The origin of quantal size variation: Vesicular glutamate concentration plays a significant role

Journal of Neuroscience

Volumn 27, Issue 11, 2007, Pages 3046-3052

  Wu, Xin Sheng ^a   Xue, Lei ^a   Mohan, Raja ^a   Paradiso, Kenneth ^a   Gillis, Kevin D ^b   Wu, Ling Gang ^a,c  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Capacitance; Glutamate; mEPSC; Quantal content; Synaptic; Transmission

Indexed keywords

AMPA RECEPTOR ANTAGONIST; GAMMA GLUTAMYLGLYCINE; GLUTAMIC ACID; POSTSYNAPTIC RECEPTOR; VESICULAR GLUTAMATE TRANSPORTER;

ARTICLE; DIALYSIS; ENDOCYTOSIS; EVOKED RESPONSE; MEMBRANE POTENTIAL; PRIORITY JOURNAL; QUANTITATIVE ASSAY; SYNAPTIC TRANSMISSION;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; RATS; RATS, WISTAR; SYNAPSES; SYNAPTIC VESICLES; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 33947317096     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4415-06.2007     Document Type: Article

References (52)

1. Bekkers JM, Richerson GB, Stevens CF (1990) Origin of variability in quantal size in cultured hippocampal-neurons and hippocampal slices. Proc Natl Acad Sci USA 87:5359-5362.
2. 2+ influx mediated by three different pathways during synaptic transmission at a calyx-type synapse. J Neuorsci 15:10409-10419.
3. Borst JGG, Helmchen F, Sakmann B (1995) Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J Physiol (Lond) 489:825-840.
4. Bruns D, Riedel D, Klingauf J, Jahn R (2000) Quantal release of serotonin. Neuron 28:205-220.
5. Carter AG, Regehr WG (2002) Quantal events shape cerebellar interneuron firing. Nat Neurosci 5:1309-1318.
6. 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.
7. Choi S, Klingauf J, Tsien RW (2003) Fusion pore modulation as a presynaptic mechanism contributing to expression of long-term potentiation. Philos Trans R Soc Lond B Biol Sci 358:695-705.
8. Colliver TL, Pyott SJ, Achalabun M, Ewing AG (2000) VMAT-mediated changes in quantal size and vesicular volume. J Neurosci 20:5276-5282.
9. Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, Krantz DE, DiAntonio A (2004) Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J Neurosci 24:10466-10474.
10. Fatt P, Katz B (1952) Spontaneous subthreshold activity at motor nerve endings. J Physiol (Lond) 117:109-128.
11. Franks KM, Stevens CF, Sejnowski TJ (2003) Independent sources of quantal variability at single glutamatergic synapses. J Neurosci 23:3186-3195.
12. Fremeau Jr RT, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304:1815-1819.
13. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15:193-204.
14. Gentet LJ, Stuart GJ, Clements JD (2000) Direct measurement of specific membrane capacitance in neurons. Biophys J 79:314-320.
15. Hausser M, Roth A (1997) Dendritic and somatic glutamate receptor channels in rat cerebellar Purkinje cells. J Physiol (Lond) 501:77-95.
16. He L, Wu XS, Mohan R, Wu LG (2006) Two modes of fusion pore opening revealed by cell-attached recordings at a synapse. Nature 444:102-105.
17. Ishikawa T, Sahara Y, Takahashi T (2002) A single packet of transmitter does not saturate postsynaptic glutamate receptors. Neuron 34:613-621.
18. Jonas P, Major G, Sakmann B (1993) Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J Physiol (Lond) 472:615-663.
19. Karunanithi S, Marin L, Wong K, Atwood HL (2002) Quantal size and variation determined by vesicle size in normal and mutant Drosophila glutamatergic synapses. J Neurosci 22:10267-10276.
20. Klyachko VA, Jackson MB (2002) Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 418:89-92.
21. Koike-Tani M, Saitoh N, Takahashi I (2005) Mechanisms underlying developmental speeding in AMPA-EPSC decay time at the calyx of Held. J Neurosci 25:199-207.
22. 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.
23. Lindau M, Alvarez de Toledo G (2003) The fusion pore. Biochim Biophys Acta 164:167-173.
24. Liu G (2003) Presynaptic control of quantal size: kinetic mechanisms and implications for synaptic transmission and plasticity. Curr Opin Neurobiol 13:324-331.
25. 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.
26. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
27. McKinney RA, Capogna M, Durr R, Gahwiler BH, Thompson SM (1999) Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 2:44-49.
28. 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.
29. 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.
30. Oleskevich S, Alvarez FJ, Walmsley B (1999) Glycinergic miniature synaptic currents and receptor cluster sizes differ between spinal cord interneurons. J Neurophysiol 82:312-319.
31. Otsu Y, Murphy TH (2003) Miniature transmitter release: accident of nature or careful design? Sci STKE 2003:e54.
32. Pawlu C, DiAntonio A, Heckmann M (2004) Postfusional control of quantal current shape. Neuron 42:607-618.
33. Pothos EN, Larsen KE, Krantz DE, Liu Y, Haycock JW, Setlik W, Gershon MD, Edwards RH, Sulzer D (2000) Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size. J Neurosci 20:7297-7306.
34. Sahara Y, Takahashi T (2001) Quantal components of the excitatory postsynaptic currents at a rat central auditory synapse. J Physiol (Lond) 536:189-197.
35. Sätzler K, Sohl L, Bollmann JH, Borst JGG, Frotscher M, Sakmann B, Lubke 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.
36. Schneggenburger R, Sakaba T, Neher E (2002) Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25:206-212.
37. Song HJ, Ming GL, Fon E, Bellocchio E, Edwards RH, Poo MM (1997) Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron 18:815-826.
38. Spruce AE, Breckenridge LJ, Lee AK, Almers W (1990) Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron 4:643-654.
39. Stiles JR, Van Helden D, Bartol Jr TM, Salpeter EE, Salpeter MM (1996) Miniature endplate current rise times less than 100 microseconds from improved dual recordings can be modeled with passive acetylcholine diffusion from a synaptic vesicle. Proc Natl Acad Sci USA 93:5747-5752.
40. Stiles JR, Bartol TB, Salpeter MM, Salpeter EE, Sejnowski TJ (2000) Synaptic variability. In: Synapses (Cowan TC, Sudhof TC, Stevens CF, eds), pp 681-732. Baltimore: The Johns Hopkins UP.
41. Sulzer D, Edwards R (2000) Vesicles: equal in neurotransmitter concentration but not in volume. Neuron 28:5-7.
42. Sun JY, Wu LG (2001) Fast kinetics of exocytosis revealed by simultaneous measurements of presynaptic capacitance and postsynatpic currents at a central synapse. Neuron 30:171-182.
43. Sun JY, Wu XS, Wu LG (2002) Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature 417:555-559.
44. Sun JY, Wu XS, Wu W, Jin SX, Dondzillo A, Wu LG (2004) Capacitance measurements at the calyx of Held in the medial nucleus of the trapezoid body. J Neurosci Methods 134:121-131.
45. Sutton MA, Wall NR, Aakalu GN, Schuman EM (2004) Regulation of dendritic protein synthesis by miniature synaptic events. Science 304:1979-1983.
46. Taschenberger H, Leao RM, Rowland KC, Spirou GA, Von Gersdorff H (2002) Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36:1127-1143.
47. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107.
48. Verhage M, Maia AS, Plomp JJ, Brussaard AB, Heeroma JH, Vermeer H, Toonen RF, Hammer RE, van den Berg TK, Missler M, Geuze HJ, Sudhof TC (2000) Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287:864-869.
49. Wilson NR, Kang J, Hueske EV, Leung T, Varoqui H, Murnick JG, Erickson JD, Liu G (2005) Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT1. J Neurosci 25:6221-6234.
50. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, Takamori S, Brose N, Rosenmund C (2004) An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci USA 101:7158-7163.
51. 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.
52. Zhang B, Koh YH, Beckstead RB, Budnik V, Ganetzky B, Bellen HJ (1998) Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21:1465-1475.