Interaction of inhibition and triplets of excitatory spikes modulates the NMDA-R-mediated synaptic plasticity in a computational model of spike timing-dependent plasticity

Hippocampus

Volumn 23, Issue 1, 2013, Pages 75-86

  Cutsuridis, Vassilis ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

CA1 pyramidal cell; Calcium; Computational model; Hippocampus; Inhibition; NMDA; STDP; Triplets

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ARTICLE; DENDRITE; HIPPOCAMPAL CA1 REGION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MATHEMATICAL MODEL; NERVE CELL PLASTICITY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; SPIKE; SPIKE TIMING DEPENDENT PLASTICITY;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNELS; COMPUTER SIMULATION; DENDRITES; HUMANS; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURONAL PLASTICITY; POTASSIUM CHANNELS; PYRAMIDAL CELLS; RECEPTORS, AMPA; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SODIUM CHANNELS; TIME FACTORS;

EID: 84870915478     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22057     Document Type: Article

References (75)

1. 2+ dynamics in the hippocampal CA1 network. Neuroscience 145: 80-87.
2. Allen C, Stevens CF. 1994. An evaluation of causes for unreliability of synaptic transmission. Proc Natl Acad Sci USA 91: 10380-10383.
3. Abarbanel HDI, Gibb L, Huerta R, Rabinovich MI. 2003. Biophysical model of synaptic plasticity dynamics. Biol Cybern 89: 214-226.
4. Bear MF, Cooper LN, Ebner FF. 1987. A physiological basis for a theory of synapse modification. Science 237: 42-48.
5. Bell CC, Han VZ, Sugawara Y, Grant K. 1997. Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387: 278-281.
6. Bender VA, Bender KJ, Brasier DJ, Feldman DE. 2006. Two coincidence detectors for spike-timing-dependent plasticity in somatosensory cortex. J Neurosci 26: 4166-4177.
7. Bi GQ. 2002. Spatiotemporal specificity of synaptic plasticity: Cellular rules and mechanisms. Biol Cybern 87: 319-332.
8. 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.
9. Bland BH. 1986. The physiology and pharmacology of hippocampal formation of theta rhythms. Prog Neurobiol 26: 1-54.
10. Bliss TV, Lomo T. 1970. Plasticity in a monosynaptic cortical pathway. J Physiol 207: 61.
11. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361: 31-39.
12. Buzsáki G. 2002. Theta oscillations in the hippocampus. Neuron 33: 325-340.
13. Caporale N, Dan Y. 2009. Spike timing dependent plasticity: A Hebbian learning rule. Ann Rev Neurosci 31: 25-46.
14. Cassenaer S, Laurent G. 2007. Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448: 709-713.
15. Cho K, Aggleton JP, Brown MW, Bashir ZI. 2001. An experimental test of the role of postsynaptic calcium levels in determining synaptic strength using perirhinal cortex of rat. J Physiol (London) 532: 459-466.
16. Cobb SR, Buhl EH, Halacy K, Paulsen O, Somogyi P. 1995. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378: 75-77.
17. Cutsuridis V. 2012. Bursts shape the NMDA-R mediated spike timing dependent plasticity curve: Role of burst interspike interval and GABA inhibition. Cognitive Neurodynamics, DOI: 10.1007/s11571-012-9205-1.
18. Cutsuridis V. 2011. GABA inhibition modulates NMDA-R mediated spike timing-dependent plasticity (STDP) in a biophysical model. Neural Networks 24: 29-42.
19. Cutsuridis V, Cobb S, Graham BP. 2009. How bursts shape the STDP curve in the presence/absence of GABA inhibition. In Alippi C, Polycarpou M, Panayiotou C, Ellinas G, editors. LNCS 5768; Berlin Heidelberg: Springer-Verlag. pp 229-238.
20. Cutsuridis V. 2010. Action potential bursts modulate the NMDA-R mediated spike timing dependent plasticity in a biophysical model. In Diamantaras K, Duch W, Iliadis LS, editors. ICANN 2010, Part I, LNCS 6352; Berlin Heidelberg: Springer-Verlag. pp 107-116.
21. Debanne D, Gahwiler BH, Thompson SM. 1998. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol 507: 237-247.
22. Dudek SM, Bear MF. 1993. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 13: 2910-2918.
23. Dunwiddie T, Lynch G. 1978. Long-term potentiation and depression of synaptic responses in the rat hippocampus: Localization and frequency dependency. J Physiol 276: 353-367.
24. Ermentrout B. 2002. Simulating, Analyzing and Animating Dynamical Systems. A Guide to XPPAUT for Researchers and Students. Philadelphia: SIAM.
25. Feldman DE. 2000. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27: 45-56.
26. Froemke R, Dan Y. 2002. Spike timing dependent plasticity depends on dendritic location. Nature 416: 221-225.
27. Froemke RC, Poo MM, Dan Y. 2005. Spike timing-dependent plasticity depends on dendritic location. Nature 434: 221-225.
28. Froemke R, Tsay I, Raad M, Long J, Dan Y. 2006. Contribution of individual spikes in burst-induced long-term synaptic modification. J Neurophysiol 95: 1620-1629.
29. Gall D, Prestori F, Sola E, D'Errico A, Roussel C, Forti L, Rossi R, D'Angelo E. 2005. Intracellular calcium regulation by burst discharge determines bidirectional long-term synaptic plasticity at the cerebellum input stage. J Neurosci 25: 4813-4822.
30. Gloveli T, Kopell N, Dugladze T. 2010. Network activity patterns during hippocampal network oscillations in vitro. In Cutsuridis V, Graham BP, Cobb S, Vida I, editors. Hippocampal Microcircuits: A Computational Modeler's Resource Book (Springer Series in Computational Neuroscience 5). New York, USA: Springer Science + Business Media. pp 247-276.
31. Grover LM, Kim E, Cooke JD, Holmes WR. 2009. LTP in hippocampal area CA1 is induced by burst stimulation over a broad frequency range centered around delta. Learn Mem 16: 69-81.
32. i have to be reached to induce LTP and LTD in neocortical pyramidal cells. J Physiol (Paris) 90: 317-319.
33. 2+ levels and the polarity of synaptic long-term modifications in rat visual cortex neurons. Eur J Neurosci 9: 2309-2322.
34. Harvey CD, Svoboda K. 2007. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450: 1195-1200.
35. Hebb DO. 1949. The Organization of Behavior. New York: Wiley.
36. Hennequin G, Gerstner W, Pfister JP. 2010. STDP in Adaptive Neurons Gives Close-To-Optimal Information Transmission. Front Comput Neurosci. 4: 143.
37. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME. 2003. Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23: 11725-11731.
38. 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.
39. Izhikevich EM, Desai NS, Walcott EC, Hoppensteadt FC. 2003. Bursts as a unit of neural information: Selective communication via resonance. TINS 26: 161-167.
40. Jarsky T, Roxin A, Kath WL, Spruston N. 2005. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat Neurosci 8: 1667-1676.
41. Kampa BM, Letzkus JJ, Stuart GJ. 2006. Requirement of dendritic calcium spikes for induction of spike-timing-dependent synaptic plasticity. J Physiol 574: 283-290.
42. Karmarkar UR, Buonomano DV. 2002. A model of spike timing dependent plasticity: One or two coincidence detectors? J Neurosci 88: 507-513.
43. Klausberger T. 2009. GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus. Eur J Neurosci 30: 947-957.
44. Klausberger T, Magill PJ, Marton LF, Roberts JD, Cobden PM, Buzsaki G, Somogyi P. 2003. Brain-state and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421: 844-848.
45. Klausberger T, Marton LF, Baude A, Roberts JD, Magill PJ, Somogyi P. 2004. Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7: 41-47.
46. Klausberger T, Somogyi P. 2008. Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science 321: 53-57.
47. Larson J, Lynch G. 1986. Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 232: 985-988.
48. Larson J, Lynch G. 1989. Theta pattern stimulation and the induction of LTP: The sequence at which synapses are stimulated determines the degree to which they potentiate. Brain Res 489: 49-58.
49. Larson J, Wong D, Lynch G. 1986. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368: 347-350.
50. Letzkus JJ, Kampa BM, Stuart GJ. 2006. Learning rules for spike timing-dependent plasticity depend on dendritic synapse location. J Neurosci 26: 10420-10429.
51. Lisman J. 1989. A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. PNAS 86: 9574-9578.
52. Lisman J. 1997. Bursts as a unit of neural information: Making unreliable synapses reliable. TINS 20: 38-43.
53. Magee JC, Johnston D. 1997. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275: 209-213.
54. Markram H, Luebke J, Frotscher M, Sakmann B. 1997. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275: 213-215.
55. 2+ of NMDA responses in spinal cord neurons. Nature 309: 261-263.
56. Mihalas S. 2011. Calcium messenger heterogeneity: a possible signal for spike timing-dependent plasticity. Front Comput Neurosci. 4: 158.
57. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A. 1984. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307: 462-465.
58. 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.
59. Pavlides C, Greenstein YJ, Grudman M, Winson J. 1988. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439: 383-387.
60. Pfister JP, Gerstner W. 2006. Triplets of spikes in a model of spike timing-dependent plasticity. J Neurosci 26: 9673-9682.
61. Poirazi P, Pissadaki EK. 2010. The making of a detailed CA1 pyramidal neuron model. In Cutsuridis V, Graham BP, Cobb S, Vida I, editors. Hippocampal Microcircuits: A Computational Modeler's Resource Book (Springer Series in Computational Neuroscience 5). Springer Science + Business Media. pp 317-352.
62. Rose GM, Dunwiddie TV. 1986. Induction of hippocampal long-term potentiation using physiologically patterned stimulation. Neurosci Lett 69: 244-248.
63. Rubin JE, Gerkin RC, Bi GQ, Chow CC. 2005. Calcium time course as a signal for spike-timing-dependent plasticity. J Neurophysiol 93: 2600-2613.
64. 2+ signalling in dendritic spines. Curr Opin Neurobiol 33: 439-452.
65. Seol GH, Ziburkus J, Huang SY, Song L, Kim IT, Takamiya K, Huganir RL, Lee HK, Kirkwood A. 2007. Neuromodulators control the polarity of spike timing dependent synaptic plasticity. Neuron 55: 919-929.
66. Shah NT, Yeung LC, Cooper LN, Cai Y, Shouval HZ. 2006. A biophysical basis for the inter-spike interaction of spike-timing-dependent plasticity. Biol Cybern. 95: 113-121.
67. Shouval HZ, Bear MF, Cooper LN. 2002. A unified model of NMDA receptor-dependent bidirectional synaptic plasticity. Proc Natl Acad Sci USA 99: 10831-10836.
68. Sjostrom P, Turrigiano G, Nelson S. 2001. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32: 1149-1164.
69. Stent GS. 1973. A physiological mechanism for Hebb's postulate of learning. PNAS 70: 997-1001.
70. Tsukada M, Aihara T, Kobayashi Y, Shimazaki H. 2005. Spatial analysis of spike-timing-dependent LTP and LTD in the CA1 area of hippocampal slices using optical imaging. Hippocampus 15: 104-109.
71. Tzounopoulos T, Kim Y, Oertel D, Trussell LO. 2004. Cell-specific, spike timing-dependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7: 719-725.
72. Wang HX, Gerkin RC, Nauen DW, Bi GQ. 2005. Coactivation and timing-dependent integration of synaptic potentiation and depression. Nat Neurosci 8: 187-193.
73. A) kinetics provide substrate for mixed gamma-theta rhythm. PNAS 97: 8128-8133.
74. Whittington MA, Traub RD, Jeffreys JGR. 1995. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612-615.
75. Zhang L, Tao HW, Holt CE, Harris WA, Poo M. 1998. A critical window for cooperation and competition among developing retinotectal synapses. Nature 395: 37-44.