Dynamics of excitability over extended timescales in cultured cortical neurons

Journal of Neuroscience

Volumn 30, Issue 48, 2010, Pages 16332-16342

  Gal, Asaf ^a,d   Eytan, Danny ^a,e   Wallach, Avner ^a,b   Sandler, Maya ^c   Schiller, Jackie ^c   Marom, Shimon ^a,c  

^a Network Biology Research Laboratories   (Israel)

^b Faculty of Biomedical Engineering   (Israel)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^e RAMBAM MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; LATENT PERIOD; NERVE CELL CULTURE; NERVE CELL EXCITABILITY; NERVE CELL STIMULATION; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SPIKE WAVE; STIMULUS RESPONSE; TIME;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CEREBRAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIALS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 78649735564     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4859-10.2010     Document Type: Article

References (77)

1. Abeles M (1991) Corticonics: neural circuits of the cerebral cortex. Cambridge, UK: Cambridge UP.
2. Adrian ED, Zotterman Y (1926) The impulses produced by sensory nerve endings. 3. Impulses set up by touch and pressure. J Physiol 61:465-483.
3. Anderson J (1982) Acquisition of cognitive skill. Psychol Rev 89:369-406.
4. Aston-Jones G, Segal M, Bloom FE (1980) Brain aminergic axons exhibit marked variability in conduction velocity. Brain Res 195:215-222.
5. Badel L, Lefort S, Brette R, Petersen CC, Gerstner W, Richardson MJ (2008) Dynamic i-v curves are reliable predictors of naturalistic pyramidal-neuron voltage traces. J Neurophysiol 99:656-666.
6. Bakkum DJ, Chao ZC, Potter SM (2008) Long-term activity-dependent plasticity of action potential propagation delay and amplitude in cortical networks. PLoS One 3:e2088.
7. Ballo AW, Bucher D (2009) Complex intrinsic membrane properties and dopamine shape spiking activity in a motor axon. J Neurosci 29:5062-5074.
8. Barabási AL (2005) The origin of bursts and heavy tails in human dynamics. Nature 435:207-211.
9. Bassingthwaighte J, Liebovitch L, West B (1994) Fractal physiology. An American Physiological Society Book. New York: Oxford UP.
10. Beran J (1994) Statistics for long-memory processes. Boca Raton, FL: Chapman and Hall/CRC.
11. Brette R, Rudolph M, Carnevale T, Hines M, Beeman D, Bower JM, Diesmann M, Morrison A, Goodman PH, Harris FC Jr, Zirpe M, Natschläger T, Pecevski D, Ermentrout B, Djurfeldt M, Lansner A, Rochel O, Vieville T, Muller E, Davison AP, El Boustani S, Destexhe A (2007) Simulation of networks of spiking neurons: a review of tools and strategies. J Comput Neurosci 23:349-398.
12. Buzsaki G (2006) Rhythms of the brain. New York: Oxford UP.
13. Carandini M (2004) Amplification of trial-to-trial response variability by neurons in visual cortex. PLoS Biol 2:E264.
14. Chen Y, Ding M, Kelso J (1997) Long memory processes (1/f type) in human coordination. Phys Rev Lett 79:4501-4504.
15. Clauset A, Shalizi CR, Newman ME (2009) Power-law distributions in empirical data. SIAM Rev 51:661-703.
16. De Col R, Messlinger K, Carr RW (2008) Conduction velocity is regulated by sodium channel inactivation in unmyelinated axons innervating the rat cranial meninges. J Physiol 586:1089-1103.
17. Desai NS, Rutherford LC, Turrigiano GG (1999) Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat Neurosci 2:515-520.
18. Drew PJ, Abbott LF (2006) Models and properties of power-law adaptation in neural systems. J Neurophysiol 96:826-833.
19. Ellerkmann RK, Riazanski V, Elger CE, Urban BW, Beck H (2001) Slow recovery from inactivation regulates the availability of voltage-dependent sodium channels in hippocampal granule cells, hilar neurons and basket cells. J Physiol 532:385-397.
20. Elul R, Adey W (1966) Instability of firing threshold and "remote" activation in cortical neurones. Nature 212:1424-1425.
21. Englitz B, Stiefel KM, Sejnowski TJ (2008) Irregular firing of isolated cortical interneurons in vitro driven by intrinsic stochastic mechanisms. Neural Comput 20:44-64.
22. Esposti F, Ferrario M, Signorini MG (2008) A blind method for the estimation of the hurst exponent in time series: theory and application. Chaos 18:033126.
23. Esposti F, Signorini MG, Potter SM, Cerutti S (2009) Statistical long-term correlations in dissociated cortical neuron recordings. IEEE Trans Neural Syst Rehabil Eng 17:364-369.
24. Fairhall AL, Lewen GD, Bialek W, de Ruyter Van Steveninck RR (2001) Efficiency and ambiguity in an adaptive neural code. Nature 412:787-792.
25. French AS, Torkkeli PH (2008) The power law of sensory adaptation: simulation by a model of excitability in spider mechanoreceptor neurons. Ann Biomed Eng 36:153-161.
26. Freyer F, Aquino K, Robinson PA, Ritter P, Breakspear M (2009) Bistability and non-Gaussian fluctuations in spontaneous cortical activity. J Neurosci 29:8512-8524.
27. Friedlander T, Brenner N (2009) Adaptive response by state-dependent inactivation. Proc Natl Acad Sci U S A 106:22558-22563.
28. Gerstner W, Naud R (2009) How good are neuron models? Science 326: 379-380.
29. Gilboa G, Chen R, Brenner N (2005) History-dependent multiple-time-scale dynamics in a single-neuron model. J Neurosci 25:6479-6489.
30. Gilden DL (2001) Cognitive emissions of 1/f noise. Psychol Rev 108:33-56.
31. + current to somatic bursting in ca1 pyramidal cells: combined experimental and modeling study. J Neurophysiol 96:1912-1926.
32. Greenlee MW, Magnussen S (1987) Saturation of the tilt aftereffect. Vis Res 27:1041-1043.
33. Grossman Y, Parnas I, SpiraME (1979) Mechanisms involved in differential conduction of potentials at high frequency in a branching axon. J Physiol 295:307-322.
34. Heck D, Rotter S, Aertsen A (1993) Spike generation in cortical neurons: probabilistic threshold function shows intrinsic long-lasting dynamics brain theory: spatio-temporal aspects of brain function. New York: Elsevier Science.
35. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500-544.
36. Izhikevich EM (2003) Simple model of spiking neurons. IEEE Trans Neural Netw 14:1569-1572.
37. Izhikevich EM (2004) Which model to use for cortical spiking neurons? IEEE Trans Neural Netw 15:1063-1070.
38. Jolivet R, Kobayashi R, Rauch A, Naud R, Shinomoto S, Gerstner W (2008) A benchmark test for a quantitative assessment of simple neuron models. J Neurosci Methods 169:417-424.
39. Kobayashi R, Tsubo Y, Shinomoto S (2009) Made-to-order spiking neuron model equipped with a multi-timescale adaptive threshold. Front Comput Neurosci 3:9.
40. Liebovitch LS, Fischbarg J, Koniarek JP, Todorova I, Wang M (1987) Fractal model of ion-channel kinetics. Biochim Biophys Acta 896:173-180.
41. Linkenkaer-Hansen K, Nikouline VV, Palva JM, Ilmoniemi RJ (2001) Long-range temporal correlations and scaling behavior in human brain oscillations. J Neurosci 21:1370-1377.
42. Linkenkaer-Hansen K, Monto S, Rytsälä H, Suominen K, Isometsä E, Kähkönen S (2005) Breakdown of long-range temporal correlations in theta oscillations in patients with major depressive disorder. J Neurosci 25:10131-10137.
43. Logan G (1988) Toward an instance theory of automatization. Psychol Rev 95:492-527.
44. Lowen SB, Teich MC (1992) Auditory-nerve action potentials form a non-renewal point process over short as well as long time scales. J Acoust Soc Am 92:803-806.
45. Lowen SB, Teich MC (1996) The periodogram and allan variance reveal fractal exponents greater than unity in auditory-nerve spike trains. J Acoust Soc Am 99:3585-3591.
46. Lowen SB, Teich MC (2005) Fractal-based point processes. Hoboken, NJ: Wiley-Blackwell.
47. Lowen SB, Cash SS, Poo M, Teich MC (1997) Quantal neurotransmitter secretion rate exhibits fractal behavior. J Neurosci 17:5666-5677.
48. Lowen S, Liebovitch L, White J (1999) Fractal ion-channel behavior generates fractal firing patterns in neuronal models. Phys Rev E 59:5970-5980.
49. Lundstrom BN, Higgs MH, Spain WJ, Fairhall AL (2008) Fractional differentiation by neocortical pyramidal neurons. Nat Neurosci 11:1335-1342.
50. Magnussen S, Greenlee MW (1985) Marathon adaptation to spatial contrast: saturation in sight. Vis Res 25:1409-1411.
51. Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268:1503-1506.
52. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
53. Marom S (2009) Adaptive transition rates in excitable membranes. Front Comput Neurosci 3:2.
54. Marom S (2010) Neural timescales or lack thereof. Prog Neurobiol 90:16-28.
55. Marom S, Shahaf G (2002) Development, learning and memory in large random networks of cortical neurons: lessons beyond anatomy. Q Rev Biophys 35:63-87.
56. Monto S, Palva S, Voipio J, Palva JM (2008) Very slow EEG fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans. J Neurosci 28:8268-8272.
57. Newell KM, Liu YT, Mayer-Kress G (2001) Time scales in motor learning and development. Psychol Rev 108:57-82.
58. Nir Y, Fisch L, Mukamel R, Gelbard-Sagiv H, Arieli A, Fried I, Malach R (2007) Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Curr Biol 17:1275-1285.
59. Nir Y, Mukamel R, Dinstein I, Privman E, Harel M, Fisch L, Gelbard-Sagiv H, Kipervasser S, Andelman F, Neufeld MY, Kramer U, Arieli A, Fried I, Malach R (2008) Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat Neurosci 11:1100-1108.
60. Peng CK, Havlin S, Stanley HE, Goldberger AL (1995) Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos 5:82-87.
61. Robinson PM (2003) Time series with long memory. New York: Oxford UP.
62. Rose D, Lowe I (1982) Dynamics of adaptation to contrast. Perception 11:505-528.
63. Scharf R, Meesmann M, Boese J, Chialvo DR, Kniffki KD (1995) General relation between variance-time curve and power spectral density for point processes exhibiting 1/f beta-fluctuations, with special reference to heart rate variability. Biol Cybern 73:255-263.
64. Scroggs RS (2008) Evidence of a physiological role for use-dependent inactivation of nav1.8 sodium channels. J Physiol 586:923.
65. Selz K, Mandell A (1992) Critical coherence and characteristic times in brain stem neuronal discharge patterns. Single neuron computation. San Diego: Academic.
66. Shahaf G, Eytan D, Gal A, Kermany E, Lyakhov V, Zrenner C, Marom S (2008) Order-based representation in random networks of cortical neurons. PLoS Comput Biol 4:e1000228.
67. Soen Y, Braun E (2000) Scale-invariant fluctuations at different levels of organization in developing heart cell networks. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 61:R2216-R2219.
68. Soudry D, Meir R (2010) History dependent dynamics in a generic model of ion channels-an analytic study. Front Comput Neurosci 4:3.
69. Spira ME, Yarom Y, Parnas I (1976) Modulation of spike frequency by regions of special axonal geometry and by synaptic inputs. J Neurophysiol 39:882-899.
70. Tal D, Jacobson E, Lyakhov V, Marom S (2001) Frequency tuning of inputoutput relation in a rat cortical neuron in-vitro. Neurosci Lett 300:21-24.
71. Taqqu M, Teverovsky V, Willinger W (1995) Estimators for long range dependence. Fractals 3:785-798.
72. Teich MC (1989) Fractal character of the auditory neural spike train. IEEE Trans Biomed Eng 36:150-160.
73. Teich MC, Heneghan C, Lowen SB, Ozaki T, Kaplan E (1997) Fractal character of the neural spike train in the visual system of the cat. J Opt Soc Am A Opt Image Sci Vis 14:529-546.
74. + channels. J Neurosci 18:1893-1903.
75. Turrigiano G, Abbott LF, Marder E (1994) Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264:974-977. (Pubitemid 24196170)
76. van Pelt J, Wolters PS, Corner MA, Rutten WL, Ramakers GJ (2004) Longterm characterization of firing dynamics of spontaneous bursts in cultured neural networks. IEEE Trans Biomed Eng 51:2051-2062.
77. Wink AM, Bullmore E, Barnes A, Bernard F, Suckling J (2008) Monofractal and multifractal dynamics of low frequency endogenous brain oscillations in functional mri. Hum Brain Mapp 29:791-801.