Extracellular diffusivity determines contribution of high-versus low-affinity receptors to neural signaling

NeuroImage

Volumn 25, Issue 1, 2005, Pages 101-111

  Savtchenko, Leonid P ^a   Rusakov, Dmitri A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Affinity; Dextran molecule; Diffusivity

Indexed keywords

AMPA RECEPTOR; DEXTRAN; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER;

ANIMAL TISSUE; ARTICLE; BATH; BRAIN SLICE; CONTROLLED STUDY; DIFFUSION; EVOKED RESPONSE; EXTRACELLULAR SPACE; LIQUID CULTURE; MALE; MEMBRANE CURRENT; MICROSCOPY; MOLECULE; NERVE CELL; NERVE CELL NETWORK; NERVE EXCITABILITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PHOTON; PRIORITY JOURNAL; RAT; RECEPTOR AFFINITY; RECORDING; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANE;

EID: 14244257039     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2004.11.020     Document Type: Article

References (82)

1. R.D. Andrew, and B.A. Macvicar Imaging cell volume changes and neuronal excitation in the hippocampal slice Neuroscience 62 1994 371 383
2. N. Arnth-Jensen, D. Jabaudon, and M. Scanziani Cooperation between independent hippocampal synapses is controlled by glutamate uptake Nat. Neurosci. 5 2002 325 331
3. F. Asztely, G. Erdemli, and D.M. Kullmann Extrasynaptic glutamate spillover in the hippocampus: dependence on temperature and the role of active glutamate uptake Neuron 18 1997 281 293
4. B.A. Ballyk, S.J. Quackenbush, and R.D. Andrew Osmotic effects on the CA1 neuronal population in hippocampal slices with special reference to glucose J. Neurophysiol. 65 1991 1055 1066
5. B. Barbour, B.U. Keller, I. Llano, and A. Marty Prolonged presence of glutamate during excitatory synaptic transmission to cerebellar Purkinje cells Neuron 12 1994 1331 1343
6. T.A. Basarsky, D. Feighan, and B.A. MacVicar Glutamate release through volume-activated channels during spreading depression J. Neurosci. 19 1999 6439 6445
7. D.P. Bradley, J.M. Smith, M.I. Smith, K.H. Bockhorst, N.G. Papadakis, L.D. Hall, A.A. Parsons, M.F. James, and C.L. Huang Cortical spreading depression in the feline brain following sustained and transient stimuli studied using diffusion-weighted imaging J. Physiol. 544 2002 39 56
8. A.G. Carter, and W.G. Regehr Prolonged synaptic currents and glutamate spillover at the parallel fiber to stellate cell synapse J. Neurosci. 20 2000 4423 4434
9. J.D. Clements Transmitter timecourse in the synaptic cleft: its role in central synaptic function Trends Neurosci. 5 1996 163 170
10. J.D. Clements, and J.M. Bekkers Detection of spontaneous synaptic events with an optimally scaled template Biophys. J. 73 1997 220 229
11. 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
12. J.S. Diamond Neuronal glutamate transporters limit activation of NMDA receptors by neurotransmitter spillover on CA1 pyramidal cells J. Neurosci. 21 2001 8328 8338
13. R.M. Dijkhuizen, and K. Nicolay Magnetic resonance imaging in experimental models of brain disorders J. Cereb. Blood Flow Metab. 23 2003 1383 1402
14. T.Q. Duong, J.V. Sehy, D.A. Yablonskiy, B.J. Snider, J.J. Ackerman, and J.J. Neil Extracellular apparent diffusion in rat brain Magn. Reson. Med. 45 2001 801 810
15. 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 34 1995 1387 1395
16. W.R. Holmes Modeling the effect of glutamate diffusion and uptake on NMDA and non-NMDA receptor saturation Biophys. J. 69 1995 1734 1747
17. T. Hosokawa, D.A. Rusakov, T.V.P. Bliss, and A. Fine Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP J. Neurosci. 15 1995 5560 5573
18. S. Hrabetova, J. Hrabe, and C. Nicholson Dead-space microdomains hinder extracellular diffusion in rat neocortex during ischemia J. Neurosci. 23 2003 8351 8359
19. P. Jonas, G. Major, and B. Sakmann Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus J. Physiol. 472 1993 615 663
20. K. Khanafer, K. Vafai, and A. Kangarlu Computational modeling of cerebral diffusion-application to stroke imaging Magn. Reson. Imaging 21 2003 651 661
21. C.D. Kroenke, J.J. Ackerman, and J.J. Neil Magnetic resonance measurement of tetramethylammonium diffusion in rat brain: comparison of magnetic resonance and ionophoresis in vivo diffusion measurements Magn. Reson. Med. 50 2003 717 726
22. D.M. Kullmann Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation Neuron 12 1994 1111 1120
23. D.M. Kullmann, M.Y. Min, F. Asztely, and D.A. Rusakov Extracellular glutamate diffusion determines the occupancy of glutamate receptors at CA1 synapses in the hippocampus Philos. Trans. R. Soc., Ser. B 354 1999 395 402
24. J. Kume-Kick, T. Mazel, I. Vorisek, S. Hrabetova, L. Tiao, and C. Nicholson Independence of extracellular tortuosity and volume fraction during osmotic challenge in rat neocortex J. Physiol. 542 2002 515 527
25. J.H. Lee, and C.S. Springer Jr. Effects of equilibrium exchange on diffusion-weighted NMR signals: the diffusigraphic "shutter-speed" Magn. Reson. Med. 49 2003 450 458
26. K.P. Lehre, and N.C. Danbolt The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain J. Neurosci. 18 1998 8751 8757
27. K.P. Lehre, and D.A. Rusakov Asymmetry of glia near central synapses favors presynaptically directed glutamate escape Biophys. J. 83 2002 125 134
28. R.A.J. Lester, and C.E. Jahr NMDA channel behavior depends on agonist affinity J. Neurosci. 12 1992 635 643
29. T. Li, and A.W. Song Fast functional brain signal changes detected by diffusion weighted fMRI Magn. Reson. Imaging 21 2003 829 833
30. L. Liu, T.P. Wong, M.F. Pozza, K. Lingenhoehl, Y. Wang, M. Sheng, Y.P. Auberson, and Y.T. Wang Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity Science 304 2004 1021 1024
31. N.A. Lozovaya, S.E. Grebenyuk, T.S. Tsintsadze, B. Feng, D.T. Monaghan, and O. Krishtal Extrasynaptic NR2B and NR2D subunits of NMDA receptors are shaping "superslow" afterburst EPSC in hippocampus J. Physiol. 558 2004 457 463
32. H.D. Lux, U. Heinemann, and I. Dietzel Ionic changes and alterations in the size of the extracellular space during epileptic activity Adv. Neurol. 44 1986 619 639
33. T. Mazel, Z. Simonova, and E. Sykova Diffusion heterogeneity and anisotropy in rat hippocampus NeuroReport 9 1998 1299 1304
34. C.J. McBain, S.F. Traynelis, and R. Dingledine Regional variation of extracellular space in the hippocampus Science 249 1990 674 677
35. M.Y. Min, D.A. Rusakov, and D.M. Kullmann Activation of AMPA, kainate, and metabotropic receptors at hippocampal mossy fiber synapses: role of glutamate diffusion Neuron 21 1998 561 570
36. S.J. Mitchell, and R.A. Silver GABA spillover from single inhibitory axons suppresses low-frequency excitatory transmission at the cerebellar glomerulus J. Neurosci. 20 2000 8651 8658
37. G.C. Newman, F.E. Hospod, H. Qi, and H. Patel Effects of dextran on hippocampal brain slice water, extracellular space, calcium kinetics and histology J. Neurosci. Methods 61 1995 33 46
38. C. Nicholson, and E. Sykova Extracellular space structure revealed by diffusion analysis Trends Neurosci. 21 1998 207 215
39. C. Nicholson, and L. Tao Hindered diffusion of high molecular weight compounds in brain extracellular microenvironment measured with integrative optical imaging Biophys. J. 65 1993 2277 2290
40. T.A. Nielsen, D.A. DiGregorio, and R.A. Silver Modulation of glutamate mobility reveals the mechanism underlying slow-rising AMPAR EPSCs and the diffusion coefficient in the synaptic cleft Neuron 42 2004 757 771
41. Z. Nusser, R. Lujan, G. Laube, J.D.B. Roberts, E. Molnar, and P. Somogyi Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus Neuron 21 1998 545 559
42. T.G. Oertner, B.L. Sabatini, E.A. Nimchinsky, and K. Svoboda Facilitation at single synapses probed with optical quantal analysis Nat. Neurosci. 5 2002 657 664
43. J.M. O'Shea, S.R. Williams, N. van Bruggen, and A.R. Gardner-Medwin Apparent diffusion coefficient and MR relaxation during osmotic manipulation in isolated turtle cerebellum Magn. Reson. Med. 44 2000 427 432
44. T.S. Otis, and M.P. Kavanaugh Isolation of current components and partial reaction cycles in the glial glutamate transporter EAAT2 J. Neurosci. 20 2000 2749 2757
45. C.S. Patlak, F.E. Hospod, S.D. Trowbridge, and G.C. Newman Diffusion of radiotracers in normal and ischemic brain slices J. Cereb. Blood Flow Metab. 18 1998 776 802
46. M.A. Perez-Pinon, L. Tao, and C. Nicholson Extracellular potassium, volume fraction, and tortuosity in rat hippocampal CA1, CA3, and cortical slices during ischemia J. Neurophysiol. 74 1995 565 573
47. D. Perrais, and N. Ropert Altering the concentration of GABA in the synaptic cleft potentiates miniature IPSCs in rat occipital cortex Eur. J. Neurosci. 12 2000 400 404
48. J. Pfeuffer, I. Tkac, and R. Gruetter Extracellular-intracellular distribution of glucose and lactate in the rat brain assessed noninvasively by diffusion-weighted 1H nuclear magnetic resonance spectroscopy in vivo J. Cereb. Blood Flow Metab. 20 2000 736 746
49. S. Prokopova-Kubinova, L. Vargova, L. Tao, K. Ulbrich, V. Subr, E. Sykova, and C. Nicholson Poly[N-(2-hydroxypropyl)methacrylamide] polymers diffuse in brain extracellular space with same tortuosity as small molecules Biophys. J. 80 2001 542 548
50. C. Racca, F.A. Stephenson, P. Streit, J.D.B. Roberts, and P. Somogyi NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area J. Neurosci. 20 2000 2512 2522
51. C.A. Reid, D.B. Dixon, M. Takahashi, T.V. Bliss, and A. Fine Optical quantal analysis indicates that long-term potentiation at single hippocampal mossy fiber synapses is expressed through increased release probability, recruitment of new release sites, and activation of silent synapses J. Neurosci. 24 2004 3618 3626
52. D.J. Rossi, and M. Hamann Spillover-mediated transmission at inhibitory synapses promoted by high affinity alpha(6) subunit GABA(A) receptors and glomerular geometry Neuron 20 1998 783 795
53. 2+ depletion Biophys. J. 81 2001 1947 1959
54. 2+ depletion contributes to fast activity-dependent modulation of synaptic transmission in the brain Neuron 37 2003 287 297
55. D.A. Rusakov, and D.M. Kullmann Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation J. Neurosci. 18 1998 3158 3170
56. D.A. Rusakov, and D.M. Kullmann Geometric and viscous components of the tortuosity of the extracellular space in the brain Proc. Natl. Acad. Sci. U. S. A. 95 1998 8975 8980
57. 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 305 2004 1912
58. 2+ current modulation by mGluRs at individual hippocampal synapses Cereb. Cortex 14 2004 748 758
59. 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
60. S. Satake, F. Saitow, J. Yamada, and S. Konishi Synaptic activation of AMPA receptors inhibits GABA release from cerebellar interneurons Nat. Neurosci. 3 2000 551 558
61. T. Schikorski, and C.F. Stevens Quantitative ultrastructural analysis of hippocampal excitatory synapses J. Neurosci. 17 1997 5858 5867
62. A. Scimemi, A. Fine, D.M. Kullmann, and D.A. Rusakov NR2B-containing receptors mediate cross talk among hippocampal synapses J. Neurosci. 24 2004 4767 4777
63. D.K. Selig, G.O. Hjelmstad, C. Herron, R.A. Nicoll, and R.C. Malenka Independent mechanisms for long-term depression of AMPA and NMDA responses Neuron 15 1995 417 426
64. A. Semyanov, and D.M. Kullmann Modulation of GABAergic signaling among interneurons by metabotropic glutamate receptors Neuron 25 2000 663 672
65. M.D. Silva, T. Omae, K.G. Helmer, F. Li, M. Fisher, and C.H. Sotak Separating changes in the intra- and extracellular water apparent diffusion coefficient following focal cerebral ischemia in the rat brain Magn. Reson. Med. 48 2002 826 837
66. G.R. Smith, and M.S.P. Sansom Dynamic properties of Na+ ions in models of ion channels: a molecular dynamics study Biophys. J. 75 1998 2767 2782
67. P.T.C. So, K.H. Kim, C. Buehler, B. Masters, L. Hsu, and C.Y. Dong Basic principles of multiphoton excitation microscopy A. Periasamy Cellular Imaging 2001 OUP Oxford, NY 147 161
68. A.W. Song, T. Harshbarger, T. Li, K.H. Kim, K. Ugurbil, S. Mori, and D.S. Kim Functional activation using apparent diffusion coefficient-dependent contrast allows better spatial localization to the neuronal activity: evidence using diffusion tensor imaging and fiber tracking NeuroImage 20 2003 955 961
69. M. Stroh, W.R. Zipfel, R.M. Williams, W.W. Webb, and W.M. Saltzman Diffusion of nerve growth factor in rat striatum as determined by multiphoton microscopy Biophys. J. 85 2003 581 588
70. E. Sykova, L. Vargova, D. Kubinova, P. Jendelova, and A. Chvatal The relationship between changes in intrinsic optical signals and cell swelling in rat spinal cord slices NeuroImage 18 2003 214 230
71. A. Szafer, J. Zhong, and J.C. Gore Theoretical model for water diffusion in tissues Magn. Reson. Med. 33 1995 697 712
72. Y. Takumi, V. Ramirez-Leon, P. Laake, E. Rinvik, and O.P. Ottersen Different modes of expression of AMPA and NMDA receptors in hippocampal synapses Nat. Neurosci. 2 1999 618 624
73. L. Tao, and C. Nicholson The three-dimensional point spread functions of a microscope objective in image and object space J. Microsc. 178 Pt 3 1995 267 271
74. I.W. Tatum, A. Malek, M. Recio, J. Orlowski, and R. Murtagh Diffusion-weighted imaging and status epilepticus during vagus nerve stimulation Epilepsy Behav. 5 2004 411 415
75. J. Trommershauser, J. Marienhagen, and A. Zippelius Stochastic model of central synapses: slow diffusion of transmitter interacting with spatially distributed receptors and transporters J. Theor. Biol. 198 1999 101 120
76. E. Tsvetkov, R.M. Shin, and V.Y. Bolshakov Glutamate uptake determines pathway specificity of long-term potentiation in the neural circuitry of fear conditioning Neuron 41 2004 139 151
77. R. Ventura, and K.M. Harris Three-dimensional relationships between hippocampal synapses and astrocytes J. Neurosci. 19 1999 6897 6906
78. T. Watanabe, A. Ohtsuka, N. Murase, P. Barth, and K. Gersonde NMR studies on water and polymer diffusion in dextran gels. Influence of potassium ions on microstructure formation and gelation mechanism Magn. Reson. Med. 35 1996 697 705
79. K.L. Yam, D.K. Anderson, and R.E. Buxbaum Diffusion of small solutes in polymer-containing solutions Science 241 1988 330
80. A. Zador, and C. Koch Linearized models of calcium dynamics-Formal equivalence to the cable equation J. Neurosci. 14 1994 4705 4715
81. G.A. Zampighi, and R.S. Fisher Polyhedral protein cages encase synaptic vesicles and participate in their attachment to the active zone J. Struct. Biol. 119 1997 347 359
82. W.R. Zipfel, and W.W. Webb In vivo diffusion measurements using multiphoton excitation fluorescence photobleaching recovery and fluorescence correlation microscopy A. Periasamy Methods in Cellular Imaging 2001 Oxford Univ. Press Oxford 216 235