Heterosynaptic plasticity prevents runaway synaptic dynamics

Journal of Neuroscience

Volumn 33, Issue 40, 2013, Pages 15915-15929

  Chen, Jen Yung ^a   Lonjers, Peter ^a   Lee, Christopher ^b   Chistiakova, Marina ^b   Volgushev, Maxim ^b   Bazhenov, Maxim ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; CALCIUM TRANSPORT; CONTROLLED STUDY; DEPRESSION; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; INTRACELLULAR RECORDING; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SODIUM TRANSPORT; SPIKE WAVE; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; VISUAL CORTEX;

EID: 84884963409     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5088-12.2013     Document Type: Article

References (101)

1. Abbott LF, Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci 3:1178-1183. CrossRef Medline
2. Abbott LF, Varela JA, Sen K, Nelson SB (1997) Synaptic depression and cortical gain control. Science 275:220-224. Medline
3. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126-130. CrossRef Medline
4. Aitkin LM, Anderson DJ, Brugge JF (1970) Tonotopic organization and discharge characteristics of single neurons in nuclei of the lateral lemniscus of the cat. J Neurophysiol 33:421-440. Medline
5. Alzheimer C, Schwindt PC, Crill WE (1993) Modal gating of Na+ channels as a mechanism of persistent Na+ current in pyramidal neurons from rat and cat sensorimotor cortex. J Neurosci 13:660-673. Medline
6. Astman N, Gutnick MJ, Fleidervish IA (2006) Persistent sodium current in layer 5 neocortical neurons is primarily generated in the proximal axon. J Neurosci 26:3465-3473. CrossRef Medline
7. Babadi B, Abbott LF (2010) Intrinsic Stability of Temporally Shifted Spike- Timing Dependent Plasticity. PLoS Comput Biol 6:e1000961. CrossRef
8. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ (2002) Model of thalamocortical slow-wave sleep oscillations and transitions to activated states. J Neurosci 22:8691-8704. Medline
9. Bazhenov M, Stopfer M, Sejnowski TJ, Laurent G (2005) Fast odor learning improves reliability of odor responses in the locust antennal lobe. Neuron 46:483-492. CrossRef Medline
10. 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. Medline
11. 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. Medline
12. Birtoli B, Ulrich D (2004) Firing mode-dependent synaptic plasticity in rat neocortical pyramidal neurons. J Neurosci 24:4935-4940. CrossRef Medline
13. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39. CrossRef Medline
14. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331-356.
15. Bloodgood BL, Sabatini BL (2007) Ca2+signaling in dendritic spines. Cucc Opinion in Neurobiol 17:345-351. CrossRef
16. Bonhoeffer T, Staiger V, Aertsen A (1989) Synaptic plasticity in rat hippocampal slice cultures: local "Hebbian" conjunction of pre- and postsynaptic stimulation leads to distributed synaptic enhancement. Proc Natl Acad Sci U S A 86:8113-8117. CrossRef Medline
17. Caporale N, Dan Y (2008) Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 31:25-46. CrossRef Medline
18. Chen JY, Chauvette S, Skorheim S, Timofeev I, Bazhenov M (2012) Interneuron-mediated inhibition synchronizes neuronal activity during slow oscillation. J Physiol 590:3987-4010. CrossRef Medline
19. Chistiakova M, Volgushev M (2009) Heterosynaptic plasticity in the neocortex. Exp Brain Res 199:377-390. CrossRef Medline
20. 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. CrossRef Medline
21. D'Agostino RB, Belanger A, D'Agostino RB Jr (1990) A suggestion for using powerful and informative testes of normality. Am Stat 44:316-321.CrossRef
22. Delgado JY, Gómez-González JF, Desai NS (2010) Pyramidal neuron conductance state gates spike-timing-dependent plasticity. J Neurosci 30: 15713-15725. CrossRef Medline
23. Destexhe A, Marder E (2004) Plasticity in single neuron and circuit computations. Nature 431:789-795. CrossRef Medline
24. Destexhe A, Paré D (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81: 1531-1547. Medline
25. Destexhe A, Mainen ZF, Sejnowski TJ (1994) Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J Comp Neurosci 1:195-230. CrossRef
26. Elliott T, Shadbolt NR (2002) Multiplicative synaptic normalization and a nonlinear Hebb rule underlie a neurotrophic model of competitive synaptic plasticity. Neural Comput 14:1311-1322. CrossRef Medline
27. Engert F, Bonhoeffer T (1997) Synapse specificity of long-term potentiation breaks down at short distances. Nature 388:279-284. CrossRef Medline
28. Feldman DE (2009) Synaptic mechanisms for plasticity in neocortex. Annu Rev Neurosci 32:33-55. CrossRef Medline
29. Finelli LA, Haney S, Bazhenov M, Stopfer M, Sejnowski TJ (2008) Synaptic learning rules and sparse coding in a model sensory system. PLoS Comput Biol 4:e1000062. CrossRef
30. Fröhlich F, Bazhenov M (2006) Coexistence of tonic firing and bursting in cortical neurons. Phys Rev E Stat Nonlin Soft Matter Phys 74:031922. CrossRef Medline
31. Fröhlich F, Bazhenov M, Sejnowski TJ (2008) Pathological effect of homeostatic synaptic scaling on network dynamics in diseases of the cortex. J Neurosci 28:1709-1720. CrossRef Medline
32. Fröhlich F, Sejnowski TJ, Bazhenov M (2010) Network bistability mediates spontaneous transitions between normal and pathological brain states. J Neurosci 30:10734-10743. CrossRef Medline
33. Galarreta M, Hestrin S (1998) Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci 1:587-594. CrossRef Medline
34. Gilson M, Fukai T (2011) Stability versus neuronal specialization for STDP: long-tail weight distributions solve the dilemma. PLoS ONE 6:e25339. CrossRef
35. Graupner M, Brunel N (2010) Mechanisms of induction and maintenance of spike-timing dependent plasticity in biophysical synapse models. Front Comput Neurosci 4:136. CrossRef Medline
36. Gütig R, Aharonov R, Rotter S, Sompolinsky H (2003) Learning input correlations through nonlinear temporally asymmetric Hebbian plasticity. J Neurosci 23:3697-3714. Medline
37. Haas JS, Nowotny T, Abarbanel HD (2006) Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex. J Neurophysiol 96: 3305-3313. CrossRef Medline
38. Hansel C, Artola A, Singer W (1997) Relation between dendritic Ca2+ levels and the polarity of synaptic long-term modifications in rat visual cortex neurons. Eur J Neurosci 9:2309-2322. CrossRef Medline
39. Hardingham NR, Hardingham GE, Fox KD, Jack JJ (2007) Presynaptic efficacy directs normalization of synaptic strength in layer 2/3 rat neocortex after paired activity. J Neurophysiol 97:2965-2975. CrossRef Medline
40. Ismailov I, Kalikulov D, Inoue T, Friedlander MJ (2004) The kinetic profile of intracellular calcium predicts long-term potentiation and long-term depression. J Neurosci 24:9847-9861. CrossRef Medline
41. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10:100-107. CrossRef Medline
42. Kay AR, Sugimori M, Llinas R (1998) Kinetic and stochastic properties of a persistent sodium current in mature guinea pig cerebellar Purkinje cells. J Neurophysiol 80:1167-1179. Medline
43. Kempter R, Gerstner W, van Hemmen JL (1999) Hebbian learning and spiking neurons. Phys Rev E 59:4498-4514. CrossRef
44. Kempter R, Gerstner W, van Hemmen JL (2001) Intrinsic stabilization of output rates by spike-based Hebbian learning. Neural Comp 13:2709-2741. CrossRef
45. Kossel A, Bonhoeffer T, Bolz J (1990) Non-Hebbian synapses in rat visual cortex. Neuroreport 1:115-118. CrossRef Medline
46. Kuhnt U, Kleschevnikov AM, Voronin LL (1994) Long-term enhancement of synaptic transmission in the hippocampus after tetanization of single neurons by short intracellular current pulses. Neurosci Res Communications 14:115-123.
47. Kuznetsov Y (1995) Elements of applied bifurcation theory. New York: Springer.
48. Larkman A, Hannay T, Stratford K, Jack J (1992) Presynaptic release probability influences the locus of long-term potentiation. Nature 360:70-73. CrossRef Medline
49. Lee CM, Stoelzel C, Chistiakova M, Volgushev M (2012) Heterosynaptic plasticity induced by intracellular tetanization in layer 2/3 pyramidal neurons in rat auditory cortex. J Physiol 590 10:2253-2271.
50. 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. CrossRef Medline
51. Lüscher C, Nicoll RA, Malenka RC, Muller D (2000) Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3:545-550. CrossRef Medline
52. Lynch GS, Dunwiddie T, Gribkoff V (1977) Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature 266:737-739. CrossRef Medline
53. Magee JC, Johnston D (1997) A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275:209-213. CrossRef Medline
54. Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363-366. CrossRef Medline
55. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21. CrossRef Medline
56. Malenka RC, Kauer JA, Zucker RS, Nicoll RA (1988) Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science 242:81-84. CrossRef Medline
57. Malinow R, Mainen ZF, Hayashi Y (2000) LTP mechanisms: from silence to four-lane traffic. Curr Opin Neurobiol 10:352-357. CrossRef Medline
58. Manninen T, Hituri K, Kotaleski JH, Blackwell KT, Linne ML (2010) Postsynaptic signal transduction models for long-term potentiation and depression. Frontiers Comput Neurosci 4:152. CrossRef Medline
59. Markram H, Tsodyks M (1996) Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature 382:807-810. CrossRef Medline
60. Markram H, Lüebke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215. CrossRef Medline
61. Merzenich MM, Knight PL, Roth GL (1975) Representation of cochlea within primary auditory cortex in the cat. J Neurophysiol 38:231-249. Medline
62. Miller KD (1996) Synaptic economics: competition and cooperation in synaptic plasticity. Neuron 17:371-374. CrossRef Medline
63. Miller KD, MacKay DJ (1993) The role of constraints in Hebbian learning. Neural Comput 6:100-126.
64. Miyakawa H, Ross WN, Jaffe D, Callaway JC, Lasser-Ross N, Lisman JE, Johnston D (1992) Synaptically activated increases in Ca2+ concentration in hippocampal CA1 pyramidal cells are primarily due to voltagegated Ca2+ channels. Neuron 9:1163-1173. CrossRef Medline
65. Morrison A, Aertsen A, Diesmann M (2007) Spike-timing-dependent plasticity in balanced random networks. Neural Comp 19:1437-1467. CrossRef
66. Neveu D, Zucker RS (1996) Long-lasting potentiation and depression without presynaptic activity J Neurophysiol 75:2157-2160.
67. Nevian T, Sakmann B (2006) Single spine Ca2+ signals evoked by coincident EPSPs and backpropagating action potentials in spiny stellate cells of layer 4 in the juvenile rat somatosensory barrel cortex. J Neurosci 26: 11001-11013. CrossRef Medline
68. Nishiyama M, Hong K, Mikoshiba K, Poo MM, Kato K (2000) Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 408:584-588. CrossRef Medline
69. Oja E (1982) A simplified neuron model as a principal component analyzer. J Math Biol 15:267-273. CrossRef Medline
70. Peyrache A, Khamassi M, Benchenane K, Wiener SI, Battaglia FP (2009) Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci 12:919-926. CrossRef Medline
71. Royer S, Paré D (2003) Conservation of total synaptic weight through balanced synaptic depression and potentiation. Nature 422:518-522. CrossRef Medline
72. Rubin J, Lee DD, Sompolinsky H (2001) Equilibrium properties of temporally asymmetric Hebbian plasticity. Phys Rev Lett 86:364-367. CrossRef Medline
73. Schiller J, Schiller Y, Clapham DE (1998) NMDAreceptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat Neurosci 1:114-118. CrossRef Medline
74. Schuman EM, Madison DV (1994) Locally distributed synaptic potentiation in the hippocampus. Science 263:532-536. CrossRef Medline
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. CrossRef Medline
76. Sjöström PJ, Turrigiano GG, Nelson SB (2001) Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32:1149-1164. CrossRef Medline
77. Sjöström PJ, Turrigiano GG, Nelson SB (2007) Multiple forms of long-term plasticity at unitary neocortical layer 5 synapses. Neuropharmacology 52:176-184. CrossRef Medline
78. Song S, Abbott LF (2001) Cortical development and remapping through spike timing-dependent plasticity. Neuron 32:339-350. CrossRef Medline
79. Song S, Miller KD, Abbott LF (2000) Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci 3:919-926. CrossRef Medline
80. Song S, Sjöström PJ, Reigl M, Nelson S, Chklovskii DB (2005) Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 3:e68. CrossRef
81. Stuart GJ, Häusserm (2001) Dendritic coincidence detection of EPSPs and action potentials. Nat Neurosci 4:63-71. CrossRef Medline
82. Thompson ID, Kossut M, Blakemore C (1983) Development of orientation columns in cat striate cortex revealed by 2-deoxyglucose autoradiography. Nature 301:712-715. CrossRef Medline
83. Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M (2000) Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex 10:1185-1199. CrossRef Medline
84. Trujillo-Ortiz A, Hernandez-Walls R (2003) DagosPtest: D'Agostino- Pearson's K2 test for assessing normality of data using skewness and kurtosis. MATLAB file. http://www.mathworks.com/matlabcentral/fileexchange/loadFile.do?objectId_3954&objectType_FILE
85. Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A 94:719-723. CrossRef Medline
86. Turrigiano GG (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135:422-435. CrossRef Medline
87. van Rossum MC, Bi GQ, Turrigiano GG (2000) Stable Hebbian learning from spike timing-dependent plasticity. J Neurosci 20:8812-8821. Medline
88. Vitureira N, Letellier M, Goda Y (2012) Homeostatic synaptic plasticity: from single synapses to neural circuits. Curr Opin Neurobiol 22:516-521. CrossRef Medline
89. Volgushev M, Voronin LL, Chistiakova M, Singer W (1994) Induction of LTP and LTD in visual cortex neurons by intracellular tetanization. Neuroreport 5:2069-2072. CrossRef Medline
90. Volgushev M, Voronin LL, Chistiakova M, Singer W (1997) Relations between long-term synaptic modifications and paired-pulse interactions in the rat neocortex. Eur J Neurosci 9:1656-1665. CrossRef Medline
91. Volgushev M, Mittmann T, Chistiakova M, Balaban P, Eysel UT (1999) Interaction between intracellular tetanization and pairing-induced longterm synaptic plasticity in the rat visual cortex. Neuroscience 93:1227-1232. CrossRef Medline
92. Volgushev M, Balaban P, Chistiakova M, Eysel UT (2000) Retrograde signalling with nitric oxide at neocortical synapses. Eur J Neurosci 12:4255-4267. CrossRef Medline
93. von der Malsburg C (1973) Self-organization of orientation sensitive cells in the striate cortex. Kybernetik 14:85-100. CrossRef Medline
94. White G, Levy WB, Steward O (1990) Spatial overlap between populations of synapses determines the extent of their associative interaction during the induction of long-term potentiation and depression. J Neurophysiol 64:1186-1198. Medline
95. Wiesel TN, Hubel DH (1963) Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. J Neurophysiol 26:978-993. Medline
96. Wu Z, Yamaguchi Y (2006) Conserving total synaptic weight ensures onetrial sequence learning of place fields in the hippocampus. Neural Netw 19:547-563. CrossRef Medline
97. Yang SN, Tang YG, Zucker RS (1999) Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. J Neurophysiol 81:781-787. Medline
98. Yasuda R, Sabatini BL, Svoboda K (2003) Plasticity of calcium channels in dendritic spines. Nat Neurosci 6:948-955. CrossRef Medline
99. Yeung LC, Shouval HZ, Blais BS, Cooper LN (2004) Synaptic homeostasis and input selectivity follow from a calcium-dependent plasticity model. Proc Natl Acad Sci U S A 101:14943-14948. CrossRef Medline
100. Yuste R, Denk W (1995) Dendritic spines as basic functional units of neuronal integration. Nature 375:682-684. CrossRef Medline
101. Zhou YD, Acker CD, Netoff TI, Sen K, White JA (2005) Increasing Ca2+ transients by broadening postsynaptic action potentials enhances timingdependent synaptic depression. Proc Natl Acad Sci U S A 102:19121-19125. CrossRef Medline