A tale of two stories: Astrocyte regulation of synaptic depression and facilitation

PLoS Computational Biology

Volumn 7, Issue 12, 2011, Pages

  de Pittà, Maurizio ^a   Volman, Vladislav ^b,c   Berry, Hugues ^d   Ben Jacob, Eshel ^a,b  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NEURONS;

COMPUTATIONAL MODELLING; GLIAL CELLS; IN-VIVO; INFORMATION TRANSFERS; MEAN FIELD ANALYSIS; NEURONAL FIRINGS; PRESYNAPTIC; PRESYNAPTIC PLASTICITY; SHORT TERM PLASTICITY; SYNAPTIC DEPRESSION;

MODULATION;

CALCIUM ION; GLUTAMIC ACID; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CALCIUM;

AMINO ACID ANALYSIS; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CELL FUNCTION; CONTROLLED STUDY; FACILITATION; HIPPOCAMPUS; INTRACELLULAR SIGNALING; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROTRANSMITTER RELEASE; OSCILLATION; PHASE TRANSITION; SPIKE WAVE; SYNAPTIC INHIBITION; SYNAPTIC POTENTIAL; BIOLOGICAL MODEL; COMPUTER SIMULATION; METABOLISM; PHYSIOLOGY; SYNAPSE; SYNAPTIC TRANSMISSION;

ASTROCYTES; CALCIUM; COMPUTER SIMULATION; HIPPOCAMPUS; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84855283333     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002293     Document Type: Article

References (95)

1. Barak O, Tsodyks M, (2007) Persistent activity in neural networks with dynamic synapses. PLoS Comput Biol 32: e35.
2. Abbott LF, Regehr WG, (2004) Synaptic computation. Nature 431: 796-803.
3. Zucker RS, Regehr WG, (2002) Short-term synaptic plasticity. Annual Rev Physiol 64: 355-405.
4. Mongillo M, Barak O, Tsodyks M, (2008) Synaptic theory of working memory. Science 319: 1543-1546.
5. Citri A, Malenka RC, (2008) Synaptic plasticity: multiple forms, functions and mechanisms. Neuropsychopharmacology Rev 33: 18-41.
6. Tsodyks MV, Markram H, (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci USA 94: 719-723.
7. Dobrunz LE, Stevens CF, (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008.
8. Südhof TC, (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547.
9. Schneggenburger R, Sakaba T, Neher E, (2002) Vesicle pools and short-term synaptic depression: lessons form a large synapse. Trends Neurosci 25: 206-212.
10. Nadkarni S, Bartol TM, Sejnowski TJ, Levine H, (2010) Modelling vesicular release at hippocampal synapses. PLoS Comput Biol 6: e1000983.
11. Sun J, Pang ZP, Qin D, Fahim AT, Adachi R, Südhof TC, (2007) A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 450: 676-682.
12. Abbott LF, Varela JA, Sen K, Nelson SB, (1997) Synaptic depression and cortical gain control. Science 25: 220-224.
13. Dittman JS, Kreitzer AC, Regehr WG, (2000) Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20: 1374-1385.
14. Debanne D, Guerineau NC, Giihwiler BH, Thompson SM, (1996) Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J Physiol 491: 163-176.
15. Haydon PG, Carmignoto G, (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86: 1009-1031.
16. Herculano-Houzel S, (2009) The human brain in numbers: a linearly scaled-up primate brain. Frontiers Human Neurosci 3: 1-11.
17. Savchenko VL, McKanna JA, Nikonenko IR, Skibo GG, (2000) Microglia and astrocytes in the adult rat brain: comparative immunocytochemical analysis demonstrates the efficacy of lipocortin 1 immunoreactivity. Neuroscience 96: 196-203.
18. Ventura R, Harris KM, (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19: 6897-6906.
19. Haydon PG, (2001) Glia: listening and talking to the synapse. Nature Rev Neurosci 2: 185-193.
20. Araque A, Parpura V, Sanzgiri RP, Haydon PG, (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 23: 208-215.
21. Volterra A, Meldolesi J, (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nature Rev Neurosci 6: 626-640.
22. Parpura V, Zorec R, (2010) Gliotransmission: exocytotic release from astrocytes. Brain Res Rev 63: 83-92.
23. Perea G, Navarrete M, Araque A, (2009) Tripartite synapse: astrocytes process and control synaptic information. Trends Neurosci 32: 421-431.
24. Agulhon C, Petravicz J, McMullen AB, Sweger EJ, Minton SK, et al. (2008) What is the role of astrocyte calcium in neurophysiology? Neuron 59: 932-946.
25. Barnes BA, (2008) The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60: 430-440.
26. Pinheiro PS, Mulle C, (2008) Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nature Rev 9: 423-436.
27. Santello M, Volterra A, (2009) Synaptic modulation by astrocytes via Ca2+-dependent glutamate release. Neuroscience 158: 253-259.
28. Andersson M, Hanse E, (2010) Astrocytes impose postburst depression of release probability at hippocampal glutamate synapses. J Neurosci 30: 5776-5780.
29. Andersson M, Blomstrand F, Hanse E, (2007) Astrocytes play a critical role in transient heterosynaptic depression in the rat hippocampal CA1 region. J Physiol 585: 843-852.
30. Perea G, Araque A, (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317: 1083-1086.
31. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, Domercq M, et al. (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nature Neurosci 10: 331-339.
32. Fiacco TA, McCarthy KD, (2004) Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons. J Neurosci 24: 722-732.
33. Araque A, Parpura V, Sanzgiri RP, Haydon PG, (1998) Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur J Neurosci 10: 2129-2142.
34. Araque A, Sanzgiri RP, Parpura V, Haydon PG, (1998) Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J Neurosci 18: 6822-6829.
35. Kang J, Jiang L, Goldman SA, Nedergaard M, (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1: 683-692.
36. Serrano A, Haddjeri N, Lacaille J, Robitaille R, (2006) GABAergic network activation of glial cells underlies heterosynaptic depression. J Neurosci 26: 5370-5382.
37. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, et al. (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310: 113-116.
38. Gordon GRJ, Iremonger KJ, Kantevari S, Ellis-Davies GCR, MacVicar BA, et al. (2009) Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron 64: 391-403.
39. Newman EA, (2003) Glial cell inhibition of neurons by release of ATP. J Neurosci 23: 1659-1666.
40. Rousse I, St-Amour A, Darabid H, Robitaille R, (2010) Synapse-glia interactions are governed by synaptic and intrinsic glial properties. Neuroscience 167: 621-632.
41. Todd KJ, Darabid H, Robitaille R, (2010) Perisynaptic glia discriminate patterns of motor nerve activity and influence plasticity at the neuromuscular junction. J Neurosci 30: 11870-11882.
42. Robinson R, (1998) Modulation of synaptic efficacy and synaptic depression by glial cells at the frog neuromuscular junction. Neuron 21: 847-855.
43. Fellin T, (2009) Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity. J Neurochem 108: 533-544.
44. Montana V, Malarkey EB, Verderio C, Matteoli M, Parpura V, (2006) Vesicular transmitter release from astrocytes. Glia 54: 700-715.
45. Giaume C, Koulakoff A, Roux L, Holcman D, Rouach N, (2010) Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat Rev Neurosci 11: 87-99.
46. Kang N, Xu J, Xu Q, Nedergaard M, Kang J, (2005) Astrocytic glutamate release-induced transient depolarization and epileptiform discharges in hippocampal CA1 pyramidal neurons. J Neurophysiol 94: 4121-4130.
47. Shigetomi E, Kracun S, Sovfroniew MS, Khakh BS, (2010) A genetically targeted optical sensor to monitor calcium signals in astrocyte processes. Nature Neurosci 13: 759-766.
48. Nimmerjahn A, (2009) Astrocytes going live: advances and challenges. J Physiol 587: 1639-1647.
49. Bonansco C, Couve A, Perea G, Ferradas CA, Roncagliolo M, et al. (2011) Glutamate released spontaneously from astrocytes sets the threshold for synaptic plasticity. Eur J Neurosci 33: 1483-1492.
50. Nett WJ, Oloff SH, McCarthy KD, (2002) Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. J Neurophysiol 87: 528-537.
51. Tsodyks M, Pawelzik K, Markram H, (1998) Neural networks with dynamic synapses. Neural Comput 10: 821-835.
52. Amit DJ, Tsodyks MV, (1991) Quantitative study of attractor neural network retrieving at low spike rates: I. Substrate-spikes, rates and neuronal gain. Network 2: 259-273.
53. Del Castillo J, Katz B, (1954) Quantal components of the end-plate potential. J Physiol 124: 560-573.
54. Fuhrmann G, Segev I, Markram H, Tsodyks M, (2002) Coding of temporal information by activity-dependent synapses. J Neurophysiol 87: 140-148.
55. Markram H, Pikus D, Gupta A, Tsodyks M, (1998) Potential for multiple mechanisms, phenomena and algorithms for synaptic plasticity at single synapses. Neuropharmacology 37: 489-500.
56. Dittman JS, Regehr WG, (1998) Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18: 6147-6162.
57. Tsodyks M, (2005) Activity-dependent transmission in neocortical synapses. In: Chow CC, Gutkin B, Hansel D, Meunier C, Dalibard J, editors. Methods and Models in Neurophysics Amsterdam, The Netherlands Elsevier pp. 245-266.
58. Lee W, Parpura V, (2007) Exocytotic release of glutamate from astrocytes: comparison to neurons. In: Bean A, editors. Protein trafficking in neurons Amsterdam, The Netherlands Elsevier pp. 329-365.
59. Pasti L, Zonta M, Pozzan T, Vicini S, Carmignoto G, (2001) Cytosolic calcium oscillations in astrocytes may regulate exocytotic release of glutamate. J Neurosci 21: 477-484.
60. Bergersen LH, Gundersen V, (2009) Morphological evidence for vesicular glutamate release from astrocytes. Neuroscience 158: 260-265.
61. Zhang Q, Fukuda M, Van Bockstaele E, Pascual O, Haydon PG, (2004) Synaptotagmin IV regulates glial glutamate release. Proc Natl Acad Sci USA 101: 9441-9446.
62. Marchaland J, Calì C, Voglmaier SM, Li H, Regazzi R, et al. (2008) Fast subplasma membrane Ca2+ transients control exo-endocytosis of synaptic-like microvesicles in astrocytes. J Neurosci 28: 9122-9132.
63. Parpura V, Haydon PG, (2000) Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc Natl Acad Sci USA 97: 8629-8634.
64. Hori T, Takahashi T, (2009) Mechanisms underlying short-term modulation of transmitter release by presynaptic depolarization. J Physiol 587: 2987-3000.
65. Softky W, Koch C, (1993) The highly irregular firing pattern of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13: 334-350.
66. Bowser DN, Khakh BS, (2007) Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy. Proc Natl Acad Sci USA 104: 4212-4217.
67. Pasti L, Volterra A, Pozzan T, Carmignoto G, (1997) Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J Neurosci 17: 7817-7830.
68. Markram H, Wang Y, Tsodyks M, (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95: 5323-5328.
69. Agulhon C, Fiacco TA, McCarthy KD, (2010) Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signalling. Science 327: 1250-1254.
70. Fiacco TA, Agulhon C, Taves SR, Petravicz J, Casper KB, et al. (2007) Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 54: 611-626.
71. Volman V, Ben-Jacob E, Levine H, (2007) The astrocyte as a gatekeeper of synaptic information transfer. Neur Comput 19: 303-326.
72. Nadkarni S, Jung P, Levine H, (2008) Astrocytes optimize the synaptic transmission of information. PLoS Comput Biol 4: e1000088.
73. Goldberg M, De Pittà M, Volman V, Berry H, Ben-Jacob E, (2010) Nonlinear gap junctions enable long-distance propagation of pulsating calcium waves in astrocyte networks. PLoS Comput Biol 6: e1000909.
74. De Pittà M, Goldberg M, Volman V, Berry H, Ben-Jacob E, (2009) Glutamate-dependent intracellular calcium and IP3 oscillating and pulsating dynamics in astrocytes. J Biol Phys 35: 383-411.
75. De Pittà M, Volman V, Levine H, Ben-Jacob E, (2009) Multimodal encoding in a simplified model of intracellular calcium signaling. Cogn Proc 10: 55-70.
76. De Pittà M, Volman V, Levine H, Pioggia G, De Rossi D, et al. (2008) Coexistence of amplitude and frequency modulations in intracellular calcium dynamics. Phys Rev E 77: 030903(R).
77. Haber M, Zhou L, Murai KK, (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci 26: 8881-8891.
78. Rusakov DA, Kullmann DM, (1998) Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J Neurosci 18: 3158-3170.
79. Angulo MC, Kozlov AS, Charpak S, Audinat E, (2004) Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J Neurosci 24: 6920-6927.
80. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, et al. (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43: 729-743.
81. Sasaki T, Kuga T, Namiki S, Matsuki N, Ikegaya Y, (2011) Locally synchronized astrocytes. Cerebral Cortex In press.
82. Tian GF, Azmi H, Takahiro T, Xu Q, Peng W, et al. (2005) An astrocytic basis of epilepsy. Nature Med 11: 973-981.
83. Oliet SHR, Piet R, Poulain DA, (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292: 923-926.
84. Bezzi P, Volterra A, (2001) A neuron-glia signalling network in the active brain. Curr Opinion Neurobiol 11: 387-394.
85. Aguado F, Espinosa-Parrilla JF, Carmona MA, Soriano E, (2002) Neuronal activity regulates correlated network properties of spontaneous calcium transients in astrocytes in situ. J Neurosci 22: 9430-9444.
86. Halassa MM, Fellin T, Takano H, Dong JH, Haydon PG, (2007) Synaptic islands defined by the territory of a single astrocyte. J Neurosci 27: 6473-6477.
87. Dan Y, Poo MM, (2004) Spike timing-dependent plasticity of neural circuits. Neuron 44: 23-30.
88. Henneberger C, Papouin T, Oliet SHR, Rusakov DA, (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463: 232-237.
89. Santello M, Volterra A, (2010) Astrocytes as aide-mémoires. Nature 463: 169-170.
90. Abbott LF, Nelson SB, (2000) Synaptic plasticity: taming the beast. Nature 3: 1178-1183.
91. Li Y, Rinzel J, (1994) Equations for InsP3 receptor-mediated [Ca2+]i oscillations derived from a detailed kinetic model: A Hodgkin-Huxley like formalism. J Theor Biol 166: 461-473.
92. Diamond JS, Jahr CE, (2000) Synaptically released glutamate does not overwhelm transporters on hippocampal astrocytes during high-frequency stimulation. J Neurophysiol 83: 2835-2843.
93. Cochilla AJ, Alford S, (1998) Metabotropic glutamate receptor-mediated control of neurotransmitter release. Neuron 20: 1007-1016.
94. Gereau RW IV, Conn J, (1995) Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J Neurosci 15: 6879-6889.
95. Baskys A, Malenka RC, (1991) Agonists at metabotropic glutamate receptors presynaptically inhibit EPSCs in neonatal rat hippocampus. J Physiol 444: 687-701.