Tonic excitation and inhibition of neurons: Ambient transmitter sources and computational consequences

Progress in Biophysics and Molecular Biology

Volumn 87, Issue 1 SPEC. ISS., 2005, Pages 3-16

  Cavelier, Pauline ^a   Hamann, Martine ^a   Rossi, David ^a   Mobbs, Peter ^a   Attwell, David ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Ambient; Extracellular; GABA; Glutamate; Release; Tonic; Uptake

Indexed keywords

EID: 4744367001     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2004.06.001     Document Type: Review

References (93)

1. D. Attwell, B. Barbour, and M. Szatkowski Nonvesicular release of neurotransmitter Neuron 11 1993 401 407
2. D.A. Baker, Z. Xi, H. Shen, C.J. Swanson, and P.W. Kalivas The origin and neuronal function of in vivo nonsynaptic glutamate J. Neurosci. 22 2002 9134 9141
3. D.A. Baker, K. McFarland, R.W. Lake, H. Shen, X.C. Tang, S. Toda, and P.W. Kalivas Neuroadaptations in cystine-glutamate exchange underlie cocaine relapse Nat. Neurosci. 6 2003 743 749
4. T.G. Banke, and S.F. Traynelis Activation of NR1/NR2B NMDA receptors Nat. Neurosci. 6 2003 144 152
5. S. Bannai Transport of cystine and cysteine in mammalian cells Biochem. Biophys. Acta 779 1984 289 306
6. M.V.L. Bennett, J.E. Contreras, F.F. Bukauskas, and J.C. Saez New roles for astrocytes gap junction hemichannels have something to communicate Trends Neurosci. 26 2003 610 617
7. H. Benveniste, J. Drejer, A. Schousboe, and N.H. Diemer Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis J. Neurochem. 43 1984 1369 1374
8. O. Bernander, R.J. Douglas, K.A.C. Martin, and C. Koch Synaptic background activity influences spatiotemporal integration in single pyramidal cells Proc. Natl. Acad. Sci. USA 88 1991 11569 11573
9. P. Bezzi, G. Carmignoto, L. Pasti, S. Vesce, D. Rossi, B.L. Rizzini, T. Pozzan, and A. Volterra Prostaglandins stimulate calcium-dependent glutamate release in astrocytes Nature 391 1998 281 285
10. L.J. Borg-Graham, C. Monier, and Y. Fregnac Visual input evokes transient and strong shunting inhibition in visual cortical neurons Nature 393 1998 369 372
11. A receptors J. Physiol. 497 1996 753 759
12. S.G. Brickley, V. Revilla, S.G. Cull-Candy, W. Wisden, and M. Farrant Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance Nature 409 2001 88 92
13. 2+ transients and their transmission in the developing chick retina Curr. Biol. 8 1998 283 286
14. Cavelier, P., Attwell, D., 2004. Tonic release of glutamate in rat hippocampal slices by a DIDS-sensitive mechanism. J. Physiol. Proc., 555p, C46 (http://www.physoc.org/publications/proceedings/archive/article.asp?ID=555PC46).
15. F.S. Chance, L.F. Abbott, and A.D. Reyes Gain modulation from background synaptic input Neuron 35 2002 773 782
16. K. Chergui, P.J. Charlety, H. Akaoka, C.F. Saunier, J.L. Brunet, M. Buda, T.H. Svensson, and G. Chouvet Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo Eur. J. Neurosci. 5 1993 137 144
17. Y. Cho, and S. Bannai Uptake of glutamate and cystine in C-6 glioma cells and in cultured astrocytes J. Neurochem. 55 1990 2091 2097
18. D.W. Choi Ionic dependence of glutamate neurotoxicity J. Neurosci. 7 1987 369 379
19. D. Colquhoun, and A.G. Hawkes Desensitization of NMDA receptors a problem of interpretation Proc. Natl. Acad. Sci. USA 92 1995 10327 10329
20. D. Colquhoun, P. Jonas, and B. Sakmann Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices J. Physiol. 458 1992 261 287
21. N.O. Dalby, and I. Mody Activation of NMDA receptors in rat dentate gyrus granule cells by spontaneous and evoked transmitter release J. Neurophysiol. 90 2003 786 797
22. 2+- and SNARE-independent release of GABA and glutamate prior to synapse formation Neuron 36 2002 1051 1061
23. A. Destexhe, and D. Pare Impact of network activity on the integrative properties of neocortical pyramidal cells in vivo Journal of Neurophysiology 81 1999 1531 1547
24. R. Dingledine, K. Borges, D. Bowie, and S.F. Traynelis The glutamate receptor ion channels Pharmacol. Rev. 51 1999 7 61
25. 7 receptor-mediated release of excitatory amino acids from astrocytes J. Neurosci. 23 2003 1320 1328
26. A.C. Flint, X. Liu, and A.R. Kriegstein Nonsynaptic glycine receptor activation during early neocortical development Neuron 20 1998 43 53
27. I.D. Forsythe, and J.D. Clements Presynaptic glutamate receptors depress excitatory monosynaptic transmission between mouse hippocampal neurones J. Physiol. 429 1990 1 16
28. +-independent neutral amino acid transporter that associates with the 4F2 heavy chain and exhibits substrate selectivity for small neutral d- and l-amino acids J. Biol. Chem. 275 2000 9690 9698
29. F. Gabbiani, J. Midtgaard, and T. Knopfel Synaptic integration in a model of cerebellar granule cells J. Neurophysiol. 72 1994 999 1009
30. H. Hagberg, A. Lehmann, M. Sandberg, B. Nystrom, I. Jacobson, and A. Hamberger Ischemia-induced shift of inhibitory and excitatory amino acids from intra- to extracellular compartments J. Cerebral Blood Flow Metab. 5 1985 413 419
31. M. Hamann, D. Rossi, and D. Attwell Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex Neuron 33 2002 625 633
32. M. Hausser, and B.A. Clark Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration Neuron 19 1997 665 678
33. J.A. Hirsch, J.-M. Alonso, R.C. Reid, and L.M. Martinez Synaptic integration in striate cortical simple cells J. Neurosci. 18 1998 9517 9528
34. G.R. Holt, and C. Koch Shunting inhibition does not have a divisive effect on firing rates Neural Comput. 9 1997 1001 1013
35. D. Jabaudon, K. Shimamoto, Y. Yasuda-Kamatani, M. Scanziani, B.H. Gähwiler, and U. Gerber Inhibition of uptake unmasks rapid extracellular turnover of glutamate of nonvesicular origin Proc. Natl. Acad. Sci. USA 96 1999 8733 8738
36. M. Kaneda, M. Farrant, and S.G. Cull-Candy Whole-cell and single-channel currents activated by GABA and glycine in granule cells of the rat cerebellum J. Physiol. 485 1995 419 435
37. T. Kenet, D. Bibitchkov, M. Tsodyks, A. Grinvald, and A. Arieli Spontaneously emerging cortical representations of visual attributes Nature 425 2003 954 956
38. S.J. Kim, Y.S. Kim, J.P. Yuan, R.S. Petralia, P.F. Worley, and D.J. Linden Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1 Nature 426 2003 285 291
39. H.K. Kimelberg, S.K. Goderie, S. Higman, S. Pang, and R.A. Waniewski Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures J. Neurosci. 10 1990 1583 1591
40. H. Komuro, and P. Rakic Modulation of neuronal migration by NMDA receptors Science 260 1993 95 97
41. M. Krzan, M. Stenovec, M. Kreft, T. Pangrsic, S. Grilc, P.G. Haydon, and R. Zorec Calcium-dependent exocytosis of atrial natriuretic peptide from astrocytes J. Neurosci. 23 2003 1580 1583
42. A receptor subunit mRNAs in the rat brain II olfactory bulb and cerebellum J. Neurosci. 12 1992 1063 1076
43. +-dependent glutamate uptake J. Neurosci. 18 1998 9620 9628
44. F. Lin, and C.F. Stevens Both open and closed NMDA receptors desensitize J. Neurosci. 14 1994 2153 2160
45. - channels by astrocyte-derived GABA in cultured embryonic rat hippocampal neurons J. Neurophysiol. 84 2000 1392 1403
46. A. Losonczy, P. Somogyi, and Z. Nusser Reduction of excitatory postsynaptic responses by persistently active metabotropic glutamate receptors in the hippocampus J. Neurophysiol. 89 2003 1910 1919
47. J.J. LoTurco, D.F. Owens, M.J. Heath, M.B. Davis, and A.R. Kriegstein GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis Neuron 15 1995 1287 1298
48. R. Maex, and E. De Schutter Synchronization of Golgi and granule cell firing in a detailed network model of the cerebellar granule cell layer J. Neurophysiol. 80 1998 2521 2537
49. D. Marr A theory of cerebellar cortex J. Physiol. 202 1969 437 470
50. C.J. McBain, T.J. DiChiara, and J.A. Kauer Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission J. Neurosci. 14 1994 4433 4445
51. S.J. Mitchell, and R.A. Silver Shunting inhibition modulates neuronal gain during synaptic excitation Neuron 38 2003 433 445
52. F.C. Moos, K. Rossi, and P. Richard Activation of N-methyl-d-aspartate receptors regulates basal electrical activity of oxytocin and vasopressin neurons in lactating rats Neuroscience 77 1997 993 1002
53. T.H. Murphy, M. Miyamoto, A. Sastre, R.L. Schnaar, and J.T. Coyle Glutamate toxicity in a neuronal cell line involves inhibition of cystine transport leading to oxidative stress Neuron 2 1989 1547 1558
54. A receptors to synaptic and extrasynaptic membranes of cerebellar granule cells J. Neurosci. 18 1998 1693 1703
55. A.V. Paternain, A. Rodriguez-Moreno, A. Villarroel, and J. Lerma Activation and desensitization properties of native and recombinant kainate receptors Neuropharmacology 37 1998 1249 1259
56. D.K. Patneau, and M.L. Mayer Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-d-aspartate and quisqualate receptors J. Neurosci. 10 1990 2385 2399
57. I.A. Pearce, M.A. Cambray-Deakin, and R.D. Burgoyne Glutamate acting on NMDA receptors stimulates neurite outgrowth from cerebellar granule cells FEBS Lett. 223 1987 143 147
58. J.W. Phillis, M. Smith-Barbour, L.M. Perkins, and M.H. O'Regan Characterization of glutamate, aspartate, and GABA release from ischemic rat cerebral cortex Brain Res. Bull. 34 1994 457 466
59. J.P. Pin, and R. Duvoisin The metabotropic glutamate receptors structure and functions Neuropharmacology 34 1995 1 26
60. S.A. Prescott, and Y. De Koninck Gain control of firing rate by shunting inhibition roles of synaptic noise and dendritic saturation Proc. Natl. Acad. Sci. USA 100 2003 2076 2081
61. S. Rabacchi, Y. Bailly, N. Delhaye-Bouchaud, and J. Mariani Involvement of the NMDA receptor in synapse elimination during cerebellar development Science 256 1992 1823 1825
62. M. Rapp, Y. Yarom, and I. Segev The impact of parallel fibre background activity on the cable properties of cerebellar Purkinje cells Neural Comput. 4 1992 518 532
63. G.B. Richerson, and Y. Wu Dynamic equilibrium of neurotransmitter transporters not just for reuptake anymore J. Neurophysiol. 90 2003 1363 1374
64. D.J. Rossi, and N.T. Slater The developmental onset of NMDA receptor-channel activity during neuronal migration Neuropharmacology 32 1993 1239 1248
65. D. Rossi, T. Oshima, and D. Attwell Glutamate release in severe brain ischaemia is mainly by reversed uptake Nature 403 2000 316 321
66. D.J. Rossi, M. Hamann, and D. Attwell Multiple modes of GABAergic inhibition of rat cerebellar granule cells J. Physiol. 548 2003 97 110
67. 3H]-d-aspartate from primary astrocyte cultures in response to raised external potassium J. Neurosci. 16 1996 7803 7811
68. P. Sah, S. Hestrin, and R.A. Nicoll Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons Science 246 1989 815 818
69. H. Sato, M. Tamba, T. Ishii, and S. Bannai Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins J. Biol. Chem. 274 1999 11455 11458
70. A receptor isoforms Mol. Pharmacol. 49 1996 567 579
71. A. Semyanov, M.C. Walker, and D.M. Kullmann GABA uptake regulates cortical excitability via cell type-specific tonic inhibition Nat. Neurosci. 6 2003 484 490
72. W. Singer Synchronization of cortical activity and its putative role in information processing and learning Annu. Rev. Physiol. 55 1993 349 374
73. T.C. Smith, and J.R. Howe Concentration-dependent substate behavior of native AMPA receptors Nat. Neurosci. 3 2000 992 997
74. 7 receptors in the regulation of neurotransmitter release in the rat hippocampus J. Neurochem. 81 2002 1196 1211
75. A conductances in hippocampal neurons J. Neurosci. 22 2002 RC223
76. A receptors Proc. Natl. Acad. Sci. USA 100 2003 14439 14444
77. S. Supplisson, and M.J. Roux Why glycine transporters have different stoichiometries FEBS Lett. 529 2002 93 101
78. K. Takagi, M.D. Ginsberg, M.Y.T. Globus, D. Dietrich, E. Martinez, S. Kraydieh, and R. Busto Changes in amino acid neurotransmitters and cerebral blood flow in the ischemic penumbral region following middle cerebral artery occlusion in the rat correlation with histopathology J. Cerebral Blood Flow Metab. 13 1993 575 585
79. J. Taylor, and P.R. Gordon-Weeks Calcium-independent gamma-aminobutyric acid release from growth cones role of gamma-aminobutyric acid transport J. Neurochem. 56 1991 273 280
80. 6 subunit J. Neurosci. 16 1996 3630 3640
81. T. Tyrrell, and D. Willshaw Cerebellar cortex its simulation and the relevance of Marr's theory Philos. Trans. Roy. Soc. London B 336 1992 239 257
82. F. Wahl, T.P. Obrenovitch, A.M. Hardy, M. Plotkine, R. Boulu, and L. Symon Extracellular glutamate during focal cerebral ischaemia in rats time course and calcium-dependency J. Neurochem. 63 1994 1003 1011
83. A receptor expression at adult rat Golgi cell to granule cell synapses Neuropharmacology 43 2002 737 749
84. A receptor-mediated currents in granule cells of postnatal rat cerebellum Eur. J. Neurosci. 9 1997 533 548
85. --dependent mechanism Glia 37 2002 8 18
86. O. Warr, M. Takahashi, and D. Attwell Modulation of extracellular glutamate concentration in rat brain slices by cystine-glutamate exchange J. Physiol. 514 1999 783 793
87. L. Westergren, B. Nystrom, A. Hamberger, and B.B. Johansson Intracerebral dialysis and the blood brain barrier J. Neurochem. 64 1995 229 234
88. M.A. Whittington, R.D. Traub, and J.G. Jefferys Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation Nature 373 1995 612 615
89. T.J. Wilding, and J.E. Huettner Activation and desensitization of hippocampal kainate receptors J. Neurosci. 17 1997 2713 2721
90. I. Wyatt, A. Gyte, M.G. Simpson, P.S. Widdowson, and E.A. Lock The role of glutathione in L-2-chloropropionic acid induced cerebellar granule cell necrosis in the rat Arch. Toxicol. 70 1996 724 735
91. Z.C. Ye, M.S. Wyeth, S. Baltan-Tekkok, and B.R. Ransom Functional hemichannels in astrocytes a novel mechanism of glutamate release J. Neurosci. 23 2003 3588 3596
92. N. Zerangue, and M.P. Kavanaugh Flux coupling in a neuronal glutamate transporter Nature 383 1996 634 637
93. C.F. Zorumski, S. Mennerick, and J. Que Modulation of excitatory synaptic transmission by low concentrations of glutamate in cultured rat hippocampal neurons J. Physiol. 494 1996 465 477