Number and density of AMPA receptors in single synapses in immature cerebellum

Journal of Neuroscience

Volumn 25, Issue 4, 2005, Pages 799-807

  Tanaka, Jun Ichi ^a,b   Matsuzaki, Masanori ^a,b   Tarusawa, Etsuko ^a,b   Momiyama, Akiko ^b   Molnar, Elek ^d   Kasai, Haruo ^a,b   Shigemoto, Ryuichi ^a,b,c  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

AMPA; Cerebellum; Freeze fracture; Glutamate; Postnatal; Purkinje cell; Receptor; Slice; Synapse; Ultrastructure

Indexed keywords

AMPA RECEPTOR; GLUTAMIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CEREBELLUM; CONTROLLED STUDY; NERVE CELL STIMULATION; NEUROBLAST; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PURKINJE CELL; RAT; RECEPTOR DENSITY; RECEPTOR UPREGULATION; SYNAPTIC TRANSMISSION;

ANIMALS; CEREBELLUM; EXCITATORY POSTSYNAPTIC POTENTIALS; FREEZE FRACTURING; GLUTAMATES; IMMUNOHISTOCHEMISTRY; INDOLES; KINETICS; PURKINJE CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SYNAPSES;

EID: 12844250540     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4256-04.2005     Document Type: Article

References (49)

1. Altman J, Bayer S (1997) Development of the cerebellar system. Boca Raton, FL: CRC.
2. Auger C, Marty A (1997) Heterogeneity of functional synaptic parameters among single release sites. Neuron 19:139-150.
3. Barbour B (2001) An evaluation of synapse independence. J Neurosci 21:7969-7984.
4. Barbour B, Keller BU, Llano I, Marty A (1994) Prolonged presence of glutamate during excitatory synaptic transmission to cerebellar Purkinje cells. Neuron 12:1331-1343.
5. Carroll RC, Beattie EC, von Zastrow M, Malenka RC (2001) Role of AMPA receptor endocytosis in synaptic plasticity. Nat Rev Neurosci 2:315-324.
6. Carter AG, Regehr WG (2000) Prolonged synaptic currents and glutamate spillover at the parallel fiber to stellate cell synapse. J Neurosci 20:4423-4434.
7. 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.
8. Dittman JS, Regehr WG (1997) Mechanism and kinetics of heterosynaptic depression at a cerebellar synapse. J Neurosci 17:9048-9059.
9. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18:995-1008.
10. Dzubay JA, Jahr CE (1999) The concentration of synaptically released glutamate outside of the climbing fiber-Purkinje cell synaptic cleft. J Neurosci 19:5265-5274.
11. Ellis RJ (2001) Macromolecular crowding: obvious but underappreciated. Trends Biochem Sci 26:597-604.
12. Franks KM, Bartol TM, Sejnowski TJ (2002) A Monte Carlo model reveals independent signaling at central glutamatergic synapses. Biophys J 83:2333-2348.
13. Franks KM, Stevens CF, Sejnowski TJ (2003) Independent sources of quantal variability at single glutamatergic synapses. J Neurosci 23:3186-3195.
14. Fujimoto K (1995) Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J Cell Sci 108:3443-3449.
15. Harris KM, Landis DM (1986) Membrane structure at synaptic junctions in area CA1 of the rat hippocampus. Neuroscience 19:857-872.
16. Hashimoto K, Kano M (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38:785-796.
17. Häusser M, Roth A (1997) Dendritic and somatic glutamate receptor channels in rat cerebellar Purkinje cells. J Physiol (Lond) 501:77-95.
18. Hopt A, Neher E (2001) Highly nonlinear photodamage in two-photon fluorescence microscopy. Biophys J 80:2029-2036.
19. Huang S, Heikal AA, Webb WW (2002) Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein. Biophys J 82:2811-2825.
20. Isaac JT, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434.
21. Ishikawa T, Sahara Y, Takahashi T (2002) A single packet of transmitter does not saturate postsynaptic glutamate receptors. Neuron 34:613-621.
22. Kiskin NI, Chillingworth R, McCray JA, Piston D, Ogden D (2002) The efficiency of two-photon photolysis of a "caged" fluorophore, O-1-(2-nitrophenyl)ethylpyranine, in relation to photodamage of synaptic terminals. Eur Biophys J 30:588-604.
23. 2+ fluorescence imaging with pico- and femtosecond two-photon excitation: signal and photodamage. Biophys J 77:2226-2236.
24. Kruk PJ, Korn H, Faber DS (1997) The effects of geometrical parameters on synaptic transmission: a Monte Carlo simulation study. Biophys J 73:2874-2890.
25. Lei S, Pelkey KA, Topolnik L, Congar P, Lacaille JC, McBain CJ (2003) Depolarization-induced long-term depression at hippocampal mossy fiber-CA3 pyramidal neuron synapses. J Neurosci 23:9786-9795.
26. Lim R, Alvarez FJ, Walmsley B (1999) Quantal size is correlated with receptor cluster area at glycinergic synapses in the rat brainstem. J Physiol (Lond) 516:505-512.
27. Linden DJ (2001) The expression of cerebellar LTD in culture is not associated with changes in AMPA-receptor kinetics, agonist affinity, or unitary conductance. Proc Natl Acad Sci USA 98:14066-14071.
28. Litschig S, Gasparini F, Rueegg D, Stoehr N, Flor PJ, Vranesic I, Prézeau L, Pin JP, Thomsen C, Kuhn R (1999) CPCCOEt, a noncompetitive metabotropic glutamate receptor 1 antagonist, inhibits receptor signaling without affecting glutamate binding. Mol Pharmacol 55:453-461.
29. Liu G (2003) Presynaptic control of quantal size: kinetic mechanisms and implications for synaptic transmission and plasticity. Curr Opin Neurobiol 13:324-331.
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. Lübke J (1993) Photoconversion of diaminobenzidine with different fluorescent neuronal markers into a light and electron microscopic dense reaction product. Microsc Res Tech 24:2-14.
32. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086-1092.
33. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
34. Momiyama A, Silver RA, Hausser M, Notomi T, Wu Y, Shigemoto R, Cull-Candy SG (2003) The density of AMPA receptors activated by a transmitter quantum at the climbing fibre-Purkinje cell synapse in immature rats. J Physiol (Lond) 549:75-92.
35. Nusser Z (1999) A new approach to estimate the number, density and variability of receptors at central synapses. Eur J Neurosci 11:745-752.
36. Nusser Z, Cull-Candy S, Farrant M (1997) Differences in synaptic GABA(A) receptor number underlie variation in GABA mini amplitude. Neuron 19:697-709.
37. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21:545-559.
38. Nusser Z, Naylor D, Mody I (2001) Synapse-specific contribution of the variation of transmitter concentration to the decay of inhibitory postsynaptic currents. Biophys J 80:1251-1261.
39. Otis TS, Wu YC, Trussell LO (1996) Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J Neurosci 16:1634-1644.
40. Partin KM, Fleck MW, Mayer ML (1996) AMPA receptor flip/flop mutants affecting deactivation, desensitization, and modulation by cyclothiazide, aniracetam, and thiocyanate. J Neurosci 16:6634-6647.
41. Pereda A, O'Brien J, Nagy JI, Bukauskas F, Davidson KG, Kamasawa N, Yasumura T, Rash JE (2003) Connexin35 mediates electrical transmission at mixed synapses on Mauthner cells. J Neurosci 23:7489-7503.
42. Rusakov DA, Kullmann DM (1998) Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J Neurosci 18:3158-3170.
43. Sigworth FJ (1980) The variance of sodium current fluctuations at the node of Ranvier. J Physiol (Lond) 307:97-129.
44. Silver RA (2003) Estimation of nonuniform quantal parameters with multiple-probability fluctuation analysis: theory, application and limitations. J Neurosci Methods 130:127-141.
45. Silver RA, Cull-Candy SG, Takahashi T (1996) Non-NMDA glutamate receptor occupancy and open probability at a rat cerebellar synapse with single and multiple release sites. J Physiol (Lond) 494:231-250.
46. Smith MA, Ellis-Davies GC, Magee JC (2003) Mechanism of the distance-dependent scaling of Schaffer collateral synapses in rat CA1 pyramidal neurons. J Physiol (Lond) 548:245-258.
47. Takumi Y, Ramírez-León V, Laake P, Rinvik E, Ottersen OP (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2:618-624.
48. Wadiche JI, Jahr CE (2001) Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32:301-313.
49. Xu C, Zipfel W, Shear JB, Williams RM, Webb WW (1996) Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy. Proc Natl Acad Sci USA 93:10763-10768.