Evaluation of glutamate concentration transient in the synaptic cleft of the rat calyx of Held

Journal of Physiology

Volumn 591, Issue 1, 2013, Pages 219-239

  Budisantoso, Timotheus ^a,b   Harada, Harumi ^a   Kamasawa, Naomi ^a   Fukazawa, Yugo ^a,b,c   Shigemoto, Ryuichi ^a,b,c   Matsui, Ko ^a,b,c  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMIC ACID; POSTSYNAPTIC RECEPTOR; SYNAPSE RECEPTOR;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALYX OF HELD SYNAPSE; CONTROLLED STUDY; DENDRITE; ELECTRICAL SYNAPSE; EVOKED RESPONSE; FREEZE FRACTURE; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE ENDING; NONHUMAN; PERINATAL PERIOD; POSTSYNAPTIC MEMBRANE; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SECRETION; RAT; SIMULATION; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN; COMPUTER SIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; MODELS, BIOLOGICAL; RATS; RATS, LONG-EVANS; RATS, WISTAR; RECEPTORS, AMPA; SYNAPSES;

EID: 84872034574     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.241398     Document Type: Article

References (68)

1. Auger C, Kondo S & Marty A (1998). Multivesicular release at single functional synaptic sites in cerebellar stellate and basket cells. J Neurosci 18, 4532-4547.
2. Barbour B (2001). An evaluation of synapse independence. J Neurosci 21, 7969-7984.
3. Barbour B & Häusser M (1997). Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20, 377-384.
4. Beato M (2008). The time course of transmitter at glycinergic synapses onto motoneurons. J Neurosci 28, 7412-7425.
5. Bekkers JM & Stevens CF (1996). Cable properties of cultured hippocampal neurons determined from sucrose-evoked miniature EPSCs. J Neurophysiol 75, 1250-1255.
6. Biró AA, Holderith NB & Nusser Z (2005). Quantal size is independent of the release probability at hippocampal excitatory synapses. J Neurosci 25, 223-232.
7. Bruns D & Jahn R (1995). Real-time measurement of transmitter release from single synaptic vesicles. Nature 7, 62-65.
8. Budisantoso T, Matsui K, Kamasawa N, Fukazawa Y & Shigemoto R (2012). Mechanisms underlying signal filtering at a multisynapse contact. J Neurosci 32, 2357-2376.
9. Cathala L, Holderith NB, Nusser Z, DiGregorio DA & Cull-Candy SG (2005). Changes in synaptic structure underlie the developmental speeding of AMPA receptor-mediated EPSCs. Nat Neurosci 8, 1310-1318.
10. Chanda S & Xu-Friedman MA (2010). A low-affinity antagonist reveals saturation and desensitization in mature synapses in the auditory brain stem. J Neurophysiol 103, 1915-1926.
11. Clark BA & Cull-Candy SG (2002). Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse. J Neurosci 22, 4428-4436.
12. Clements JD, Lester RA, Tong G, Jahr CE & Westbrook GL (1992). The time course of glutamate in the synaptic cleft. Science 258, 1498-1501.
13. Diamond JS (2001). Neuronal glutamate transporters limit activation of NMDA receptors by neurotransmitter spillover on CA1 pyramidal cells. J Neurosci 21, 8328-8338.
14. Diamond JS & Jahr CE (1997). Transporters buffer synaptically released glutamate on a submillisecond time scale. J Neurosci 17, 4672-4687.
15. DiGregorio DA, Nusser Z & Silver RA (2002). Spillover of glutamate onto synaptic AMPA receptors enhances fast transmission at a cerebellar synapse. Neuron 35, 521-533.
16. Ford MC, Grothe B & Klug A (2009). Fenestration of the calyx of Held occurs sequentially along the tonotopic axis, is influenced by afferent activity, and facilitates glutamate clearance. J Comp Neurol 514, 92-106.
17. Forsythe ID & Barnes-Davies M (1993). The binaural auditory pathway: membrane currents limiting multiple action potential generation in the rat medial nucleus of the trapezoid body. Proc R Soc Lond B Biol Sci 251, 143-150.
18. Foster KA, Crowley JJ & Regehr WG (2005). The influence of multivesicular release and postsynaptic receptor saturation on transmission at granule cell to Purkinje cell synapses. J Neurosci 25, 11655-11665.
19. Franks KM, Stevens CF & Sejnowski TJ (2003). Independent sources of quantal variability at single glutamatergic synapses. J Neurosci 23, 3186-3195.
20. Frerking M & Wilson M (1996). Saturation of postsynaptic receptors at central synapses Curr Opin Neurobiol 6, 395-403.
21. Harris KM & Sultan P (1995). 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, 1387-1395.
22. Häusser M & Roth A (1997). Dendritic and somatic glutamate receptor channels in rat cerebellar Purkinje cells. J Physiol 501, 77-95.
23. Hodgkin AL & Huxley AF (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117, 500-544.
24. Ishikawa T, Sahara Y & Takahashi T (2002). A single packet of transmitter does not saturate postsynaptic glutamate receptors. Neuron 34, 613-621.
25. Jonas P (1995). Fast application of agonists to isolated membrane patches. In Single-Channel Recording, ed. Sakmann B & Neher E, pp. 231-243. Plenum Press, New York.
26. Joshi I, Shokralla S, Titis P & Wang LY (2004). The role of AMPA receptor gating in the development of high-fidelity neurotransmission at the calyx of Held synapse. J Neurosci 24, 183-196.
27. Karayannis T, Elfant D, Huerta-Ocampo I, Teki S, Scott RS, Rusakov DA, Jones MV & Capogna M (2010). Slow GABA transient and receptor desensitization shape synaptic responses evoked by hippocampal neurogliaform cells. J Neurosci 30, 9898-9909.
28. Koike-Tani M, Saitoh N & Takahashi T (2005). Mechanisms underlying developmental speeding in AMPA-EPSC decay time at the calyx of Held. J Neurosci 25, 199-207.
29. Kuffler SW & Yoshikami D (1975). The number of transmitter molecules in a quantum: an estimate from iontophoretic application of acetylcholine at the neuromuscular synapse. J Physiol 251, 465-482.
30. Liu G, Choi S & Tsien RW (1999). Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron 22, 395-409.
31. Longsworth LG (1953). Diffusion measurements at 25° of aqueous solutions of amino acids, peptides and sugars. J Am Chem Soc 75, 5705-5709.
32. Lorteije JA, Rusu SI, Kushmerick C & Borst JG (2009). Reliability and precision of the mouse calyx of Held synapse. J Neurosci 29, 13770-13784.
33. Matsui K, Hosoi N & Tachibana M (1998). Excitatory synaptic transmission in the inner retina: paired recordings of bipolar cells and neurons of the ganglion cell layer. J Neurosci 18, 4500-4510.
34. Matsui K, Jahr CE & Rubio E (2005). High-concentration rapid transients of glutamate mediate neural-glial communication via ectopic release. J Neurosci 25, 7538-7547.
35. Murphy GJ, Glickfeld LL, Balsen Z & Isaacson JS (2004). Sensory neuron signaling to the brain: properties of transmitter release from olfactory nerve terminals. J Neurosci 24, 3023-3030.
36. Nielsen TA, DiGregorio DA & Silver RA (2004). Modulation of glutamate mobility reveals the mechanism underlying slow-rising AMPAR EPSCs and the diffusion coefficient in the synaptic cleft. Neuron 42, 757-771.
37. Nusser Z, Lujan R, Laube G, Roberts JD, Molnár E & Somogyi P (1998). Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21, 545-559.
38. Oertner TG, Sabatini BL, Nimchinsky EA & Svoboda K (2002). Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 5, 657-664.
39. Petralia RS, Zhao HM, Wang YX & Wenthold RJ (1998). Variations in the tangential distribution of postsynaptic glutamate receptors in Purkinje cell parallel and climbing fiber synapses during development. Neuropharmacology 37, 1321-1334.
40. Raghavachari S & Lisman JE (2004). Properties of quantal transmission at CA1 synapses. J Neurophysiol 92, 2456-2467.
41. Renden R, Taschenberger H, Puente N, Rusakov DA, Duvoisin R, Wang LY, Lehre KP & von Gersdorff H (2005). Glutamate transporter studies reveal the pruning of metabotropic glutamate receptors and absence of AMPA receptor desensitization at mature calyx of held synapses. J Neurosci 25, 8482-8497.
42. Riveros N, Fiedler J, Lagos N, Muñoz C & Orrego F (1986). Glutamate in rat brain cortex synaptic vesicles: influence of the vesicle isolation procedure. Brain Res 29, 405-408.
43. Rudolph S, Overstreet-Wadiche L & Wadiche JI (2011). Desynchronization of multivesicular release enhances Purkinje cell output. Neuron 70, 991-1004.
44. Rusakov DA & Kullmann DM (1998). Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J Neurosci 18, 3158-3170.
45. Sahara Y & Takahashi T (2001). Quantal components of the excitatory postsynaptic currents at a rat central auditory synapse. J Physiol 536, 189-197.
46. Sätzler K, Söhl LF, Bollmann JH, Borst JG, Frotscher M, Sakmann B & Lübke JH (2002). Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci 22, 10567-10579.
47. Savtchenko LP & Rusakov DA (2007). The optimal height of the synaptic cleft. Proc Natl Acad Sci U S A 6, 1823-1828.
48. Scimemi A & Beato M (2009). Determining the neurotransmitter concentration profile at active synapses. Mol Neurobiol 40, 289-306.
49. Sigworth FJ (1980). The variance of sodium current fluctuations at the node of Ranvier. J Physiol 307, 97-129.
50. Somogyi P, Tamás G, Lujan R & Buhl EH (1998). Salient features of synaptic organisation in the cerebral cortex. Brain Res Rev 26, 113-135.
51. Takamori S, Holt M, Stenius K, Lemke EA, Grønborg M, Riedel D, Urlaub H, Schenck S, Brügger B, Ringler P, Müller SA, Rammner B, Gräter F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmüller H, Heuser J, Wieland F & Jahn R (2006). Molecular anatomy of a trafficking organelle. Cell 17, 831-846.
52. Tanaka J, Matsuzaki M, Tarusawa E, Momiyama A, Molnár E, Kasai H & Shigemoto R (2005). Number and density of AMPA receptors in single synapses in immature cerebellum. J Neurosci 25, 799-807.
53. Tang CM, Margulis M, Shi QY & Fielding A (1994). Saturation of postsynaptic glutamate receptors after quantal release of transmitter. Neuron 13, 1385-1393.
54. Tarusawa E, Matsui K, Budisantoso T, Molnár E, Watanabe M, Matsui M, Fukazawa Y & Shigemoto R (2009). Input-specific intrasynaptic arrangements of ionotropic glutamate receptors and their impact on postsynaptic responses. J Neurosci 29, 12896-12908.
55. Taschenberger H, Leão RM, Rowland KC, Spirou GA & von Gersdorff H (2002). Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36, 1127-1143.
56. Tong G & Jahr CE (1994). Multivesicular release from excitatory synapses of cultured hippocampal neurons. Neuron 12, 51-59.
57. Triller A & Korn H (1982). Transmission at a central inhibitory synapse. III. Ultrastructure of physiologically identified and stained terminals. J Neurophysiol 48, 708-736.
58. Trommershäuser J, Marienhagen J & Zippelius A (1999). Stochastic model of central synapses: slow diffusion of transmitter interacting with spatially distributed receptors and transporters. J Theor Biol 198, 101-120.
59. Trussell LO, Zhang S & Raman IM (1993). Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10, 1185-1196.
60. Uteshev VV & Pennefather PS (1996). A mathematical description of miniature postsynaptic current generation at central nervous system synapses. Biophys J 71, 1256-1266.
61. Wadiche JI & Jahr CE (2001). Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32, 301-313.
62. Wahl LM, Pouzat C & Stratford KJ (1996). Monte Carlo simulation of fast excitatory synaptic transmission at a hippocampal synapse. J Neurophysiol 75, 597-608.
63. Wong AY, Graham BP, Billups B & Forsythe ID (2003). Distinguishing between presynaptic and postsynaptic mechanisms of short-term depression during action potential trains. J Neurosci 23, 4868-4877.
64. Yamashita T, Ishikawa T & Takahashi T (2003). Developmental increase in vesicular glutamate content does not cause saturation of AMPA receptors at the calyx of held synapse. J Neurosci 23, 3633-3638.
65. Yamashita T, Kanda T, Eguchi K & Takahashi T (2009). Vesicular glutamate filling and AMPA receptor occupancy at the calyx of Held synapse of immature rats. J Physiol 587, 2327-2339.
66. Zampighi GA & Fisher RS (1997). Polyhedral protein cages encase synaptic vesicles and participate in their attachment to the active zone. J Struct Biol 119, 347-359.
67. Zhao S, Studer D, Chai X, Graber W, Brose N, Nestel S, Young C, Rodriguez EP, Saetzler K & Frotscher M (2012). Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing. J Comp Neurol 520, 2340-2351.
68. Zheng K, Scimemi A & Rusakov DA (2008). Receptor actions of synaptically released glutamate: the role of transporters on the scale from nanometers to microns. Biophys J 95, 4584-4596.