Modulation of Synaptic Plasticity by Glutamatergic Gliotransmission: A Modeling Study

Neural Plasticity

Volumn 2016, Issue , 2016, Pages

  De Pittà, Maurizio ^a,b   Brunel, Nicolas ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b INRIA RHÔNE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; GLUTAMIC ACID;

ARTICLE; ASTROCYTE; BIOPHYSICS; GLUTAMATERGIC GLIOTRANSMISSION; GLUTAMATERGIC SYNAPSE; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; SIGNAL TRANSDUCTION; SLOW INWARD CURRENT; SYNAPTIC POTENTIAL; ANIMAL; BIOLOGICAL MODEL; HIPPOCAMPUS; METABOLISM; PHYSIOLOGY; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; ASTROCYTES; GLUTAMIC ACID; HIPPOCAMPUS; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84971475341     PISSN: 20905904     EISSN: 16875443     Source Type: Journal    
DOI: 10.1155/2016/7607924     Document Type: Article

References (203)

1. A. Volterra and J. Meldolesi, "Astrocytes, from brain glue to communication elements: the revolution continues, " Nature Reviews Neuroscience, vol. 6, no. 8, pp. 626-640, 2005.
2. G. Perea and A. Araque, "Astrocytes potentiate transmitter release at single hippocampal synapses, " Science, vol. 317, no. 5841, pp. 1083-1086, 2007.
3. M. M. Halassa and P. G. Haydon, "Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior, " Annual Review of Physiology, vol. 72, pp. 335-355, 2009.
4. P. Bezzi and A. Volterra, "A neuron-glia signalling network in the active brain, " Current Opinion in Neurobiology, vol. 11, no. 3, pp. 387-394, 2001.
5. A. Araque, G. Carmignoto, P. G. Haydon, S. H. R. Oliet, R. Robitaille, and A. Volterra, "Gliotransmitters travel in time and space, " Neuron, vol. 81, no. 4, pp. 728-739, 2014.
6. M. Santello and A. Volterra, "Synaptic modulation by astrocytes via Ca2+-dependent glutamate release, " Neuroscience, vol. 158, no. 1, pp. 253-259, 2009.
7. T. A. Fiacco and K. D. McCarthy, "Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons, " The Journal of Neuroscience, vol. 24, no. 3, pp. 722-732, 2004.
8. P. Jourdain, L. H. Bergersen, K. Bhaukaurally et al., "Glutamate exocytosis from astrocytes controls synaptic strength, " Nature Neuroscience, vol. 10, no. 3, pp. 331-339, 2007.
9. C. Bonansco, A. Couve, G. Perea, C. ' A. Ferradas, M. Roncagliolo, and M. Fuenzalida, "Glutamate released spontaneously from astrocytes sets the threshold for synaptic plasticity, " European Journal of Neuroscience, vol. 33, no. 8, pp. 1483-1492, 2011.
10. A. Panatier, J. Vall'ee, M. Haber, K. K. Murai, J.-C. Lacaille, and R. Robitaille, "Astrocytes are endogenous regulators of basal transmission at central synapses, " Cell, vol. 146, no. 5, pp. 785-798, 2011.
11. G. Perea, A. Yang, E. S. Boyden, and M. Sur, "Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo, " Nature Communications, vol. 5, article 3262, 2014.
12. M. Navarrete and A. Araque, "Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes, " Neuron, vol. 68, no. 1, pp. 113-126, 2010.
13. Q. Liu, Q.-S. Xu, J. Kang, and M. Nedergaard, "Astrocyte activation of presynaptic metabotropic glutamate receptors modulates hippocampal inhibitory synaptic transmission, " Neuron Glia Biology, vol. 1, no. 4, pp. 307-316, 2004.
14. Q.-S. Liu, Q. Xu, G. Arcuino, J. Kang, and M. Nedergaard, "Astrocyte-mediated activation of neuronal kainate receptors, " Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 9, pp. 3172-3177, 2004.
15. B. Benedetti, V. Matyash, and H. Kettenmann, "Astrocytes control GABAergic inhibition of neurons in the mouse barrel cortex, " Journal of Physiology, vol. 589, no. 5, pp. 1159-1172, 2011.
16. H. Markram, Y. Wang, and M. Tsodyks, "Differential signaling via the same axon of neocortical pyramidal neurons, " Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 9, pp. 5323-5328, 1998.
17. L. F. Abbott and W. G. Regehr, "Synaptic computation, " Nature, vol. 431, no. 7010, pp. 796-803, 2004.
18. M. De Pittà, N. Brunel, and A. Volterra, "Astrocytes: orchestrating synaptic plasticitY" Neuroscience, 2015.
19. H. R. Parri, T. M. Gould, and V. Crunelli, "Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation, " Nature Neuroscience, vol. 4, no. 8, pp. 803-812, 2001.
20. M. C. Angulo, A. S. Kozlov, S. Charpak, and E. Audinat, "Glutamate released from glial cells synchronizes neuronal activity in the hippocampus, " Journal of Neuroscience, vol. 24, no. 31, pp. 6920-6927, 2004.
21. T. Fellin, O. Pascual, S. Gobbo, T. Pozzan, P. G. Haydon, and G. Carmignoto, "Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors, " Neuron, vol. 43, no. 5, pp. 729-743, 2004.
22. G. Perea and A. Araque, "Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes, " Journal of Neuroscience, vol. 25, no. 9, pp. 2192-2203, 2005.
23. M. D'Ascenzo, T. Fellin, M. Terunuma et al., "mGluR5 stimulates gliotransmission in the nucleus accumbens, " Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 6, pp. 1995-2000, 2007.
24. E. Shigetomi, D. N. Bowser, M. V. Sofroniew, and B. S. Khakh, "Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons, " The Journal of Neuroscience, vol. 28, no. 26, pp. 6659-6663, 2008.
25. R. Bardoni, A. Ghirri, M. Zonta et al., "Glutamate-mediated astrocyte-to-neuron signalling in the rat dorsal horn, " Journal of Physiology, vol. 588, no. 5, pp. 831-846, 2010.
26. R. Martn, R. Bajo-Grañeras, R. Moratalla, G. Perea, and A. Araque, "Circuit-specific signaling in astrocyte-neuron networks in basal ganglia pathways, " Science, vol. 349, no. 6249, pp. 730-734, 2015.
27. M. M. Halassa, T. Fellin, and P. G. Haydon, "The tripartite synapse: roles for gliotransmission in health and disease, " Trends in Molecular Medicine, vol. 13, no. 2, pp. 54-63, 2007.
28. M. M. Halassa, T. Fellin, H. Takano, J.-H. Dong, and P. G. Haydon, "Synaptic islands defined by the territory of a single astrocyte, " The Journal of Neuroscience, vol. 27, no. 24, pp. 6473-6477, 2007.
29. M. De Pittà, V. Volman, H. Berry, V. Parpura, A. Volterra, and E. Ben-Jacob, "Computational quest for understanding the role of astrocyte signaling in synaptic transmission and plasticity, " Frontiers in Computational Neuroscience, vol. 6, article 98, 2012.
30. T. Mizuno, I. Kanazawa, and M. Sakurai, "Differential induction of LTP and LTD is not determined solely by instantaneous calcium concentration: an essential involvement of a temporal factor, " European Journal of Neuroscience, vol. 14, no. 4, pp. 701-708, 2001.
31. T. Nevian and B. Sakmann, "Spine Ca2+ signaling in spiketiming-dependent plasticity, " The Journal of Neuroscience, vol. 26, no. 43, pp. 11001-11013, 2006.
32. N. Chen, H. Sugihara, J. Sharma et al., "Nucleus basalis-enabled stimulus-specific plasticity in the visual cortex is mediated by astrocytes, " Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 41, pp. E2832-E2841, 2012.
33. P. J. Sjöström, E. A. Rancz, A. Roth, and M. Häusser, "Dendritic excitability and synaptic plasticity, " Physiological Reviews, vol. 88, no. 2, pp. 769-840, 2008.
34. R. C. Froemke, D. Debanne, and G.-Q. Bi, "Temporal modulation of spike-timing-dependent plasticity, " Frontiers in Synaptic Neuroscience, vol. 2, article 19, 16 pages, 2010.
35. M. Graupner and N. Brunel, "Mechanisms of induction and maintenance of spike-timing dependent plasticity in biophysical synapse models, " Frontiers in Computational Neuroscience, vol. 4, no. 136, pp. 1-19, 2010.
36. J. J. Wade, L. J. McDaid, J. Harkin, V. Crunelli, and J. A. S. Kelso, "Bidirectional coupling between astrocytes and neurons mediates learning and dynamic coordination in the brain: a multiple modeling approach, " PLoS ONE, vol. 6, no. 12, Article ID e29445, 2011.
37. M. Naeem, L. J. McDaid, J. Harkin, J. J. Wade, and J. Marsland, "On the role of astroglial syncytia in self-repairing spiking neural networks, " IEEE Transactions on Neural Networks and Learning Systems, vol. 26, no. 10, pp. 2370-2380, 2015.
38. Y. Ni, E. B. Malarkey, and V. Parpura, "Vesicular release of glutamate mediates bidirectional signaling between astrocytes and neurons, " Journal of Neurochemistry, vol. 103, no. 4, pp. 1273-1284, 2007.
39. V. Parpura and R. Zorec, "Gliotransmission: exocytotic release fromastrocytes, " Brain Research Reviews, vol. 63, no. 1-2, pp. 83-92, 2010.
40. R. Zorec, A. Araque, G. Carmignoto, P. G. Haydon, A. Verkhratsky, and V. Parpura, "Astroglial excitability and gliotransmission: an appraisal of Ca2+ as a signalling route, " ASN Neuro, vol. 4, no. 2, Article ID e00080, pp. 103-119, 2012.
41. B. A. Barres, "The mystery and magic of glia: a perspective on their roles in health and disease, " Neuron, vol. 60, no. 3, pp. 430-440, 2008.
42. V. Parpura, V. Grubisic, and A. Verkhratsky, "Ca2+ sources for the exocytotic release of glutamate from astrocytes, " Biochimica et Biophysica Acta-Molecular Cell Research, vol. 1813, no. 5, pp. 984-991, 2011.
43. N. B. Hamilton and D. Attwell, "Do astrocytes really exocytose neurotransmitters" Nature Reviews Neuroscience, vol. 11, no. 4, pp. 227-238, 2010.
44. G. Perea, M. Navarrete, and A. Araque, "Tripartite synapses: astrocytes process and control synaptic information, " Trends in Neurosciences, vol. 32, no. 8, pp. 421-431, 2009.
45. G. Losi, L. Mariotti, andG. Carmignoto, "GABAergic interneuron to astrocyte signalling: a neglected formof cell communication in the brain, " Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 369, no. 1654, Article ID 20130609, 2014.
46. A. Nimmerjahn, "Astrocytes going live: advances and challenges, " The Journal of Physiology, vol. 587, no. 8, pp. 1639-1647, 2009.
47. A. Volterra, N. Liaudet, and I. Savtchouk, "Astrocyte Ca2+ signalling: an unexpected complexity, " Nature Reviews Neuroscience, vol. 15, no. 5, pp. 327-335, 2014.
48. N. Bazargani and D. Attwell, "Astrocyte calcium signaling: the thirdwave, " Nature Neuroscience, vol. 19, no. 2, pp. 182-189, 2016.
49. P. G. Haydon, "Glia: listening andtalking to the synapse, " Nature Reviews Neuroscience, vol. 2, no. 3, pp. 185-193, 2001.
50. M. A. Di Castro, J. Chuquet, N. Liaudet et al., "Local Ca2+ detection and modulation of synaptic release by astrocytes, " Nature Neuroscience, vol. 14, no. 10, pp. 1276-1284, 2011.
51. M. V. Tsodyks and H. Markram, "The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability, " Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 2, pp. 719-723, 1997.
52. R. S. Zucker and W. G. Regehr, "Short-term synaptic plasticity, " Annual Review of Physiology, vol. 64, pp. 355-405, 2002.
53. J. Del Castillo and B. Katz, "Quantal components of the endplate potential, " The Journal of Physiology, vol. 124, no. 3, pp. 560-573, 1954.
54. T. C. Südhof, "The synaptic vesicle cycle, " Annual Review of Neuroscience, vol. 27, pp. 509-547, 2004.
55. M. Tsodyks, "Activity-dependent transmission in neocortical synapses, " in Methods and Models in Neurophysics, C. C. Chow, B. Gutkin, D. Hansel, C. Meunier, and J. Dalibard, Eds., pp. 245-265, Elsevier, 2005.
56. J. D. Clements, "Transmitter timecourse in the synaptic cleft: its role in central synaptic function, " Trends in Neurosciences, vol. 19, no. 5, pp. 163-171, 1996.
57. J. S. Diamond, "Deriving the glutamate clearance time course from transporter currents in CA1 hippocampal astrocytes: transmitter uptake gets faster during development, " Journal of Neuroscience, vol. 25, no. 11, pp. 2906-2916, 2005.
58. A. Destexhe, Z. F. Mainen, and T. J. Sejnowski, "Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism, " Journal of Computational Neuroscience, vol. 1, no. 3, pp. 195-230, 1994.
59. G. W. De Young and J. Keizer, "A single-pool inositol 1, 4, 5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration, " Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 20, pp. 9895-9899, 1992.
60. L. Pasti, A. Volterra, T. Pozzan, and G. Carmignoto, "Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ, " The Journal of Neuroscience, vol. 17, no. 20, pp. 7817-7830, 1997.
61. J. Marchaland, C. Cal, S. M. Voglmaier et al., "Fast subplasma membrane Ca2+ transients control exo-endocytosis of synapticlike microvesicles in astrocytes, " The Journal of Neuroscience, vol. 28, no. 37, pp. 9122-9132, 2008.
62. D. A. Sahlender, I. Savtchouk, and A. Volterra, "What do we know about gliotransmitter release from astrocytes" Philosophical Transactions of the Royal Society B, vol. 369, Article ID 20130592, 2014.
63. P. Bezzi, V. Gundersen, J. L. Galbete et al., "Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate, " Nature Neuroscience, vol. 7, no. 6, pp. 613-620, 2004.
64. L. H. Bergersen andV. Gundersen, "Morphological evidence for vesicular glutamate release from astrocytes, " Neuroscience, vol. 158, no. 1, pp. 260-265, 2009.
65. M. Santello, P. Bezzi, and A. Volterra, "TNF controls glutamatergic gliotransmission in the hippocampal dentate gyrus, " Neuron, vol. 69, no. 5, pp. 988-1001, 2011.
66. M. Domercq, L. Brambilla, E. Pilati, J. Marchaland, A. Volterra, and P. Bezzi, "P2Y1 receptor-evoked glutamate exocytosis from astrocytes: control by tumor necrosis factor-and prostaglandins, "The Journal of Biological Chemistry, vol. 281, no. 41, pp. 30684-30696, 2006.
67. M. Kreft, M. Stenovec, M. Rupnik et al., "Properties of Ca2+-dependent exocytosis in cultured astrocytes, " Glia, vol. 46, no. 4, pp. 437-445, 2004.
68. E. B. Malarkey and V. Parpura, "Temporal characteristics of vesicular fusion in astrocytes: examination of synaptobrevin 2-laden vesicles at single vesicle resolution, " The Journal of Physiology, vol. 589, no. 17, pp. 4271-4300, 2011.
69. P. S. Pinheiro and C. Mulle, "Presynaptic glutamate receptors: physiological functions and mechanisms of action, " Nature Reviews Neuroscience, vol. 9, no. 6, pp. 423-436, 2008.
70. A. Banerjee, R. S. Larsen, B. D. Philpot, and O. Paulsen, "Roles of presynaptic NMDA receptors in neurotransmission and plasticity, " Trends inNeurosciences, vol. 39, no. 1, pp. 26-39, 2016.
71. A. Araque, V. Parpura, R. P. Sanzgiri, and P. G. Haydon, "Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons, " European Journal of Neuroscience, vol. 10, no. 6, pp. 2129-2142, 1998.
72. M. Navarrete, G. Perea, D. F. de Sevilla et al., "Astrocytes mediate in vivo cholinergic-induced synaptic plasticity, " PLoS Biology, vol. 10, no. 2, Article ID e1001259, 2012.
73. M. De Pittà, V. Volman, H. Berry, and E. Ben-Jacob, "A tale of two stories: astrocyte regulation of synaptic depression and facilitation, " PLoS Computational Biology, vol. 7, no. 12, Article ID e1002293, 2011.
74. J. S. Dittman, A. C. Kreitzer, and W. G. Regehr, "Interplay between facilitation, depression, and residual calcium at three presynaptic terminals, " Journal of Neuroscience, vol. 20, no. 4, pp. 1374-1385, 2000.
75. E. S. Fortune and G. J. Rose, "Short-termsynaptic plasticity as a temporal filter, " Trends in Neurosciences, vol. 24, no. 7, pp. 381-385, 2001.
76. C. Agulhon, J. Petravicz, A. B. McMullen et al., "What is the role of astrocyte calcium in neurophysiologY" Neuron, vol. 59, no. 6, pp. 932-946, 2008.
77. T. Papouin and S. H. R. Oliet, "Organization, control and function of extrasynaptic NMDA receptors, " Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 369, no. 1654, Article ID 20130601, 2014.
78. T. M. Pirttimaki, S. D. Hall, and H. R. Parri, "Sustained neuronal activity generated by glial plasticity, " The Journal of Neuroscience, vol. 31, no. 21, pp. 7637-7647, 2011.
79. M. Navarrete, G. Perea, L. Maglio, J. Pastor, R. Garciá de Sola, and A. Araque, "Astrocyte calcium signal and gliotransmission in human brain tissue, " Cerebral Cortex, vol. 23, no. 5, pp. 1240-1246, 2013.
80. M. Navarrete and A. Araque, "Endocannabinoids mediate neuron-astrocyte communication, " Neuron, vol. 57, no. 6, pp. 883-893, 2008.
81. S.-J. Oh, K.-S. Han, H. Park et al., "Protease activated receptor 1-induced glutamate release in cultured astrocytes is mediated by Bestrophin-1 channel but not by vesicular exocytosis, " Molecular Brain, vol. 5, no. 1, article 38, 2012.
82. D. H. Woo, K.-S. Han, J. W. Shim et al., "TREK-1 and Best1 channels mediate fast and slow glutamate release in astrocytes upon GPCR activation, " Cell, vol. 151, no. 1, pp. 25-40, 2012.
83. T. Papouin, L. Ladépêche, J. Ruel et al., "Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists, " Cell, vol. 150, no. 3, pp. 633-646, 2012.
84. C. J. Lee, G. Mannaioni, H. Yuan, D. H. Woo, M. B. Gingrich, and S. F. Traynelis, "Astrocytic control of synaptic NMDA receptors, " The Journal of Physiology, vol. 581, no. 3, pp. 1057-1081, 2007.
85. H. Nie, H. Zhang, and H.-R. Weng, "Bidirectional neuron-glia interactions triggered by deficiency of glutamate uptake at spinal sensory synapses, " Journal of Neurophysiology, vol. 104, no. 2, pp. 713-725, 2010.
86. D. Reyes-Haro, J. Müller, M. Boresch et al., "Neuron-astrocyte interactions in the medial nucleus of the trapezoid body, " The Journal of General Physiology, vol. 135, no. 6, pp. 583-594, 2010.
87. N. Kang, J. Xu, Q. Xu, M. Nedergaard, and J. Kang, "Astrocytic glutamate release-induced transient depolarization and epileptiform discharges in hippocampal CA1 pyramidal neurons, " Journal of Neurophysiology, vol. 94, no. 6, pp. 4121-4130, 2005.
88. T. Fellin, M. Gomez-Gonzalo, S. Gobbo, G. Carmignoto, and P. G. Haydon, "Astrocytic glutamate is not necessary for the generation of epileptiform neuronal activity in hippocampal slices, " The Journal of Neuroscience, vol. 26, no. 36, pp. 9312-9322, 2006.
89. G.-F. Tian, H. Azmi, T. Takano et al., "An astrocytic basis of epilepsy, " Nature Medicine, vol. 11, no. 9, pp. 973-981, 2005.
90. S. Ding, T. Fellin, Y. Zhu et al., "Enhanced astrocytic Ca2+ signals contribute to neuronal excitotoxicity after status epilepticus, " The Journal of Neuroscience, vol. 27, no. 40, pp. 10674-10684, 2007.
91. N. Fourcaud and N. Brunel, "Dynamics of the firing probability of noisy integrate-and fire neurons, " Neural Computation, vol. 14, no. 9, pp. 2057-2110, 2002.
92. A. N. Burkitt, "A review of the integrate-and-fire neuron model: I. Homogeneous synaptic input, " Biological Cybernetics, vol. 95, no. 1, pp. 1-19, 2006.
93. A. Rauch, G. La Camera, H.-R. Lüscher, W. Senn, and S. Fusi, "Neocortical pyramidal cells respond as integrate-and-fire neurons to in vivo-like input currents, " Journal of Neurophysiology, vol. 90, no. 3, pp. 1598-1612, 2003.
94. T. Hromádka, M. R. DeWeese, and A. M. Zador, "Sparse representation of sounds in the unanesthetized auditory cortex, " PLoS Biology, vol. 6, no. 1, article e16, 2008.
95. N. Caporale and Y. Dan, "Spike timing-dependent plasticity: a hebbian learning rule, " Annual Review of Neuroscience, vol. 31, pp. 25-46, 2008.
96. J. C. Magee and D. Johnston, "A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons, " Science, vol. 275, no. 5297, pp. 209-213, 1997.
97. I. Ismailov, D. Kalikulov, T. Inoue, and M. J. Friedlander, "The kinetic profile of intracellular calcium predicts longterm potentiation and long-term depression, " The Journal of Neuroscience, vol. 24, no. 44, pp. 9847-9861, 2004.
98. T. Nevian and B. Sakmann, "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, " The Journal of Neuroscience, vol. 24, no. 7, pp. 1689-1699, 2004.
99. V. A. Bender, K. J. Bender, D. J. Brasier, andD. E. Feldman, "Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex, " The Journal of Neuroscience, vol. 26, no. 16, pp. 4166-4177, 2006.
100. H. Z. Shouval, M. F. Bear, and L. N. Cooper, "A unified model ofNMDA receptor-dependent bidirectional synaptic plasticity, " Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 16, pp. 10831-10836, 2002.
101. Y. Cai, J. P. Gavornik, L. N. Cooper, L. C. Yeung, and H. Z. Shouval, "Effect of stochastic synaptic and dendritic dynamics on synaptic plasticity in visual cortex and hippocampus, " Journal of Neurophysiology, vol. 97, no. 1, pp. 375-386, 2007.
102. M. Graupner and N. Brunel, "Calcium-based plasticity model explains sensitivity of synaptic changes to spike pattern, rate, and dendritic location, " Proceedings of the National Academy of Sciences of theUnited States of America, vol. 109, no. 10, pp. 3991-3996, 2012.
103. R. C. Malenka and M. F. Bear, "LTPandLTD: anembarrassment of riches, " Neuron, vol. 44, no. 1, pp. 5-21, 2004.
104. J. C. Magee and D. Johnston, "Plasticity of dendritic function, " Current Opinion in Neurobiology, vol. 15, no. 3, pp. 334-342, 2005.
105. P. J. Sjöström and S. B. Nelson, "Spike timing, calcium signals and synaptic plasticity, " Current Opinion in Neurobiology, vol. 12, no. 3, pp. 305-314, 2002.
106. L. F. Abbott and S. B. Nelson, "Synaptic plasticity: taming the beast, " Nature, vol. 3, pp. 1178-1183, 2000.
107. L. Nowak, P. Bregestovski, P. Ascher, A. Herbet, and A. Prochiantz, "Magnesiumgates glutamate-activated channels inmouse central neurones, " Nature, vol. 307, no. 5950, pp. 462-465, 1984.
108. C. E. Jahr and C. F. Stevens, "Voltage dependence of NMDAactivated macroscopic conductances predicted by singlechannel kinetics, "The Journal of Neuroscience, vol. 10, no. 9, pp. 3178-3182, 1990.
109. R. C. Froemke and Y. Dan, "Spike-timing-dependent synaptic modification induced by natural spike trains, " Nature, vol. 416, no. 6879, pp. 433-438, 2002.
110. R. C. Froemke, I. A. Tsay, M. Raad, J. D. Long, and Y. Dan, "Contribution of individual spikes in burst-induced long-term synaptic modification, " Journal of Neurophysiology, vol. 95, no. 3, pp. 1620-1629, 2006.
111. S. Cull-Candy, S. Brickley, and M. Farrant, "NMDA receptor subunits: diversity, development and disease, " Current Opinion in Neurobiology, vol. 11, no. 3, pp. 327-335, 2001.
112. D.-D. Liu, Q. Yang, and S.-T. Li, "Activation of extrasynaptic NMDA receptors induces LTD in rat hippocampal CA1 neurons, " Brain Research Bulletin, vol. 93, pp. 10-16, 2013.
113. R. C. Evans and K. T. Blackwell, "Calcium: amplitude, duration, or location" The Biological Bulletin, vol. 228, no. 1, pp. 75-83, 2015.
114. B. L. Bloodgood and B. L. Sabatini, "Ca2+ signaling in dendritic spines, " Current Opinion in Neurobiology, vol. 17, no. 3, pp. 345-351, 2007.
115. D. A. Rusakov, A. Scimemi, M. C. Walker, and D. M. Kullmann, "Comment on 'Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity', " Science, vol. 305, article 1912, 2004.
116. R. S. Petralia, Y. X. Wang, F. Hua et al., "Organization of NMDA receptors at extrasynaptic locations, " Neuroscience, vol. 167, no. 1, pp. 68-87, 2010.
117. A. Araque, V. Parpura, R. P. Sanzgiri, and P. G. Haydon, "Tripartite synapses: glia, the unacknowledged partner, " Trends in Neurosciences, vol. 22, no. 5, pp. 208-215, 1999.
118. A. Perez-Alvarez, M. Navarrete, A. Covelo, E. D. Martin, and A. Araque, "Structural and functional plasticity of astrocyte processes and dendritic spine interactions, " The Journal of Neuroscience, vol. 34, no. 38, pp. 12738-12744, 2014.
119. K. A. Buchanan and J. R. Mellor, "The activity requirements for spike timing-dependent plasticity in the hippocampus, " Frontiers in Synaptic Neuroscience, vol. 2, no. 11, pp. 1-5, 2010.
120. R. M. Meredith, A. M. Floyer-Lea, and O. Paulsen, "Maturation of long-term potentiation induction rules in rodent hippocampus: role of GABAergic inhibition, "The Journal of Neuroscience, vol. 23, no. 35, pp. 11142-11146, 2003.
121. K. A. Buchanan and J. R. Mellor, "The development of synaptic plasticity induction rules and the requirement for postsynaptic spikes in rat hippocampal CA1 pyramidal neurones, " The Journal of Physiology, vol. 585, no. 2, pp. 429-445, 2007.
122. E. Campanac and D. Debanne, "Spike timing-dependent plasticity: a learning rule for dendritic integration in rat CA1 pyramidal neurons, " The Journal of Physiology, vol. 586, no. 3, pp. 779-793, 2008.
123. G.-Q. Bi and M.-M. Poo, "Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type, " The Journal of Neuroscience, vol. 18, no. 24, pp. 10464-10472, 1998.
124. G. M. Wittenberg and S. S.-H. Wang, "Malleability of spiketiming-dependent plasticity at the CA3-CA1 synapse, " The Journal of Neuroscience, vol. 26, no. 24, pp. 6610-6617, 2006.
125. D. E. Shulz and V. Jacob, "Spike-timing-dependent plasticity in the intact brain: counteracting spurious spike coincidences, " Frontiers in Synaptic Neuroscience, vol. 1, article 137, 2010.
126. F. G. Pike, R. M. Meredith, A. W. A. Olding, and O. Paulsen, "Postsynaptic bursting is essential for 'Hebbian' induction of associative long-term potentiation at excitatory synapses in rat hippocampus, " The Journal of Physiology, vol. 518, no. 2, pp. 571-576, 1999.
127. W. Sun, E. McConnell, J.-F. Pare et al., "Glutamate-dependent neuroglial calcium signaling differs between young and adult brain, " Science, vol. 339, no. 6116, pp. 197-200, 2013.
128. N. L. Golding, N. P. Staff, and N. Spruston, "Dendritic spikes as a mechanism for cooperative long-term potentiation, " Nature, vol. 418, no. 6895, pp. 326-331, 2002.
129. G.-Q. Bi and M.-M. Poo, "Synaptic modification by correlated activity: hebb's postulate revisited, " Annual Review of Neuroscience, vol. 24, pp. 139-166, 2001.
130. M. Lavialle, G. Aumann, E. Anlauf, F. PRöls, M. Arpin, and A. Derouiche, "Structural plasticity of perisynaptic astrocyte processes involves ezrin and metabotropic glutamate receptors, " Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 31, pp. 12915-12919, 2011.
131. D. O. Hebb, The Organization of Behavior; A Neuropsychological Theory, John Wiley & Sons, New York, NY, USA, 1949.
132. W. Gerstner and W. M. Kistler, "Mathematical formulations of Hebbian learning, " Biological Cybernetics, vol. 87, no. 5-6, pp. 404-415, 2002.
133. A. B. Porto-Pazos, N. Veiguela, P. Mesejo et al., "Artificial astrocytes improve neural network performance, " PLoS ONE, vol. 6, no. 4, Article ID e19109, 2011.
134. J. S. Bains and S. H. R. Oliet, "Glia: they make your memories stick!, " Trends in Neurosciences, vol. 30, no. 8, pp. 417-424, 2007.
135. R. Min, M. Santello, and T. Nevian, "The computational power of astrocytemediated synaptic plasticity, " Frontiers in Computational Neuroscience, vol. 6, article 93, 2012.
136. G. Wallach, J. Lallouette, N. Herzog et al., "Glutamate mediated astrocytic filtering of neuronal activity, " PLoS Computational Biology, vol. 10, no. 12, Article ID e1003964, 2014.
137. B.-X. Zhang, H. Zhao, and S. Muallem, "Ca2+-dependent kinase and phosphatase control inositol 1, 4, 5-trisphosphate-mediated Ca2+ release. Modification by agonist stimulation, " The Journal of Biological Chemistry, vol. 268, no. 15, pp. 10997-11001, 1993.
138. C. E. Sims and N. L. Allbrittont, "Metabolism of inositol 1, 4, 5-trisphosphate and inositol 1, 3, 4, 5-tetrakisphosphate by the oocytes of Xenopus laevis, " Journal of Biological Chemistry, vol. 273, no. 7, pp. 4052-4058, 1998.
139. M. J. Rebecchi and S. N. Pentyala, "Structure, function, and control of phosphoinositide-specific phospholipase C, " Physiological Reviews, vol. 80, no. 4, pp. 1291-1335, 2000.
140. M. J. Berridge, M. D. Bootman, and H. L. Roderick, "Calcium signalling: dynamics, homeostasis and remodelling, " Nature Reviews Molecular Cell Biology, vol. 4, no. 7, pp. 517-529, 2003.
141. M. De Pittà, M. Goldberg, V. Volman, H. Berry, and E. Ben-Jacob, "Glutamate regulation of calcium and IP3 oscillating and pulsating dynamics in astrocytes, " Journal of Biological Physics, vol. 35, no. 4, pp. 383-411, 2009.
142. Y.-X. Li and J. Rinzel, "Equations for InsP3 receptor-mediated Ca2+oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism, " Journal ofTheoretical Biology, vol. 166, no. 4, pp. 461-473, 1994.
143. M. De Pittà, V. Volman, H. Levine, and E. Ben-Jacob, "Multimodal encoding in a simplified model of intracellular calcium signaling, " Cognitive Processing, vol. 10, no. 1, pp. 55-70, 2009.
144. Y. Pankratov, U. Lalo, A. Verkhratsky, andR. A. North, "Quantal release of ATP in mouse cortex, " Journal of General Physiology, vol. 129, no. 3, pp. 257-265, 2007.
145. J. Kang, L. Jiang, S. A. Goldman, and M. Nedergaard, "Astrocyte-mediated potentiation of inhibitory synaptic transmission, " Nature Neuroscience, vol. 1, no. 8, pp. 683-692, 1998.
146. A. Serrano, N. Haddjeri, J.-C. Lacaille, and R. Robitaille, "GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression, " The Journal of Neuroscience, vol. 26, no. 20, pp. 5370-5382, 2006.
147. N. Spruston, P. Jonas, and B. Sakmann, "Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons, " The Journal of Physiology, vol. 482, no. 2, pp. 325-352, 1995.
148. J. C. Magee and E. P. Cook, "Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons, " Nature Neuroscience, vol. 3, no. 9, pp. 895-903, 2000.
149. B. K. Andrásfalvy and J. C. Magee, "Distance-dependent increase in AMPA receptor number in the dendrites of adult hippocampal CA1 pyramidal neurons, " The Journal of Neuroscience, vol. 21, no. 23, pp. 9151-9159, 2001.
150. M. Stimberg, D. F. M. Goodman, V. Benichoux, and R. Brette, "Equation-oriented specification of neural models for simulations, " Frontiers in Neuroinformatics, vol. 8, article 6, 2014.
151. Python Software Foundation, Python Language Reference, Version 2. 7, Python Software Foundation, 2015.
152. T. Schikorski and C. F. Stevens, "Quantitative ultrastructural analysis of hippocampal excitatory synapses, " The Journal of Neuroscience, vol. 17, no. 15, pp. 5858-5867, 1997.
153. C. F. Stevens and Y. Wang, "Facilitation and depression at single central synapses, " Neuron, vol. 14, no. 4, pp. 795-802, 1995.
154. H. Markram, D. Pikus, A. Gupta, and M. Tsodyks, "Potential for multiple mechanisms, phenomena and algorithms for synaptic plasticity at single synapses, " Neuropharmacology, vol. 37, no. 4-5, pp. 489-500, 1998.
155. V. N. Murthy, T. J. Sejnowski, and C. F. Stevens, "Heterogeneous release properties of visualized individual hippocampal synapses, " Neuron, vol. 18, no. 4, pp. 599-612, 1997.
156. W. G. Regehr, K. R. Delaney, and D. W. Tank, "The role of presynaptic calcium in short-term enhancement at the hippocampalmossy fiber synapse, " Journal of Neuroscience, vol. 14, no. 2, pp. 523-537, 1994.
157. N. J. Emptage, C. A. Reid, and A. Fine, "Calcium stores in hippocampal synaptic boutonsmediate short-termplasticity, storeoperated Ca2+ entry, and spontaneous transmitter release, " Neuron, vol. 29, no. 1, pp. 197-208, 2001.
158. J. L. Pyle, E. T. Kavalali, E. S. Piedras-Renteriá, and R. W. Tsien, "Rapid reuse of readily releasable pool vesicles at hippocampal synapses, " Neuron, vol. 28, no. 1, pp. 221-231, 2000.
159. D. L. Brody and D. T. Yue, "Release-independent short-term synaptic depression in cultured hippocampal neurons, " The Journal of Neuroscience, vol. 20, no. 7, pp. 2480-2494, 2000.
160. K. M. Harris and P. Sultan, "Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses, " Neuropharmacology, vol. 34, no. 11, pp. 1387-1395, 1995.
161. L. H. Bergersen, C. Morland, L. Ormel et al., "Immunogold detection of L-glutamate and D-serine in small synaptic-like microvesicles in adult hippocampal astrocytes, " Cerebral Cortex, vol. 22, no. 7, pp. 1690-1697, 2012.
162. N. C. Danbolt, "Glutamate uptake, " Progress in Neurobiology, vol. 65, no. 1, pp. 1-105, 2001.
163. S. Raghavachari and J. E. Lisman, "Properties of quantal transmission at CA1 synapses, " Journal of Neurophysiology, vol. 92, no. 4, pp. 2456-2467, 2004.
164. T. A. Nielsen, D. A. DiGregorio, and R. A. Silver, "Modulation of glutamate mobility reveals the mechanism underlying slowrising AMPAR EPSCs and the diffusion coefficient in the synaptic cleft, " Neuron, vol. 42, no. 5, pp. 757-771, 2004.
165. B. Barbour, "An evaluation of synapse independence, " The Journal of Neuroscience, vol. 21, no. 20, pp. 7969-7984, 2001.
166. R. Ventura and K. M. Harris, "Three-dimensional relationships between hippocampal synapses and astrocytes, " The Journal of Neuroscience, vol. 19, no. 16, pp. 6897-6906, 1999.
167. T. G. Oertner, B. L. Sabatini, E. A. Nimchinsky, and K. Svoboda, "Facilitation at single synapses probed with optical quantal analysis, " Nature Neuroscience, vol. 5, no. 7, pp. 657-664, 2002.
168. B. Barbour and M. Häusser, "Intersynaptic diffusion of neurotransmitter, " Trends in Neurosciences, vol. 20, no. 9, pp. 377-384, 1997.
169. J. D. Clements, R. A. J. Lester, G. Tong, C. E. Jahr, and G. L. Westbrook, "The time course of glutamate in the synaptic cleft, " Science, vol. 258, no. 5087, pp. 1498-1501, 1992.
170. M. A. Herman and C. E. Jahr, "Extracellular glutamate concentration in hippocampal slice, " The Journal of Neuroscience, vol. 27, no. 36, pp. 9736-9741, 2007.
171. Y. Okubo, H. Sekiya, S. Namiki et al., "Imaging extrasynaptic glutamate dynamics in the brain, " Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 14, pp. 6526-6531, 2010.
172. H. Hirase, L. Qian, P. Barthó, and G. Buzsáki, "Calcium dynamics of cortical astrocytic networks in vivo, " PLoS Biology, vol. 2, no. 4, article e96, 2004.
173. A. Nimmerjahn, F. Kirchhoff, J. N. D. Kerr, and F. Helmchen, "Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo, " NatureMethods, vol. 1, no. 1, pp. 31-37, 2004.
174. X. Wang, N. Lou, Q. Xu et al., "Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo, " Nature Neuroscience, vol. 9, no. 6, pp. 816-823, 2006.
175. T. Pivneva, B. Haas, D. Reyes-Haro et al., "Store-operated Ca2+ entry in astrocytes: different spatial arrangement of endoplasmic reticulum explains functional diversity in vitro and in situ, " Cell Calcium, vol. 43, no. 6, pp. 591-601, 2008.
176. J. Lytton, M. Westlin, S. E. Burk, G. E. Shull, and D. H. MacLennan, "Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps, " Journal of Biological Chemistry, vol. 267, no. 20, pp. 14483-14489, 1992.
177. I. Vandecaetsbeek, M. Trekels, M. De Maeyer et al., "Structural basis for the high Ca2+ affinity of the ubiquitous SERCA2b Ca2+ pump, " Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 44, pp. 18533-18538, 2009.
178. V. Parpura and P. G. Haydon, "Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons, " Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 15, pp. 8629-8634, 2000.
179. M. Kang and H. G. Othmer, "Spatiotemporal characteristics of calciumdynamics in astrocytes, " Chaos, vol. 19, no. 3, Article ID 037116, 2009.
180. E. Aronica, J. A. Gorter, H. Ijlst-Keizers et al., "Expression and functional role of mGluR3 and mGluR5 in human astrocytes and glioma cells: opposite regulation of glutamate transporter proteins, " European Journal of Neuroscience, vol. 17, no. 10, pp. 2106-2118, 2003.
181. I. Brabet, S. Mary, J. Bockaert, and J.-P. Pin, "Phenylglycine derivatives discriminate between mGluR1-and mGluR5-mediated responses, " Neuropharmacology, vol. 34, no. 8, pp. 895-903, 1995.
182. L. P. Daggett, A. I. Sacaan, M. Akong et al., "Molecular andfunctional characterization of recombinant human metabotropic glutamate receptor subtype 5, " Neuropharmacology, vol. 34, no. 8, pp. 871-886, 1995.
183. D. Crippa, U. Schenk, M. Francolini et al., "Synaptobrevin2-expressing vesicles in rat astrocytes: insights into molecular characterization, dynamics and exocytosis, " The Journal of Physiology, vol. 570, no. 3, pp. 567-582, 2006.
184. V. Montana, E. B. Malarkey, C. Verderio, M. Matteoli, and V. Parpura, "Vesicular transmitter release from astrocytes, " Glia, vol. 54, no. 7, pp. 700-715, 2006.
185. X. Chen, L. Wang, Y. Zhou, L.-H. Zheng, and Z. Zhou, ""Kissand-run" glutamate secretion in cultured and freshly isolated rat hippocampal astrocytes, " Journal of Neuroscience, vol. 25, no. 40, pp. 9236-9243, 2005.
186. F. Valtorta, J. Meldolesi, and R. Fesce, "Synaptic vesicles: is kissing a matter of competence?" Trends in Cell Biology, vol. 11, no. 8, pp. 324-328, 2001.
187. D. N. Bowser and B. S. Khakh, "Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy, " Proceedings of the National Academy of Sciences of theUnited States ofAmerica, vol. 104, no. 10, pp. 4212-4217, 2007.
188. D. A. Rusakov and D. M. Kullmann, "Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation, " Journal of Neuroscience, vol. 18, no. 9, pp. 3158-3170, 1998.
189. B. Innocenti, V. Parpura, and P. G. Haydon, "Imaging extracellular waves of glutamate during calcium signaling in cultured astrocytes, " The Journal of Neuroscience, vol. 20, no. 5, pp. 1800-1808, 2000.
190. A. Araque, R. P. Sanzgiri, V. Parpura, and P. G. Haydon, "Calcium elevation in astrocytes causes an NMDA receptordependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons, " Journal of Neuroscience, vol. 18, no. 17, pp. 6822-6829, 1998.
191. Y. V. Pankratov andO. A. Krishtal, "Distinct quantal features of AMPAand NMDA synaptic currents in hippocampal neurons: implication of glutamate spillover and receptor saturation, " Biophysical Journal, vol. 85, no. 5, pp. 3375-3387, 2003.
192. B. N. Routh, D. Johnston, K. Harris, and R. A. Chitwood, "Anatomical and electrophysiological comparison of CA1 pyramidal neurons of the rat and mouse, " Journal of Neurophysiology, vol. 102, no. 4, pp. 2288-2302, 2009.
193. J. C. Magee, "Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons, " The Journal of Neuroscience, vol. 18, no. 19, pp. 7613-7624, 1998.
194. N. A. Otmakhova, N. Otmakhov, and J. E. Lisman, "Pathwayspecific properties of AMPA and NMDA-mediated transmission in CA1 hippocampal pyramidal cells, " Journal of Neuroscience, vol. 22, no. 4, pp. 1199-1207, 2002.
195. S. Gasparini, M. Migliore, and J. C. Magee, "On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons, " Journal of Neuroscience, vol. 24, no. 49, pp. 11046-11056, 2004.
196. C. M. McDermott, M. N. Hardy, N. G. Bazan, and J. C. Magee, "Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus, " The Journal of Physiology, vol. 570, no. 3, pp. 553-565, 2006.
197. C. M. McDermott, G. J. LaHoste, C. Chen, A. Musto, N. G. Bazan, and J. C. Magee, "Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons, " The Journal of Neuroscience, vol. 23, no. 29, pp. 9687-9695, 2003.
198. S. Gasparini and J. C. Magee, "State-dependent dendritic computation in hippocampal CA1 pyramidal neurons, " The Journal of Neuroscience, vol. 26, no. 7, pp. 2088-2100, 2006.
199. A. E. Metz, T. Jarsky, M. Martina, and N. Spruston, "Rtype calcium channels contribute to afterdepolarization and bursting in hippocampal CA1 pyramidal neurons, " The Journal of Neuroscience, vol. 25, no. 24, pp. 5763-5773, 2005.
200. M. A. Smith, G. C. R. Ellis-Davies, and J. C. Magee, "Mechanism of the distance-dependent scaling of Schaffer collateral synapses in rat CA1 pyramidal neurons, "The Journal of Physiology, vol. 548, no. 1, pp. 245-258, 2003.
201. A. Loebel, G. Silberberg, D. Helbig, H. Markram, M. Tsodyks, and M. J. E. Richardson, "Multiquantal release underlies the distribution of synaptic efficacies in the neocortex, " Frontiers in Computational Neuroscience, vol. 3, article 27, 2009.
202. N. J. Abbott, "Astrocyte-endothelial interactions and bloodbrain barrier permeability, " Journal of Anatomy, vol. 200, no. 6, pp. 629-638, 2002.
203. S. F. Traynelis, L. P. Wollmuth, C. J. McBain et al., "Glutamate receptor ion channels: Structure, regulation, and function, " Pharmacological Reviews, vol. 62, no. 3, pp. 405-496, 2010.