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Fiorillo CD, Kim JK, Hong SZ. The meaning of spikes from the neuron's point of view: predictive homeostasis generates the appearance of randomness. Front Comput Neurosci. 2014;8:49doi: 10.3389/fncom.2014.00049.
Fiorillo, C. D., Kim, J. K., & Hong, S. Z. (2014). The meaning of spikes from the neuron's point of view: predictive homeostasis generates the appearance of randomness. Frontiers in computational neuroscience, 849. https://doi.org/10.3389/fncom.2014.00049
Fiorillo, Christopher D, et al. "The meaning of spikes from the neuron's point of view: predictive homeostasis generates the appearance of randomness." Frontiers in computational neuroscience vol. 8 (2014): 49. doi: https://doi.org/10.3389/fncom.2014.00049
Fiorillo CD, Kim JK, Hong SZ. The meaning of spikes from the neuron's point of view: predictive homeostasis generates the appearance of randomness. Front Comput Neurosci. 2014 Apr 29;8:49. doi: 10.3389/fncom.2014.00049. eCollection 2014. PMID: 24808854; PMCID: PMC4010728.
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Front Comput Neurosci. 2014 Apr 29;8:49. doi: 10.3389/fncom.2014.00049. eCollection 2014.

The meaning of spikes from the neuron's point of view: predictive homeostasis generates the appearance of randomness.

Frontiers in computational neuroscience

Christopher D Fiorillo, Jaekyung K Kim, Su Z Hong

Affiliations

  1. Department of Bio and Brain Engineering, Korean Advanced Institute of Science and Engineering (KAIST) Daejeon, South Korea.

PMID: 24808854 PMCID: PMC4010728 DOI: 10.3389/fncom.2014.00049

Abstract

The conventional interpretation of spikes is from the perspective of an external observer with knowledge of a neuron's inputs and outputs who is ignorant of the contents of the "black box" that is the neuron. Here we consider a neuron to be an observer and we interpret spikes from the neuron's perspective. We propose both a descriptive hypothesis based on physics and logic, and a prescriptive hypothesis based on biological optimality. Our descriptive hypothesis is that a neuron's membrane excitability is "known" and the amplitude of a future excitatory postsynaptic conductance (EPSG) is "unknown". Therefore excitability is an expectation of EPSG amplitude and a spike is generated only when EPSG amplitude exceeds its expectation ("prediction error"). Our prescriptive hypothesis is that a diversity of synaptic inputs and voltage-regulated ion channels implement "predictive homeostasis", working to insure that the expectation is accurate. The homeostatic ideal and optimal expectation would be achieved when an EPSP reaches precisely to spike threshold, so that spike output is exquisitely sensitive to small variations in EPSG input. To an external observer who knows neither EPSG amplitude nor membrane excitability, spikes would appear random if the neuron is making accurate predictions. We review experimental evidence that spike probabilities are indeed maintained near an average of 0.5 under natural conditions, and we suggest that the same principles may also explain why synaptic vesicle release appears to be "stochastic". Whereas the present hypothesis accords with principles of efficient coding dating back to Barlow (1961), it contradicts decades of assertions that neural activity is substantially "random" or "noisy". The apparent randomness is by design, and like many other examples of apparent randomness, it corresponds to the ignorance of external macroscopic observers about the detailed inner workings of a microscopic system.

Keywords: Bayesian; Jaynes; inference; neural code; noise; prediction; random; stochastic

References

  1. J Vis. 2007 Dec 28;7(14):20.1-11 - PubMed
  2. Behav Brain Sci. 2013 Jun;36(3):181-204 - PubMed
  3. J Neurosci. 2009 Nov 4;29(44):13770-84 - PubMed
  4. Nat Neurosci. 2005 Oct;8(10):1364-70 - PubMed
  5. Vision Res. 1983;23(8):775-85 - PubMed
  6. Trends Neurosci. 2010 Jun;33(6):259-66 - PubMed
  7. J Physiol. 2011 Dec 1;589(Pt 23):5801-18 - PubMed
  8. Nat Rev Neurosci. 2000 Nov;1(2):125-32 - PubMed
  9. Proc R Soc Lond B Biol Sci. 1982 Nov 22;216(1205):427-59 - PubMed
  10. Curr Opin Neurobiol. 1994 Aug;4(4):569-79 - PubMed
  11. J Comput Neurosci. 2008 Apr;24(2):235-52 - PubMed
  12. Nature. 2006 Feb 23;439(7079):936-42 - PubMed
  13. Neuron. 2010 Feb 11;65(3):422-35 - PubMed
  14. J Physiol. 2010 May 1;588(Pt 9):1647-59 - PubMed
  15. J Cereb Blood Flow Metab. 2001 Oct;21(10):1133-45 - PubMed
  16. J Neurosci. 1993 Jan;13(1):334-50 - PubMed
  17. J Neurophysiol. 1968 Jul;31(4):574-87 - PubMed
  18. J Neurosci. 1998 May 15;18(10):3870-96 - PubMed
  19. J Neurosci. 1982 Jan;2(1):32-48 - PubMed
  20. Neuron. 2000 Jun;26(3):695-702 - PubMed
  21. Nature. 2005 Jul 7;436(7047):71-7 - PubMed
  22. J Neurosci. 2008 Oct 8;28(41):10206-19 - PubMed
  23. Neural Comput. 1996 Aug 15;8(6):1185-202 - PubMed
  24. Nat Neurosci. 2003 Jun;6(6):632-40 - PubMed
  25. Science. 1995 Jun 9;268(5216):1503-6 - PubMed
  26. Curr Opin Neurobiol. 1995 Apr;5(2):239-47 - PubMed
  27. Z Naturforsch C Biosci. 1981 Sep-Oct;36(9-10):910-2 - PubMed
  28. Exp Brain Res. 1984;55(1):111-6 - PubMed
  29. Science. 2013 Aug 2;341(6145):546-9 - PubMed
  30. J Neurosci. 2005 Mar 9;25(10):2712-22 - PubMed
  31. Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7121-6 - PubMed
  32. J Neurosci. 2010 Oct 13;30(41):13567-77 - PubMed
  33. Neuron. 2005 Mar 24;45(6):917-28 - PubMed
  34. Curr Opin Neurobiol. 2011 Oct;21(5):726-33 - PubMed
  35. Nat Rev Neurosci. 2010 Feb;11(2):127-38 - PubMed
  36. J Neurosci. 2010 Oct 6;30(40):13326-37 - PubMed
  37. Nature. 2007 Sep 6;449(7158):92-5 - PubMed
  38. J Neurophysiol. 2007 Aug;98(2):807-20 - PubMed
  39. Front Psychol. 2012 May 08;3:130 - PubMed
  40. Nat Neurosci. 2010 Mar;13(3):369-78 - PubMed
  41. Science. 2007 Jan 19;315(5810):390-3 - PubMed
  42. Trends Neurosci. 1989 Feb;12(2):75-80 - PubMed
  43. Neuron. 2008 Dec 26;60(6):1142-52 - PubMed
  44. Annu Rev Neurosci. 2001;24:1193-216 - PubMed
  45. J Comput Neurosci. 1999 Jul-Aug;7(1):5-15 - PubMed
  46. Science. 2011 Jan 7;331(6013):83-7 - PubMed
  47. J Physiol. 1987 Oct;391:267-88 - PubMed
  48. Nature. 2003 May 15;423(6937):288-93 - PubMed
  49. Neuron. 2007 Aug 2;55(3):465-78 - PubMed
  50. PLoS One. 2009 Oct 02;4(10):e7014 - PubMed
  51. Nat Rev Neurosci. 2009 May;10(5):373-83 - PubMed
  52. J Neurosci. 2011 Mar 16;31(11):4260-73 - PubMed
  53. J Physiol. 2003 Mar 15;547(Pt 3):665-89 - PubMed
  54. J Neurosci. 2007 Jun 13;27(24):6461-72 - PubMed
  55. Nature. 2004 Jan 15;427(6971):244-7 - PubMed
  56. J Neurosci. 2003 Aug 27;23(21):7940-9 - PubMed
  57. Nat Rev Neurosci. 2012 Nov;13(11):798-810 - PubMed
  58. Annu Rev Physiol. 2007;69:291-316 - PubMed
  59. J Neurosci. 2006 Jan 11;26(2):448-57 - PubMed
  60. PLoS Biol. 2004 Sep;2(9):E264 - PubMed
  61. Nature. 2003 Nov 27;426(6965):442-6 - PubMed
  62. J Neurosci. 1996 May 15;16(10):3351-62 - PubMed
  63. Nat Neurosci. 1999 Jun;2(6):521-7 - PubMed
  64. J Neurophysiol. 2010 Jun;103(6):3337-48 - PubMed
  65. J Neurosci. 2006 Nov 22;26(47):12206-18 - PubMed
  66. Nature. 2010 Jul 1;466(7302):123-7 - PubMed
  67. Nature. 1998 Sep 24;395(6700):384-7 - PubMed
  68. Neural Comput. 2008 Jan;20(1):118-45 - PubMed
  69. Nat Neurosci. 2001 Aug;4(8):826-31 - PubMed
  70. J Neurosci. 2013 Mar 13;33(11):4710-25 - PubMed
  71. Nat Neurosci. 2008 May;11(5):535-7 - PubMed
  72. Proc Natl Acad Sci U S A. 1997 May 13;94(10):5411-6 - PubMed
  73. J Neurosci. 2004 Mar 17;24(11):2643-7 - PubMed
  74. J Assoc Res Otolaryngol. 2003 Mar;4(1):1-23 - PubMed
  75. PLoS One. 2008 Oct 01;3(10):e3298 - PubMed
  76. Science. 2001 Aug 10;293(5532):1159-63 - PubMed
  77. Nature. 2004 Apr 22;428(6985):856-60 - PubMed
  78. Neuron. 2011 Mar 10;69(5):885-92 - PubMed
  79. PLoS Comput Biol. 2013;9(10):e1003263 - PubMed
  80. Nature. 2003 Mar 6;422(6927):76-80 - PubMed
  81. Nat Neurosci. 2006 Nov;9(11):1432-8 - PubMed
  82. Nature. 2008 Aug 14;454(7206):881-5 - PubMed
  83. J Neurosci. 2007 Mar 7;27(10):2683-92 - PubMed
  84. Science. 1997 Mar 14;275(5306):1593-9 - PubMed
  85. Science. 2010 Apr 2;328(5974):106-9 - PubMed
  86. Nat Neurosci. 2006 May;9(5):690-6 - PubMed
  87. Neural Comput. 2008 Jan;20(1):91-117 - PubMed
  88. Cereb Cortex. 2007 Oct;17(10):2443-52 - PubMed
  89. J Neurophysiol. 2003 Jun;89(6):3279-93 - PubMed
  90. Nat Neurosci. 2002 Jun;5(6):598-604 - PubMed
  91. Neuron. 2010 Dec 22;68(6):1187-201 - PubMed
  92. Science. 1997 Mar 21;275(5307):1805-8 - PubMed
  93. J Neurophysiol. 2007 Aug;98(2):769-85 - PubMed

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