Stable learning in stochastic network states

Journal of Neuroscience

Volumn 32, Issue 1, 2012, Pages 194-214

  El Boustani, Sami ^a   Yger, Pierre ^a   Frégnac, Yves ^a   Destexhe, Alain ^a  

^a Unite de Neurosciences Integratives et Computationnelles   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ALGORITHM; ANIMAL; ARTICLE; ARTIFICIAL NEURAL NETWORK; BIOLOGICAL MODEL; BRAIN CORTEX; HUMAN; LEARNING; NERVE CELL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; PHYSIOLOGY; STATISTICS;

ACTION POTENTIALS; ALGORITHMS; ANIMALS; CEREBRAL CORTEX; HUMANS; LEARNING; MODELS, NEUROLOGICAL; NERVE NET; NEURAL NETWORKS (COMPUTER); NEURONAL PLASTICITY; NEURONS; STOCHASTIC PROCESSES;

EID: 84855965119     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2496-11.2012     Document Type: Article

References (94)

1. Abraham WC (2008) Metaplasticity: tuning synapses and networks for plasticity. Nat Rev Neurosci 9:387.
2. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126-130.
3. Artola A, Singer W (1993) Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci 16:480-487.
4. Artola A, Bröcher S, Singer W (1990) Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347:69-72.
5. Badoual M, Zou Q, Davison AP, Rudolph M, Bal T, Frégnac Y, Destexhe A (2006) Biophysical and phenomenological models of multiple spike interactions in spike-timing dependent plasticity. Int J Neural Syst 16:79-97.
6. Bar Ilan L, Gidon A, Segev I (2011) Inter-regional synaptic competition in neurons with multiple STDP-inducing signals. J Neurophysiol 105:989-998.
7. Bear MF (1995) Mechanism for a sliding synaptic modification threshold. Neuron 15:1-4.
8. Bell CC, Han VZ, Sugawara Y, Grant K (1997) Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387:278-281.
9. Benucci A, Frazor RA, Carandini M (2007) Standing waves and traveling waves distinguish two circuits in visual cortex. Neuron 55:103-117.
10. Benuskova L, Abraham WC (2007) STDP rule endowed with the BCM sliding threshold accounts for hippocampal heterosynaptic plasticity. J Comput Neurosci 22:129-133.
11. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464-10472.
12. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32-48.
13. Bringuier V, Chavane F, Glaeser L, Frégnac Y (1999) Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 283:695-699.
14. Brunel N (2000) Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J Comput Neurosci 8:183-208.
15. Burkitt AN, Meffin H, Grayden DB (2004) Spike-timing-dependent plasticity: the relationship to rate-based learning for models with weight dynamics determined by a stable fixed point. Neural Comput 16:885-940.
16. Bush D, Philippides A, Husbands P, O'Shea M (2010) Reconciling the STDP and BCM models of synaptic plasticity in a spiking recurrent neural network. Neural Comput 22:2059-2085.
17. Christie BR, Abraham WC (1992) Priming of associative long-term depression in the dentate gyrus by theta frequency synaptic activity. Neuron 9:79-84.
18. Clopath C, Büsing L, Vasilaki E, Gerstner W (2010) Connectivity reflects coding: a model of voltage-based stdp with homeostasis. Nat Neurosci 13:344-352.
19. Davison AP, Brüderle D, Eppler J, Kremkow J, Muller E, Pecevski D, Perrinet L, Yger P (2008) PyNN: a common interface for neuronal network simulators. Front Neuroinform 2:11.
20. Deisseroth K, Bito H, Schulman H, Tsien RW (1995) Synaptic plasticity: a molecular mechanism for metaplasticity. Curr Biol 5:1334-1338.
21. Destexhe A, Hughes SW, Rudolph M, Crunelli V (2007) Are corticothalamic "up" states fragments of wakefulness? Trends Neurosci 30:334-342.
22. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51-86.
23. Dunfield D, Haas K (2009) Metaplasticity governs natural experiencedriven plasticity of nascent embryonic brain circuits. Neuron 64:240-250.
24. El Boustani S, Destexhe A (2009) A master equation formalism for macroscopic modeling of asynchronous irregular activity states. Neural Comput 21:46-100.
25. El Boustani S, Pospischil M, Rudolph-Lilith M, Destexhe A (2007) Activated cortical states: experiments, analyses and models. J Physiol Paris 101:99-109.
26. Elgersma Y, Fedorov NB, Ikonen S, Choi ES, Elgersma M, Carvalho OM, Giese KP, Silva AJ (2002) Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity, and learning. Neuron 36:493-505.
27. 2+ signals. Nat Neurosci 14:301-304.
28. Frégnac Y (2002) Hebbian synaptic plasticity. In: Handbook of brain theory and neural networks (Arbib MA, ed), pp 512-522. Cambridge, MA: MIT.
29. Frégnac Y (1999) A tale of two spikes. Nat Neurosci 2:299-301.
30. Frégnac Y, Shulz D, Thorpe S, Bienenstock E (1988) A cellular analogue of visual cortical plasticity. Nature 333:367-370.
31. Fu YX, Djupsund K, Gao H, Hayden B, Shen K, Dan Y (2002) Temporal specificity in the cortical plasticity of visual space representation. Science 296:1999-2003.
32. Fu YX, Shen Y, Gao H, Dan Y (2004) Asymmetry in visual cortical circuits underlying motion-induced perceptual mislocalization. J Neurosci 24:2165-2171.
33. Fusi S, Drew PJ, Abbott LF (2005) Cascade models of synaptically stored memories. Neuron 45:599-611.
34. Gais S, Plihal W, Wagner U, Born J (2000) Early sleep triggers memory for early visual discrimination skills. Nat Neurosci 3:1335-1339.
35. Gerstner W, Kempter R, van Hemmen JL, Wagner H (1996) A neuronal learning rule for sub-millisecond temporal coding. Nature 383:76-81.
36. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ (1998) Autophosphorylation at thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279:870-873.
37. Gilson M, Burkitt A, van Hemmen LJ (2010) Stdp in recurrent neuronal networks. Front Comput Neurosci 4.pii:23.
38. Gold PE (2008) Protein synthesis inhibition and memory: formation vs amnesia. Neurobiol Learn Mem 89:201-211.
39. Graef IA, Mermelstein PG, Stankunas K, Neilson JR, Deisseroth K, Tsien RW, Crabtree GR (1999) L-type calcium channels and gsk-3 regulate the activity of nf-atc4 in hippocampal neurons. Nature 401:703-708.
40. Graupner M, Brunel N (2007) Stdp in a bistable synapse model based on CaMKII and associated signaling pathways. PLoS Comput Biol 3:e221.
41. 2+/calmodul independent protein kinase II activity by dopamine D4 receptors in prefrontal cortex. Mol Pharmacol 66:948-955.
42. Gütig R, Aharonov R, Rotter S, Sompolinsky H (2003) Learning input correlations through nonlinear temporally asymmetric hebbian plasticity. J Neurosci 23:3697-3714.
43. Harvey CD, Yasuda R, Zhong H, Svoboda K (2008) The spread of ras activity triggered by activation of a single dendritic spine. Science 321:136-140.
44. Huang YY, Colino A, Selig DK, Malenka RC (1992) The influence of prior synaptic activity on the induction of long-term potentiation. Science 255:730-733.
45. Iannella NL, Launey T, Tanaka S (2010) Spike timing-dependent plasticity as the origin of the formation of clustered synaptic efficacy engrams. Front Comput Neurosci 4.pii:21.
46. Izhikevich EM, Desai NS (2003) Relating STDP to BCM. Neural Comput 15:1511-1523.
47. Izhikevich EM, Gally JA, Edelman GM (2004) Spike-timing dynamics of neuronal groups. Cereb Cortex 14:933-944.
48. Jia H, Rochefort NL, Chen X, Konnerth A (2010) Dendritic organization of sensory input to cortical neurons in vivo. Nature 464:1307-1312.
49. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10:100-107.
50. Kang S, Kitano K, Fukai T (2008) Structure of spontaneous up and down transitions self-organizing in a cortical network model. PLoS Comput Biol 4:e1000022.
51. Kasamatsu T, Pettigrew JD (1976) Depletion of brain catecholamines: failure of ocular dominance shift after monocular occlusion in kittens. Science 194:206-209.
52. Kumar A, Schrader S, Aertsen A, Rotter S (2008) The high-conductance state of cortical networks. Neural Comput 20:1-43.
53. Legenstein R, Pecevski D, Maass W (2008) A learning theory for rewardmodulated spike-timing-dependent plasticity with application to biofeedback. PLoS Comput Biol 4:e1000180.
54. Levy WB, Steward O (1983) Temporal contiguity requirements for longterm associative potentiation/depression in the hippocampus. Neuroscience 8:791-797.
55. Lisman J (1989) A mechanism for the hebb and the anti-hebb processes underlying learning and memory. Proc Natl Acad Sci U S A 86:9574-9578.
56. Lisman J (1994) The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci 17:406-412.
57. Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175-190.
58. Lubenov EV, Siapas AG (2008) Decoupling through synchrony in neuronal circuits with propagation delays. Neuron 58:118-131.
59. Markram H, Lübke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215.
60. Marre O, Yger P, Davison AP, Frégnac Y (2009) Reliable recall of spontaneous activity patterns in cortical networks. J Neurosci 29:14596-14606.
61. Mayford M, Wang J, Kandel ER, O'Dell TJ (1995) CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and LTP. Cell 81:891-904.
62. McGaugh JL (2000) Memory: a century of consolidation. Science 287:248-251.
63. Mehta MR, Quirk MC, Wilson MA (2000) Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron 25:707-715.
64. Mockett B, Coussens C, Abraham WC (2002) NMDA receptor-mediated metaplasticity during the induction of long-term depression by lowfrequency stimulation. Eur J Neurosci 15:1819-1826.
65. Morrison A, Aertsen A, Diesmann M (2007) Spike-timing-dependent plasticity in balanced random networks. Neural Comput 19:1437-1467.
66. Okamoto H, Ichikawa K (1994) Model for an enzymatic reaction-diffusion system realizing storage of graded information. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 50:1704-1707.
67. Pawlak V, Kerr JN (2008) Dopamine receptor activation is required for corticostriatal spike-timing-dependent plasticity. J Neurosci 28:2435-2446.
68. Pawlak V, Wickens JR, Kirkwood A, Kerr JN (2010) Timing is not everything: neuromodulation opens the stdp gate. Front Synaptic Neurosci 2:146.
69. Pfister JP, Gerstner W (2006) Triplets of spikes in a model of spike timingdependent plasticity. J Neurosci 26:9673-9682.
70. Pi HJ, Otmakhov N, Lemelin D, De Koninck P, Lisman J (2010) Autonomous camkii can promote either long-term potentiation or long-term depression, depending on the state of t305/t306 phosphorylation. J Neurosci 30:8704-8709.
71. Renart A, de la Rocha J, Bartho P, Hollender L, Parga N, Reyes A, Harris KD (2010) The asynchronous state in cortical circuits. Science 327:587-590.
72. Romo R, Schultz W (1990) Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements. J Neurophysiol 63:592-606.
73. Sejnowski TJ (1977) Statistical constraints on synaptic plasticity. J Theor Biol 69:385-389.
74. Senn W, Markram H, Tsodyks M (2001) An algorithm for modifying neurotransmitter release probability based on pre-and postsynaptic spike timing. Neural Comput 13:35-67.
75. Seol GH, Ziburkus J, Huang S, Song L, Kim IT, Takamiya K, Huganir RL, Lee HK, Kirkwood A (2007) Neuromodulators control the polarity of spiketiming-dependent synaptic plasticity. Neuron 55:919-929.
76. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870-3896.
77. Shen W, Flajolet M, Greengard P, Surmeier DJ (2008) Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321:848-851.
78. Shouval HZ, Castellani GC, Blais BS, Yeung LC, Cooper LN (2002) Converging evidence for a simplified biophysical model of synaptic plasticity. Biol Cybern 87:383-391.
79. Sjöström PJ, Turrigiano GG, Nelson SB (2001) Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32:1149-1164.
80. Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334-350.
81. Song S, Abbott LF (2001) Cortical development and remapping through spike timing-dependent plasticity. Neuron 32:339-350.
82. Song S, Miller KD, Abbott LF (2000) Competitive hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci 3:919-926.
83. Steriade M (2001) Impact of network activities on neuronal properties in corticothalamic systems. J Neurophysiol 86:1-39.
84. Stickgold R, Hobson JA, Fosse R, Fosse M (2001) Sleep, learning, and dreams: off-line memory reprocessing. Science 294:1052-1057.
85. Tronson NC, Taylor JR (2007) Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci 8:262-275.
86. van Rossum MC, Bi GQ, Turrigiano GG (2000) Stable hebbian learning from spike timing-dependent plasticity. J Neurosci 20:8812-8821.
87. Vinje WE, Gallant JL (2000) Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287:1273-1276.
88. Vogels TP, Abbott LF (2005) Signal propagation and logic gating in networks of integrate-and-fire neurons. J Neurosci 25:10786-10795.
89. Wang HX, Gerkin RC, Nauen DW, Bi GQ (2005) Coactivation and timingdependent integration of synaptic potentiation and depression. Nat Neurosci 8:187-193.
90. Wang Y, Wu J, Rowan MJ, Anwyl R (1998) Role of protein kinase c in the induction of homosynaptic long-term depression by brief low frequency stimulation in the dentate gyrus of the rat hippocampus in vitro. J Physiol 513:467-475.
91. Yu X, Shouval HZ, Knierim JJ (2008) A biophysical model of synaptic plasticity and metaplasticity can account for the dynamics of the backward shift of hippocampal place fields. J Neurophysiol 100:983-992.
92. Zhang JC, Lau PM, Bi GQ (2009) Gain in sensitivity and loss in temporal contrast of STDP by dopaminergic modulation at hippocampal synapses. Proc Natl Acad Sci U S A 106:13028-13033.
93. 2+/calmodulin-dependent kinase II. J Neurosci 25:7697-7707.
94. Zhou Q, Tao HW, Poo MM (2003) Reversal and stabilization of synaptic modifications in a developing visual system. Science 300:1953-1957.