Skip to main content
SpringerLink
Log in

Energetics of Functional Activation in Neural Tissues

  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Glucose utilization (lCMRglc) increases linearly with spike frequency in neuropil but not perikarya of functionally activated neural tissues. Electrical stimulation, increased extracellular [K+] ([K+]0), or opening of Na+ channels with veratridine stimulates 1CMRglc in neural tissues; these increases are blocked by ouabain, an inhibitor of Na+,K+-ATPase. Stimulating Na+,K+-ATPase activity to restore ionic gradients degraded by enhanced spike activity appears to trigger these increases in lCMRglc. Cultured neurons behave similarly. Astrocytic processes that envelop synapses in neuropil probably contribute to the increased lCMRglc. lCMRglc in cultured astroglia is unaffected by elevated [K+]0 but is stimulated by increased intracellular [Na+] ([Na+]i), and this stimulation is blocked by ouabain or tetrodotoxin. L-Glutamate also stimulates lCMRglc in astroglia. This effect is unaffected by inhibitors of NMDA or non-NMDA receptors, blocked by ouabain, and absent in Na+-free medium; it appears to be mediated by increased [Na+]i due to combined uptake of Na+ with glutamate via Na+/glutamate co-transporters.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. Sokoloff. L., Reivich, M., Kennedy, C., Des Rosiers, M. H., Patlak, C. S., Pettigrew, K. D., Sakurada, O., and 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.

    PubMed  Google Scholar 

  2. Sokoloff, L. 1981. 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.

    PubMed  Google Scholar 

  3. Miyaoka, M., Shinohara, M., Batipps, M., Pettigrew, K. D., Kennedy, C., and Sokoloff, L. 1979. 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.

    Google Scholar 

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

    Google Scholar 

  5. Kadekaro, M., Carne, A. M., and Sokoloff, L. 1985. 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 82:6010–6013.

    Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  15. Medzihradsky, F, Nandhasri, P. S., Idoyaga-Vargas, V, and Sellinger, O. Z. 1971. 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.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  25. Peng, L., Zhang, X., and 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. 663:168–172.

    PubMed  Google Scholar 

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

    Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  30. Magistretti, P. J., and Pellerin, L. 1996. Cellular bases of brain energy metabolism and their relevance to functional brain imaging: Evidence for a prominent role of astrocytes. Cerebral Cortex 6:50–61.

    PubMed  Google Scholar 

  31. Tsacopoulos, M., and Magistretti, P. 1996. Metabolic coupling between glia and neurons. J. Neurosci. 16:877–885.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Cerebral Metabolism, National Institute of Mental Health, Bethesda, MD, 20892-4030

    Louis Sokoloff

Authors
  1. Louis Sokoloff
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sokoloff, L. Energetics of Functional Activation in Neural Tissues. Neurochem Res 24, 321–329 (1999). https://doi.org/10.1023/A:1022534709672

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022534709672

Search

Navigation