Article  PubMed  CAS  Google Scholar 

  24. M. Shinohara, B. Dollinger, G. Brown, S. Rapoport, L. Sokoloff, Cerebral glucose utilization: Local changes during and after recovery from spreading cortical depression. Science 203:188–190 (1979).

    Article  PubMed  CAS  Google Scholar 

  25. M. Mata, D.J. Fink, H. Gainer, C.B. Smith, L. Davidsen, H. Savaki, W.J. Schwartz, and L. Sokoloff, Activity-dependent energy metabolism in rat posterior pituitary primarily reflects sodium pump activity. J. Neurochem. 34: 213–215 (1980).

    Article  PubMed  CAS  Google Scholar 

  26. R.K. Orkand, J.G. Nicholls, and S.W. Kuffler, Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29:788–806 (1966).

    PubMed  CAS  Google Scholar 

  27. F. Medzihradsky, P.S. Nandhasri, V. Idoyaga-Vargas, and O.Z. Sellinger, A comparison of ATPase activity of the glial cell fraction and the neuronal perikaryal fraction isolated in bulk from rat cerebral cortex. J. Neurochem. 18:1599–1603 (1971).

    Article  PubMed  CAS  Google Scholar 

  28. F.A. Henn, H. Haljamäe, and A. Hamberger, Glial cell function: active control of extracellular K+ concentration. Brain Res. 43: 437–443 (1972).

    Article  PubMed  CAS  Google Scholar 

  29. L. Hertz, Drug-induced alterations of ion distribution at the cellular level of the central nervous system. Pharmacol. Rev. 29, 35–65 (1977).

    PubMed  CAS  Google Scholar 

  30. M. Erecinska and I.A. Silver, Metabolism and role of glutamate in mammalian brain. Progress in Neurobiol. 43, 37–71 (1994).

    Article  CAS  Google Scholar 

  31. M. A. Kai-Kai and V.W. Pentreath, High resolution analysis of [3H]2-deoxyglucose incorporation into neurons and glial cells in invertebrate ganglia: histological processing of nervous tissue for selective marking of glycogen. J. Neurocytol. 10:693–708 (1981).

    Article  PubMed  CAS  Google Scholar 

  32. V.W. Pentreath and M.A. Kai-Kai, Significance of the potassium signal from neurons to glial cells. Nature 295, 59–61 (1982).

    Article  PubMed  CAS  Google Scholar 

  33. P. Yarowsky, A.F. Boyne, R. Wierwille, and N. Brookes, Effect of monensin on deoxyglucose uptake in cultured astrocytes: energy metabolism is coupled to sodium entry. J. Neurosci. 6:859–866 (1986).

    PubMed  CAS  Google Scholar 

  34. R.S. Badar-Goffer, O. Ben-Yoseph, H.S. Bachelard, and P.G. Morris, Neuronal-glial metabolism under depolarizing conditions. A 13C-n.m.r. study. Biochem. J. 282,225–230 (1992).

    Google Scholar 

  35. C. J. Cummins, R.A Glover, and O.Z. Sellinger, Neuronal cues regulate uptake in cultured astrocytes. Brain Res. 170: 190–193 (1979).

    Article  PubMed  CAS  Google Scholar 

  36. C.J. Cummins, R.A. Glover, and O.Z. Sellinger, Astroglial uptake is modulated by extracellular K+. J. Neurochem. 33:779–785 (1979).

    Article  PubMed  CAS  Google Scholar 

  37. N. Brookes and P. J. Yarowsky, Determinants of deoxyglucose uptake in cultured astrocytes: the role of the sodium pump. J. Neurochem. 44:473–479 (1985).

    Article  PubMed  CAS  Google Scholar 

  38. L. Hertz and L. Peng, Energy metabolism at the cellur level of the CNS. Can. J. Physiol Pharmacol. 70 (Suppl.):S145–S157 (1992).

    Article  PubMed  CAS  Google Scholar 

  39. L. Peng, X. Zhang, and L. Hertz, High extracellular potassium concentrations stimulate oxidative metabolism in a glutamatergic neuronal culture and glycolysis in cultured astrocytes but have no stimulatory efect in a GABAergic neuronal culture. BrainRes. 663:168–172 (1994).

    CAS  Google Scholar 

  40. S. Takahashi, B.F. Driscoll, M.J. Law, and L. Sokoloff, Role of sodium and potassium in regulation of glucose metabolism in cultured astroglia. Proc. Natl. Acad. Sci., U.S.A. 92: 4616–4620 (1995).

    Article  PubMed  CAS  Google Scholar 

  41. P.R. Smith, R.I. Krohn, G.T. Hermanson, A.K. Mallia, F.H. Gartner, M.D. Provenzano, E. K. Fujimoto, N.M. Goeke, B.J. Olson, and D.C. Klenk, Measurement of protein using bicinchoninic acid. Anal. Biochem. 15:76–85 (1985).

    Article  Google Scholar 

  42. B. Flott and W. Seifert, Characterization of glutamate uptake in astrocyte primary cultures from rat brain. Glia 4: 293–304 (1991).

    Article  PubMed  CAS  Google Scholar 

  43. L. Pellerin and P.J. Magistretti, Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad Sci. U.S.A. 91:10625–10629 (1994).

    Article  PubMed  CAS  Google Scholar 

  44. N. Brookes and R. J. Turner, K+-induced alkalinization in mouse cerebral astrocytes mediated by reversal of electrogenic Na+-HCO3 cotransport. Am. J. Physiol. 267 (Cell Physiol. 36):C1633–C1640 (1994).

    PubMed  CAS  Google Scholar 

  45. P.P. Li and T.D. White, Rapid effects of veratridine, tetrodotoxin, gramicidin D, valinomycin and NaCN on the Na+, K+ and ATP contents of synaptosomes. J. Neurochem. 28: 967–975 (1977).

    Article  PubMed  CAS  Google Scholar 

  46. W.A. Catterall, Cellular and molecular biology of voltage-gated sodium channels. Physiol Rev. 72 (suppl.):S15–S48 (1992).

    PubMed  CAS  Google Scholar 

  47. H.K. Kimelberg, S. Biddlecome, S. Narumi, and R.S. Bourke, ATPase and carbonic anhydrase activities of bulk-isolated neuron, astroglia and synaptosome fractions from rat brain, Brain Res. 141:305–323 (1978).

    Article  PubMed  CAS  Google Scholar 

  48. B.C. Pressman and M. Fahim, Pharmacology and toxicology of the monovalent carboxylic ionophores. Annual Rev. Pharmacol Toxicol 22:465–490 (1982).

    Article  CAS  Google Scholar 

  49. B. Trivedi and W.H. Danforth, Effect of pH on the kinetics of frog muscle phosphofructokinase J. Biol Chem. 241:4110–4112 (1966).

    PubMed  CAS  Google Scholar 

  50. M. Erecinska, F. Dagani, D. Nelson, J. Deas, and I.A. Silver, Relations between intracellular ions and energy metabolism: A study with monensin in synaptosomes, neurons, and C6 glioma cells. J. Neurosci. 11:2410–2421 (1991).

    PubMed  CAS  Google Scholar 

  51. G. Moonen, G. Frank, and E. Schoffeniels, Glial control of neuronal excitability in mammals: I. Electrophysiological and isotopic evidence in culture. Neurochem. Int. 2, 299–310 (1980).

    Article  CAS  Google Scholar 

  52. B.A. Barres, New roles for glia. J. Neurosci. 11:3685–3694 (1991).

    PubMed  CAS  Google Scholar 

  53. B.A. Barres, L.L.Y. Chun, and D.P. Corey, Glial and neuronal forms of the voltage-dependent sodium channel: characteristics and cell-type distribution. Neuron 2:1375–1388 (1989).

    Article  PubMed  CAS  Google Scholar 

  54. K. Hisanaga, S.M. Sagar, K.J. Hicks, R.A. Swanson, and F.R. Sharp, c-fos proto-oncogene expression in astrocytes assocxiated wuth differentiatyion or proliferation but not depolarization. Mol. Brain Res. 8:69–75 (1990).

    Article  PubMed  CAS  Google Scholar 

  55. L. Hertz, An intense potassium uptake into astrocytes, its enhancement by high concentrations of potassium, and its possible involvement in potassium homeostasis at the cellular level. Brain Res. 145:202–208 (1978).

    Article  PubMed  CAS  Google Scholar 

  56. L. Hertz, Features of astrocytic function apparently involved in the response of central nervous tissue to ischemia-hypoxia. J. Cereb. Blood Flow Metab. 1:143–153 (1981).

    Article  PubMed  CAS  Google Scholar 

  57. Y. Kanai and M.A. Hediger, Primary structure and functional characterization of a high-affinity glutamate transporter. Nature (London) 360: 467–471 (1992).

    Article  CAS  Google Scholar 

  58. G. Pines, N.C. Danbolt, M. Bjørås, Y. Zhang, A. Bendahan, L. Eide, H. Koepsell, J. Storm-Mathisen, E. Seeberg, and B.I. Kanner, Cloning and expression of a rat brain L-glutamate transporter. Nature (London) 360:464–467 (1992).

    Article  CAS  Google Scholar 

  59. T. Storck, S. Schulte, K. Hofmann, and W. Stoffel, Structure, expression, and functional analysis of a Na+-dependent glutamate/aspartate transporter from rat brain. Proc. Natl Acad. Sci. USA 89: 10955–10959. (1992).

    Article  PubMed  CAS  Google Scholar 

  60. J.D. Rothstein, L. Martin, A.I. Levey, M. Dykes-Hoberg, L. Jin, D. Wu, N. Nash, and R.W. Kuncl, Neuron 13:713–725 (1994).

    Article  PubMed  CAS  Google Scholar 

  61. C.A. Bowman and H.K. Kimelberg, Excitatory amino acids depolarize rat brain astrocytes in primary culture. Nature (London) 311: 656-659. (1984).

    Google Scholar 

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Authors and Affiliations

  1. Laboratory of Cerebral Metabolism, National Institute of Mental Health, Bethesda, Maryland, 20892, USA

    Louis Sokoloff & Shinichi Takahashi

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  1. Louis Sokoloff
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  2. Shinichi Takahashi
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  1. The George Washington University Medical Center, Washington, D.C., USA

    Gary Fiskum

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Sokoloff, L., Takahashi, S. (1996). Functional Activation of Energy Metabolism in Nervous Tissue: Where and Why. In: Fiskum, G. (eds) Neurodegenerative Diseases. GWUMC Department of Biochemistry and Molecular Biology Annual Spring Symposia. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-0209-2_21

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  • DOI: https://doi.org/10.1007/978-1-4899-0209-2_21

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