[go: up one dir, main page]
More Web Proxy on the site http://driver.im/
Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

The metabolic cost of neural information

Abstract

We derive experimentally based estimates of the energy used by neural mechanisms to code known quantities of information. Biophysical measurements from cells in the blowfly retina yield estimates of the ATP required to generate graded (analog) electrical signals that transmit known amounts of information. Energy consumption is several orders of magnitude greater than the thermodynamic minimum. It costs 104 ATP molecules to transmit a bit at a chemical synapse, and 106 - 107 ATP for graded signals in an interneuron or a photoreceptor, or for spike coding. Therefore, in noise-limited signaling systems, a weak pathway of low capacity transmits information more economically, which promotes the distribution of information among multiple pathways.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Cells, synapses and signals in blowfly compound eye.
Figure 2: The electrical models of photoreceptor and LMC membranes.
Figure 3: The cost of a bit of information plotted against information transmission rate for a single chemical synapse, a hypothetical LMC using spikes, and the graded signals of a photoreceptor and an LMC.
Figure 4: The rise in cost per bit with bit rate is illustrated by modeling the transfer of signals from a photoreceptor (PR) to an LMC via a parallel array of ns identical synapses.

Similar content being viewed by others

References

  1. Kety, S.S. in Metabolism of the Nervous System (ed. Richter, D.) 221–237 (Pergamon, London, 1957)

    Book  Google Scholar 

  2. Ames, A. Energy-requirements of CNS cells as related to their function and to their vulnerability to ischemia - a commentary based on studies on retina. Can. J. Physiol. Pharmacol. 70, S158–S164 (1992)

    Article  CAS  Google Scholar 

  3. Ames, A. in Mitochondria and Free Radicals in Neurodegenerative Disease (eds Beal, M.F., Howell, N. & Bodis-Wollner, I.) 17–27 (Wiley-Liss, New York, 1997)

    Google Scholar 

  4. Aiello, L.C. & Wheeler, P. The expensive tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr. Anthropol. 36, 199–221 (1995)

    Article  Google Scholar 

  5. Martin, R.D. Scaling of the mammalian brain - the maternal energy hypothesis. News In Physiol. Sci. 11, 149–156 (1996)

    Google Scholar 

  6. Levy, W.B. & Baxter, R.A. Energy-efficient neural codes. Neural Computation 8, 531–543 (1996)

    Article  CAS  Google Scholar 

  7. Sarpeshkar, R. Analog versus digital: extrapolating from electronics to neurobiology. Neural Computation (in press, 1998)

  8. de Ruyter van Steveninck, R.R. & Laughlin, S.B. The rate of information-transfer at graded-potential synapses. Nature 379, 642–645 (1996)

    Article  CAS  Google Scholar 

  9. Laughlin, S.B. Matching coding, circuits, cells, and molecules to signals - general principles of retinal design in the fly's eye. Prog. Ret. Eye. Res. 13, 165–196 (1994)

    Article  CAS  Google Scholar 

  10. Gerster, U., Stavenga, D.G. & Backhaus, W. Na+/K+ pump activity in photoreceptors of the blowfly Calliphora: A model analysis based on membrane potential measurements . J. Comp. Physiol. A. 180, 113– 122 (1997)

    Article  CAS  Google Scholar 

  11. Hamdorf, K., Hochstrate, P., Hoglund, G., Burbach, B. & Wiegand, U. Light activation of the sodium-pump in blowfly photoreceptors . J. Comp. Physiol. A. 162, 285– 300 (1988)

    Article  Google Scholar 

  12. Jansonius, N.M. Properties of the sodium-pump in the blowfly photoreceptor cell. J. Comp. Physiol. A. 167, 461–467 (1990)

    Article  Google Scholar 

  13. Tsacopoulos, M., Veuthey, A.L., Saravelos, S.G., Perrottet, P. & Tsoupras, G. Glial-cells transform glucose to alanine, which fuels the neurons in the honeybee retina. J. Neurosci. 14, 1339–1351 (1994)

    Article  CAS  Google Scholar 

  14. Beersma, D.G.M., Stavenga, D.G. & Kuiper, J.W. Retinal lattice, visual field and binocularities in flies. J. Comp. Physiol. 119, 207– 220 (1977)

    Article  Google Scholar 

  15. Hardie, R.C. & Minke, B. Phosphoinositide-mediated phototransduction in Drosophila photoreceptors - the role of Ca2+ and trp. Cell Calcium 18, 256– 274 (1995)

    Article  CAS  Google Scholar 

  16. Nicol, D. & Meinertzhagen, I.A. An analysis of the number and composition of the synaptic populations formed by photoreceptors of the fly. J. Comp. Neurol. 207, 29– 44 (1982)

    Article  CAS  Google Scholar 

  17. Hardie, R.C. A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse . Nature 339, 704–706 (1989)

    Article  CAS  Google Scholar 

  18. Laughlin, S.B. & Osorio, D. Mechanisms for neural signal enhancement in the blowfly compound eye. J. Exp. Biol. 144, 113–146 (1989)

    Google Scholar 

  19. van Hateren, J.H. & Laughlin, S.B. Membrane parameters, signal transmission, and the design of a graded potential neuron. J. Comp. Physiol. A. 166, 437–448 (1990)

    Article  CAS  Google Scholar 

  20. Uusitalo, R.O. & Weckström, M. The regulation of chloride homeostasis in the small nonspiking visual interneurons of the fly compound eye. J. Neurophysiol. 71, 1381– 1389 (1994)

    Article  CAS  Google Scholar 

  21. Borst, J.G.G. & Sakmann, B. Calcium influx and transmitter release in a fast CNS synapse. Nature 383, 431– 434 (1996)

    Article  CAS  Google Scholar 

  22. Hall, Z.W. An introduction to molecular neurobiology, 555 (Sinauer, Sunderland, Mass., 1992)

    Google Scholar 

  23. Rieke, F., Warland, D., de Ruyter van Steveninck, R.D. & Bialek, W. Spikes - exploring the neural code, 395 (MIT Press, Cambridge, Mass., 1997)

    Google Scholar 

  24. Keister, M. & Buck, J. in The Physiology of Insecta 2nd edn Vol. 6 (ed. Rockstein, M.) (Academic Press, N.Y., 1974)

    Google Scholar 

  25. Aiello, L.C. Brains and guts in human evolution: The expensive tissue hypothesis. Braz. J. Genetics 20, 141–148 (1997)

    Article  Google Scholar 

  26. Diamond, J.M. Competition for brain space. Nature 382, 756– 757 (1996)

    Article  CAS  Google Scholar 

  27. Szilard, L. Uber die Entropieverminderung in einem thermodynamischen System bei Eingriffen intelligenter Wesen. Z.Physik 53, 840–856 (1929)

    Article  CAS  Google Scholar 

  28. Leff, H.S. & Rex, A.F. Maxwell's Demon: Entropy, Information, Computing, 349 (Adam Hilger, Bristol, 1990 )

    Google Scholar 

  29. Howard, J. The movement of kinesin along microtubules. Ann. Rev. Physiol. 58, 703–729 (1996)

    Article  CAS  Google Scholar 

  30. Hua, W., Young, E.C., Fleming, M.L. & Gelles, J. Coupling of kinesin steps to ATP hydrolysis . Nature 388, 390–393 (1997)

    Article  CAS  Google Scholar 

  31. Schnitzer, M.J. & Block, S.M. Kinesin hydrolyses one ATP per 8-nm step. Nature 388, 386–390 (1997)

    Article  CAS  Google Scholar 

  32. Hille, B. Ionic Channels of Excitable Membranes, 607 (Sinauer, Sunderland, Mass., 1992)

    Google Scholar 

  33. Bray, D. Signaling complexes . Ann. Rev. Biophys. (in press, 1998)

  34. Weckström, M., Hardie, R.C. & Laughlin, S.B. Voltage-activated potassium channels in blowfly photoreceptors and their role in light adaptation. J. Physiol. (Lond.) 440, 635–657 (1991)

    Article  Google Scholar 

  35. Weckström, M., Kouvalainen, E. & Juusola, M. Measurement of cell impedance in frequency-domain using discontinuous current clamp and white-noise-modulated current injection. Pflugers Arch.-Eur. J. Physiol. 421, 469– 472 (1992)

    Article  Google Scholar 

  36. Hardie, R.C. Whole-cell recordings of the light-induced current in dissociated Drosophila photoreceptors - evidence for feedback by calcium permeating the light-sensitive channels . Proc. R. Soc. Lond. B. 245, 203– 210 (1991)

    Article  Google Scholar 

  37. Stuart, A.E., Morgan, J.R., Mekeel, H.E., Kempter, E. & Callaway, J.C. Selective, activity-dependent uptake of histamine into an arthropod photoreceptor. J. Neurosci. 16, 3178–3188 (1996)

    Article  CAS  Google Scholar 

  38. Sonders, M.S. & Amara, S.G. Channels in transporters. Current Opinion In Neurobiology 6, 294– 302 (1996)

    Article  CAS  Google Scholar 

  39. Schuldiner, S., Shirvan, A. & Linial, M. Vesicular neurotransmitter transporters - from bacteria to humans. Physiol. Rev. 75, 369– 392 (1995)

    Article  CAS  Google Scholar 

  40. Laughlin, S.B., Howard, J. & Blakeslee, B. Synaptic limitations to contrast coding in the retina of the blowfly Calliphora. Proc. R. Soc. Lond. B. 231, 437–467 (1987)

    Article  CAS  Google Scholar 

  41. Fröhlich, A. Freeze-fracture study of an invertebrate multiple-contact synapse - the fly photoreceptor tetrad. J. Comp. Neurol. 241, 311– 326 (1985)

    Article  Google Scholar 

  42. Skingsley, D.R., Laughlin, S.B. & Hardie, R.C. Properties of histamine-activated chloride channels in the large monopolar cells of the dipteran compound eye - a comparative-study . J. Comp. Physiol. A. 176, 611– 623 (1995)

    Article  CAS  Google Scholar 

  43. Meinertzhagen, I.A. & O'Neil, S.D. Synaptic organization of columnar elements in the lamina of the wild- type in Drosophila melanogaster. J. Comp. Neurol. 305, 232–263 (1991)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank W. Bialek, D. Bray, R. Carpenter, R.C. Hardie, J.H. van Hateren and D.C. O'Carroll for their comments and suggestions, and A. Ames for his encouragement and an excellent introduction to the energetics of neural function.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Simon B. Laughlin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Laughlin, S., de Ruyter van Steveninck, R. & Anderson, J. The metabolic cost of neural information. Nat Neurosci 1, 36–41 (1998). https://doi.org/10.1038/236

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/236

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing