The effect of cell size and channel density on neuronal information encoding and energy efficiency

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 9, 2013, Pages 1465-1473

  Sengupta, Biswa ^a,b   Faisal, A Aldo ^c,d   Laughlin, Simon B ^e   Niven, Jeremy E ^f  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b INDIAN INSTITUTE OF SCIENCE   (India)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d MRC CLINICAL SCIENCES CENTRE   (United Kingdom)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

action potentials; energy metabolism; K channels; mathematical modeling; Na channels

Indexed keywords

VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

ARTICLE; CELL SIZE; CELLULAR PARAMETERS; CHANNEL DENSITY; CODING ALGORITHM; COMPARTMENT MODEL; DENSITY; ENERGY CONSUMPTION; NERVE CONDUCTION; NERVE POTENTIAL; PRIORITY JOURNAL; SPIKE WAVE; STIMULUS RESPONSE; STOCHASTIC MODEL; SYNAPTIC TRANSMISSION;

ANIMALS; CELL SIZE; ENERGY METABOLISM; HUMANS; MODELS, NEUROLOGICAL; NEURONS; POTASSIUM CHANNELS, VOLTAGE-GATED; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84883739502     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.103     Document Type: Article

References (40)

1. Cajal SRy. Nobel Lecture: The Structure and Connexions of Neurons. Elsevier Publishing Company: Amsterdam, 1906.
2. Golgi C. Nobel Lecture: The neuron doctrine-theory and facts. Elsevier Publishing Company: Amsterdam, 1906.
3. Quesada R, Triana E, Vargas G, Douglass JK, Seid MA, Niven JE et al. The allometry of CNS size and consequences of miniaturization in orb-weaving and cleptoparasitic spiders. Arthropod Struct Dev 2011; 40: 521-529.
4. Perge JA, Niven JE, Mugnaini E, Balasubramanian V, Sterling P. Why do axons differ in caliber? J Neurosci 2012; 32: 626-638.
5. Purves D, Lichtman JW. Geometrical differences among homologous neurons in mammals. Science 1985; 228: 298-302. (Pubitemid 15076826)
6. Faisal AA, White JA, Laughlin SB. Ion-channel noise places limits on the miniaturization of the brain's wiring. Curr Biol 2005; 15: 1143-1149. (Pubitemid 40841359)
7. Erlanger J. Nobel Lecture: Some Observations on the Responses of Single Nerve Fibers. Elsevier Publishing Company: Amsterdam, 1947.
8. Gasser H. Nobel Lecture: Mammalian nerve fibers. Elsevier Publishing Company: Amsterdam, 1945.
9. Sengupta B, Laughlin SB, Niven JE. Comparison of Langevin and Markov channel noise models for neuronal signal generation. Phys Rev E Stat Nonlin Soft Matter Phys 2010; 81: 011918.
10. Prescott SA, Ratte S, De Koninck Y, Sejnowski TJ. Pyramidal neurons switch from integrators in vitro to resonators under in vivo-like conditions. J Neurophysiol 2008; 100: 3030-3042.
11. Zeberg H, Blomberg C, Arhem P. Ion channel density regulates switches between regular and fast spiking in soma but not in axons. PLoS Comput Biol 2010; 6: e1000753.
12. Koch K, McLean J, Berry M, Sterling P, Balasubramanian V, Freed MA. Efficiency of information transmission by retinal ganglion cells. Curr Biol 2004; 14: 1523-1530. (Pubitemid 39290049)
13. Perge JA, Koch K, Miller R, Sterling P, Balasubramanian V. How the optic nerve allocates space, energy capacity, and information. J Neurosci 2009; 29: 7917-7928.
14. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 2001; 21: 1133-1145. (Pubitemid 32947479)
15. Niven JE, Anderson JC, Laughlin SB. Fly photoreceptors demonstrate energy-information trade-offs in neural coding. PLoS Biol 2007; 5: e116.
16. Skaugen E, Walloe L. Firing behaviour in a stochastic nerve membrane model based upon the Hodgkin-Huxley equations. Acta Physiol Scand 1979; 107: 343-363. (Pubitemid 10202647)
17. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 1952; 117: 500-544.
18. Destexhe A, Rudolph M, Fellous JM, Sejnowski TJ. Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neuroscience 2001; 107: 13-24. (Pubitemid 34020681)
19. Strong SP, de Ruyter van Steveninck RR, Bialek W, Koberle R. On the application of information theory to neural spike trains. In: Proceedings of the Pac Symp Biocomput 1998; 3: 621-632.
20. Treves A, Panzeri S. The upward bias in measures of information derived from limited data samples. Neural Comput 1995; 7: 399-407.
21. Skou JC. The identification of the sodium-pump as the membrane-bound Na\+/K\+-ATPase: a commentary on 'The Influence of Some Cations on an Adenosine Triphosphatase from Peripheral Nerves'. Biochim Biophys Acta 1989; 1000: 435-438.
22. Skou JC. The influence of some cations on an adenosine triphosphatase from peripheral nerves. Biochim Biophys Acta 1957; 23: 394-401.
23. Sengupta B, Stemmler M, Laughlin SB, Niven JE. Action potential energy efficiency varies among neuron types in vertebrates and invertebrates. PLoS Comput Biol 2010; 6: e1000840.
24. Chow CC, White JA. Spontaneous action potentials due to channel fluctuations. Biophys J 1996; 71: 3013-3021. (Pubitemid 26422344)
25. Schneidman E, Segev I, Tishby N. Information capacity and robustness of stochastic neuron models. In: NIPS. MIT Press: Cambridge, MA, 1999, pp 178-184.
26. Balasubramanian V, Kimber D, Berry MJ. Metabolically efficient information processing. Neural Comp 2001; 13: 799-815. (Pubitemid 33594305)
27. De Polavieja GG. Errors drive the evolution of biological signalling to costly codes. J Theor Biol 2002; 214: 657-664. (Pubitemid 34948534)
28. Levy WB, Baxter RA. Energy efficient neural codes. Neural Comput 1996; 8: 531-543. (Pubitemid 126450623)
29. Niven JE, Laughlin SB. Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 2008; 211: 1792-1804. (Pubitemid 351964926)
30. Niven JE, Farris SM. Miniaturization of nervous systems and neurons. Curr Biol 2012; 22: R323-R329.
31. Laughlin SB, de Ruyter van Steveninck RR, Anderson JC. The metabolic cost of neural information. Nat Neurosci 1998; 1: 36-41. (Pubitemid 128652639)
32. Koch K, McLean J, Segev R, Freed MA, Berry 2nd MJ, Balasubramanian V et al. How much the eye tells the brain. Curr Biol 2006; 16: 1428-1434. (Pubitemid 44066773)
33. Crotty P, Sangrey T, Levy WB. Metabolic energy cost of action potential velocity. J Neurophysiol 2006; 96: 1237-1246. (Pubitemid 44376259)
34. Doyle DA, Cabral JM, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL et al. The structure of the potassium channel: molecular basis of K\+ conduction and selectivity. Science 1998; 280: 69-77. (Pubitemid 28169082)
35. Maixent JM, Berrebi-Bertrand I. Turnover rates of the canine cardiac Na,K-ATPases. FEBS Lett 1993; 330: 297-301. (Pubitemid 23276343)
36. Shinoda T, Ogawa H, Cornelius F, Toyoshima C. Crystal structure of the sodiumpotassium pump at 2.4 Angstrom resolution. Nature 2009; 459: 446-450.
37. Kennedy MB. Signal-processing machines at the postsynaptic density. Science 2000; 290: 750-754.
38. Clarke D, Sokoloff L. Circulation and Energy Metabolism of the Brain. In: Siegel GJ, Agranoff BW, Albers RW, Fisher SK, Uhler MD (eds). Basic Neurochemsitry: Molecular, Cellular and Medical Aspects. Lippincott-Raven: Philadelphia, 1999, pp 637-669.
39. Faisal AA, Laughlin SB. Stochastic simulations on the reliability of action potential propagation in thin axons. PLoS Comput Biol 2007; 3: e79.
40. Hustert R. Giant and dwarf axons in a miniature insect, Encarsia formosa, (Hymenoptera, Calcididae). Arthropod Struct Dev 2012; 41: 535-543.