Vesicle number does not predict postsynaptic measures of miniature synaptic activity frequency in cultured cortical neurons

Neuroscience

Volumn 98, Issue 1, 2000, Pages 1-7

  MacKenzie, P J ^a   Kenner, G S ^a   Prange, O ^a   Murphy, T H ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Electron microscopy; EPSC; NMDA; Quantal; Release; Ultrastructure

Indexed keywords

CALCIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; CALCIUM TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITE; FETUS; FETUS CELL; HYPOTHESIS; IMAGING; MEMBRANE CURRENT; MINIATURE ENDPLATE POTENTIAL; NERVE CELL CULTURE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; CALCIUM; CELLS, CULTURED; CEREBRAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIALS; FETUS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NEURONS; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC VESICLES;

EID: 0034128162     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(00)00089-0     Document Type: Article

References (50)

1. Alés E., Tabares L., Poyato J.M., Valero V., Lindau M., Alvarez de Toledo G. High calcium concentrations shift the mode of exocytosis to the kiss and run mechanism. Nat. Cell Biol. 1:1999;40-44.
2. Arancio O., Kandel E.R., Hawkins R.D. Activity-dependent long-term enhancement of transmitter release by presynaptic 3′,5′-cyclic GMP in cultured hippocampal neurons. Nature. 376:1995;74-80.
3. Atwood H.L., Karunanithi S., Georgiou J., Charlton M.P. Strength of synaptic transmission at neuromuscular junctions of crustaceans and insects in relation to calcium entry. Invert. Neurosci. 3:1997;81-87.
4. Bailey C.H., Kandel E.R. Structural changes accompanying memory storage. A. Rev. Physiol. 55:1993;397-426.
5. Bruns D., Jahn R. Real-time measurement of transmitter release from single synaptic vesicles. Nature. 377:1995;62-65.
6. Calverley R.K.S., Jones D.G. Contributions of dendritic spines and perforated synapses to synaptic plasticity. Brain. Res. Rev. 15:1990;215-249.
7. Cooper R.L., Marin L., Atwood H.L. Synaptic differentiation of a single motor neuron: conjoint definition of transmitter release, presynaptic calcium signals, and ultrastructure. J. Neurosci. 15:1995;4209-4222.
8. Desmond N.L., Levy W.B. Synaptic interface surface area increases with long-term potentiation in the hippocampal dentate gyrus. Brain. Res. 453:1988;308-314.
9. Dobrunz L.E., Stevens C.F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron. 18:1997;95-1008.
10. Dubin M.W. The inner plexiform layer of the vertebrate retina: a quantitative and comparative electron microscopic analysis. J. comp. Neurol. 140:1970;479-506.
11. Edwards F.A. Anatomy and electrophysiology of fast central synapses lead to a structural model for long-term potentiation. Physiol. Rev. 75:1995;759-787.
12. Engert F., Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature. 399:1999;66-70.
13. Fifkova E., Anderson C.L., Young S.J., van Harrevald A. Effect of anisomycin on stimulation-induced changes in dendritic spines of the dentate granule cells. J. Neurocytol. 11:1982;183-210.
14. Forti L., Bossi M., Bergamaschi A., Villa A., Malgaroli A. Loose-patch recordings of single quanta at individual hippocampal synapses. Nature. 388:1997;874-878.
15. Geppert M., Goda Y., Stevens C.F., Südhof T.C. The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature. 387:1997;810-814.
16. Goda Y., Südhof T.C. Calcium regulation of neurotransmitter release: reliably unreliable? Curr. Opin. Cell Biol. 9:1997;513-518.
17. Gomperts S.N., Rao A., Craig A.M., Malenka R.C., Nicoll R.A. Postsynaptically silent synapses in single neuron cultures. Neuron. 21:1998;1443-1451.
18. Greenough W.T., West R.W., DeVoogd T.J. Subsynaptic plate perforations: changes with age and experience in the rat. Science. 202:1978;1096-1098.
19. Harris K.M., Jensen F.E., Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J. Neurosci. 12:1992;2685-2705.
20. Heuser J.E., Reese T.S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57:1973;315-344.
21. Heuser J.E., Reese T.S., Dennis M.J., Jan Y., Jan L., Evans L. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J. Cell Biol. 81:1979;275-300.
22. Hosokawa T., Rusakov D.A., Bliss T.V.P., Fine A. 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.
23. Kondo S., Marty A. Differential effects of noradrenaline on evoked, spontaneous and miniature IPSCs in rat cerebellar stellate cells. J. Physiol. 509:1998;233-243.
24. Lisman J.E., Harris K.M. Quantal analysis and synaptic anatomy - integrating two views of hippocampal plasticity. Trends Neurosci. 16:1993;141-147.
25. 2+ imaging of CNS axons in culture indicates reliable coupling between single action potentials and distal functional release sites. Neuron. 16:1996;783-795.
26. Mackenzie P.J., Kenner G.S., Prange O., Shayan H., Umemiya M., Murphy T.H. Ultrastructural correlates of synaptic function in cultured cortical neurons. J. Neurosci. 19:1999;C13.
27. Maletic-Savatic M., Malinow R., Svoboda K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science. 283:1999;1923-1927.
28. Malgaroli A., Tsien R.W. Glutamate-induced long-term potentiation of the frequency of miniature synaptic currents in cultured hippocampal neurons. Nature. 357:1992;134-139.
29. 2+ responses. Nature. 354:1991;73-76.
30. Moser M.B., Trommald M., Egeland T., Andersen P. Spatial training in a complex environment and isolation alter the spine distribution differently in rat CA1 pyramidal cells. J. comp. Neurol. 380:1997;373-381.
31. Murphy T.H., Baraban J.M., Wier W.G., Blatter L.A. Visualization of quantal synaptic transmission by dendritic calcium imaging. Science. 263:1994;529-532.
32. Murphy T.H., Baraban J.M., Wier W.G. Mapping miniature synaptic currents to single synapses using calcium imaging reveals heterogeneity in postsynaptic output. Neuron. 15:1995;159-168.
33. Murthy V.N., Stevens C.F. Reversal of synaptic vesicle docking at central synapses. Nat. Neurosci. 2:1999;503-507.
34. Murthy V.N., Sejnowski T.J., Stevens C.F. Dynamics of dendritic calcium transients evoked by quantal release at excitatory hippocampal synapses. Proc. Natl. Acad. Sci. USA. 97:2000;901-906.
35. Papa M., Segal M. Morphological plasticity in dendritic spines of cultured hippocampal neurons. Neuroscience. 71:1996;1005-1011.
36. Pierce J.P., Lewin G.R. An ultrastructural size principle. Neuroscience. 58:1994;441-446.
37. Prange O., Murphy T.H. Correlation of miniature synaptic activity and evoked release probability in cultures of cortical neurons. J. Neurosci. 19:1999;6427-6438.
38. Rosenmund C., Stevens C.F. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron. 16:1996;1197-1207.
39. Rosenmund C., Stevens C.F. The rate of aldehyde fixation of the exocytotic machinery in cultured hippocampal synapses. J. Neurosci. Meth. 76:1997;1-5.
40. Rusakov D.A., Davies H.A., Harrison E., Diana G., Richter-Levin G., Bliss T.V.P., Stewart M.G. Ultrastructural synaptic correlates of spatial learning in rat hippocampus. Neurosci. 80:1997;69-77.
41. Schikorski T., Stevens C.F. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17:1997;5858-5867.
42. Shi S.-H., Hayashi Y., Petralia R.S., Zaman S.H., Wenthold R.J., Svoboda K., Malinow R. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science. 284:1999;1811-1816.
43. Sorra K.E., Harris K.M. Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1. J. Neurosci. 18:1998;658-671.
44. Trommald M., Jensen V., Andersen P. Analysis of dendritic spines in rat CA1 pyramidal cells intracellularly filled with a fluorescent dye. J. comp. Neurol. 353:1995;260-274.
45. Trommald M., Hüllenberg G. Dimensions and density of dendritic spines from rat dentate granule cells based on reconstructions from serial electron micrographs. J. comp. Neurol. 377:1997;15-28.
46. Trudeau L.E., Doyle R.T., Emery D.G., Haydon P.G. Calcium-independent activation of the secretory apparatus by ruthenium red in hippocampal neurons: a new tool to assess modulation of presynaptic function. J. Neurosci. 16:1996;46-54.
47. Umemiya M, Senda M., Murphy T.H. Behavior of NMDA and AMPA receptor mediated miniature excitatory synaptic currents at synapses identified by calcium imaging. J. Physiol. (Lond.). 521:1999;113-122.
48. Wang S., Prange O., Murphy T.H. Amplification of calcium signals at dendritic spines provides a method for CNS quantal analysis. Can. J. Pharmac. Physiol. 77:1999;651-659.
49. Wojtowicz J.M., Marin L., Atwood H.L. Activity-induced changes in synaptic release sites at the crayfish neuromuscular junction. J. Neurosci. 14:1994;3688-3703.
50. Zucker R.S. Exocytosis: a molecular and physiological perspective. Neuron. 17:1996;1049-1055.