Multivesicular release at Schaffer collateral-CA1 hippocampal synapses

Journal of Neuroscience

Volumn 26, Issue 1, 2006, Pages 210-216

  Christie, Jason M ^a   Jahr, Craig E ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

AMPA receptor; EPSC; Glutamate spillover; Glutamate transporters; NMDA receptor; Synaptic vesicle release

Indexed keywords

AMPA RECEPTOR; GAMMA DEXTRO GLUTAMYLGLYCINE; GLUTAMATE TRANSPORTER; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; NEUROTRANSMITTER;

ANIMAL CELL; ARTICLE; BRAIN REGION; BRAIN SLICE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; NEUROTRANSMITTER RELEASE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE;

ACTION POTENTIALS; ANIMALS; EXCITATORY AMINO ACID ANTAGONISTS; GLUTAMIC ACID; HIPPOCAMPUS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; SYNAPTIC VESICLES;

EID: 30744473485     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4307-05.2006     Document Type: Article

References (61)

1. Arnth-Jensen N, Jabaudon D, Scanziani M (2002) Cooperation between independent hippocampal synapses is controlled by glutamate uptake. Nat Neurosci 5:325-331.
2. Asztely F, Erdemli G, Kullmann D (1997) Extrasynaptic glutamate spillover in the hippocampus: the role of active glutamate uptake. Neuron 18:281-293.
3. 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.
4. Barbour B, Häusser M (1997) Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20:377-384.
5. Bergles DE, Jahr CE (1997) Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19:1297-1308.
6. Bergles DE, Jahr CE (1998) Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J Neurosci 18:7709-7716.
7. Biró ÁA, Holderith N, Nusser Z (2005) Quantal size is independent of the release probability at hippocampal excitatory synapses. J Neurosci 25:223-232.
8. Blitz D, Foster KA, Regehr WG (2004) Short-term synaptic plasticity: a comparison of two synapses. Nat Rev Neurosci 5:630-640.
9. Choi S, Klingauf J, Tsien RW (2000) Postfusional regulation of cleft glutamate concentration during LTP at "silent synapses." Nat Neurosci 3:330-336.
10. 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.
11. Clements JD, Lester RA, Tong G, Jahr CE, Westbrook GL (1992) The time course of glutamate in the synaptic cleft. Science 258:1498-1501.
12. Conti R, Lisman J (2003) The high variance of AMPA receptor- and NMDA receptor-mediated responses at single hippocampal synapses: evidence for multiquantal release. Pro Natl Acad Sci USA 100:4885-4890.
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 (2000) Synaptically released glutamate does not overwhelm transporters on hippocampal astrocytes during high-frequency stimulation. J Neurophysiol 83:2835-2843.
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. Dobrunz LE, Huang EP, Stevens CF (1997) Very short-term plasticity in hippocampal synapses. Proc Natl Acad Sci USA 94:1483-1487.
17. Foster KA, Kreitzer AC, Regehr WG (2002) Interaction of postsynaptic receptor saturation with presynaptic mechanisms produces a reliable synapse. Neuron 35:1115-1126.
18. Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5:147-154.
19. Gulyás AI, Miles R, Sik A, Toth N, Tamamaki N, Freund TF (1993) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-687.
20. Hanse E, Gustafsson B (2001) Factors explaining heterogeneity in shortterm synaptic dynamics of hippocampal glutamatergic synapses in the neonatal rat. J Physiol (Lond) 537:141-149.
21. Harlow ML, Ress D, Stoschek A, Marshall RA, McMahan UJ (2001) The architecture of active zone material at the frog's neuromuscular junction. Nature 409:479-484.
22. Harris KM, Stevens JK (1989) Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9:2982-2997.
23. Hestrin S, Sah P, Nicoll RA (1990) Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5:247-253.
24. Hjelmstad GO, Nicoll RA, Malenka RC (1997) Synaptic refractory period provides a measure of probability of release in the hippocampus. Neuron 19:1309-1318.
25. Jahn R, Lang T, Südhof TC (2003) Membrane fusion. Cell 112:519-533.
26. Korn H, Triller A, Mallet A, Faber DS (1981) Fluctuating responses at a central synapse: n of binomial fit predicts number of stained presynaptic boutons. Science 213:898-901.
27. Korn H, Mallet A, Trilller A, Faber DS (1982) Transmission at a central inhibitory synapse. II. Quantal description of release, with a physical correlate for binomial n. J Neurophysiol 48:697-707.
28. Lawrence JJ, Grinspan ZM, McBain CJ (2003) Quantal transmission at mossy fibre targets in the CA3 region of the rat hippocampus. J Physiol (Lond) 554:175-193.
29. Lehre KP, Danbolt NC (1998) The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 18:8751-8757.
30. Lenzi D, Runyeon JW, Crum J, Ellisman MH, Roberts WM (1999) Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. J Neurosci 19:119-132.
31. 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.
32. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
33. Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
34. 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.
35. Nielsen TA, DiGregorio DA, Silver RA (2004) Modulation of glutamate mobility reveals mechanism of underlying slow-rising AMPA EPSCs and the diffusion coefficient in the synaptic cleft. Neuron 42:757-771.
36. Oertner TG, Sabatini BL, Nimchinsky EA, Svoboda K (2002) Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 7:657-664.
37. Patneau DK, Mayer ML (1990) Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors. J Neurosci 10:2385-2399.
38. Raghavachari S, Lisman JE (2004) Properties of quantal transmission at CA1 synapses. J Neurophysiol 92:2456-2467.
39. Redman SJ, Walmsley B (1983) Amplitude fluctuations in synaptic potentials evoked in cat spinal motoneurons at identified group 1a synapses. J Physiol (Lond) 343:135-145.
40. Renger JJ, Egles C, Liu G (2001) A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation. Neuron 29:469-484.
41. Rusakov DA, Kullmann DM (1998) Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J Neurosci 18:3158-3170.
42. Sarantis M, Ballerini L, Miller B, Silver RA, Edwards M, Attwell D (1993) Glutamate uptake from the synaptic cleft does not shape the decay of the non-NMDA component of the synaptic current. Neuron 11:541-549.
43. Sargent PB, Saviane C, Nielsen TA, DiGregorio DA, Silver RA (2005) Rapid vesicular release, quantal variability, and spillover contribute to the precision and reliability of transmission at a glomerular synapse. J Neurosci 25:8173-8187.
44. Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA (1997) Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385:630-634.
45. Schikorski T, Stevens CF (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17:5858-5867.
46. Schikorski T, Stevens CF (2001) Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4:391-395.
47. Schneggenburger R, Neher E (2005) Presynaptic calcium and control of vesicle fusion. Curr Opin Neurobiol 15:266-274.
48. Silver RA, Lübke J, Sakmann B, Feldmeyer D (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302:1981-1984.
49. Singer JH, Lassová L, Vardi N, Diamond JS (2004) Coordinated multivesicular release at a mammalian ribbon synapse. Nat Neurosci 8:826-833.
50. Stevens CF, Wang Y (1995) Facilitation and depression at single central synapses. Neuron 14:795-802.
51. Südhof T (2002) Synaptotagmins: why so many? J Biol Chem 277:7629-7632.
52. Takahashi M, Kovalchuk Y, Attwell D (1995) Presynaptic and postsynaptic determinants of EPSC waveform at cerebellar climbing fiber and parallel fiber to Purkinje cell synapses. J Neurosci 15:5693-5702.
53. Tong G, Jahr CE (1994) Multivesicular release from excitatory synapses of cultured hippocampal neurons. Neuron 12:51-59.
54. Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19:6897-6906.
55. Wadiche JI, Jahr CE (2001) Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32:301-313.
56. Watanabe J, Rozov A, Wollmuth LP (2005) Target-specific regulation of synaptic amplitudes in the neocortex. J Neurosci 25:1024-1033.
57. Watkins JC, Pook PCK, Sunter DC, Davies J, Honore T (1990) Experiments with kainite and quisqualate agonists and antagonists in relation to the sub-classification of "non-NMDA" receptors. Excitatory amino acids and neuronal plasticity. New York: Plenum.
58. Wu LG, Saggau P (1997) Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20:204-212.
59. Xu-Friedman MA, Harris KM, Regehr WG (2001) Three-dimensional comparison of ultrastructural characteristics at depressing and facilitating synapses onto cerebellar Purkinje cells. J Neurosci 21:6666-6672.
60. Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12:13-31.
61. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.