Release probability-dependent scaling of the postsynaptic responses at single hippocampal GABAergic synapses

Journal of Neuroscience

Volumn 26, Issue 48, 2006, Pages 12487-12496

  Biró, Ágota A ^a   Holderith, Noémi B ^a   Nusser, Zoltan ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Electron microscopy; Hippocampus; Interneurons; Paired recordings; Patch clamp; Quantal analysis

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 AMINOBUTYRIC ACID RECEPTOR; CANNABINOID RECEPTOR; CANNABINOID RECEPTOR AGONIST; CHOLECYSTOKININ;

ANIMAL EXPERIMENT; ARTICLE; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; COMPUTER SIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; MALE; MODELS, NEUROLOGICAL; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 33845276562     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3106-06.2006     Document Type: Article

References (48)

1. Abbott LF, Regehr WG (2004) Synaptic computation. Nature 431:796-803.
2. Auger C, Marty A (1997) Heterogeneity of functional synaptic parameters among single release sites. Neuron 19:139-150.
3. Auger C, Marty A (2000) Quantal currents at single-site central synapses. J Physiol (Lond) 526:3-11.
4. 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.
5. Bergles DE, Diamond JS, Jahr CE (1999) Clearance of glutamate inside the synapse and beyond. Curr Opin Neurobiol 9:293-298.
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. Choi S, Klingauf J, Tsien RW (2000) Postfusional regulation of cleft glutamate concentration during LTP at "silent synapses." Nat Neurosci 3:330-336.
8. Christie JM, Jahr CE (2006) Multivesicular release at Schaffer collateral-CA1 hippocampal synapses. J Neurosci 26:210-216.
9. Conti R, Lisman J (2003) The high variance of AMPA receptor- and NMDA receptor-mediated responses at single hippocampal synapses: evidence for multiquantal release. Proc Natl Acad Sci USA 100:4885-4890.
10. Foster KA, Kreitzer AC, Regehr WG (2002) Interaction of postsynaptic receptor saturation with presynaptic mechanisms produces a reliable synapse. Neuron 36:1115-1126.
11. Frerking M, Wilson M (1996) Saturation of postsynaptic receptors at central synapses? Curr Opin Neurobiol 6:395-403.
12. Frerking M, Borges S, Wilson M (1995) Variation in GABA mini amplitude is the consequence of variation in transmitter concentration. Neuron 15:885-895.
13. Gulyas AI, Miles R, Sik A, Toth K, Tamamaki N, Freund TF (1993) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-687.
14. A receptor currents in mouse fibroblasts. J Physiol (Lond) 514:27-45.
15. A receptor occupancy. Eur J Neurosci 12:810-818.
16. Hanse E, Gustafsson B (2001) Quantal variability at glutamatergic synapses in area CA1 of the rat neonatal hippocampus. J Physiol (Lond) 531:467-480.
17. Harrison J, Jahr CE (2003) Receptor occupancy limits synaptic depression at climbing fiber synapses. J Neurosci 23:377-383.
18. A channel responses to brief agonist pulses. Neuron 15:181-191.
19. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K, Freund TF (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:4544-4558.
20. 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.
21. Korn H, Mallet A, Triller A, Faber DS (1982) Transmission at a central inhibitory synapse. II. quantal description of release, with a physical correlate for binomial n. J Neurophysiol 48:679-707.
22. Korn H, Sur C, Charpier S, Legendre P, Faber DS (1994) The one-vesicle hypothesis and multivesicular release. New York: Raven.
23. Lawrence JJ, Grinspan ZM, McBain CJ (2004) Quantal transmission at mossy fibre targets in the CA3 region of the rat hippocampus. J Physiol (Lond) 554:175-193.
24. Liu GS (2003) Presynaptic control of quantal size: kinetic mechanisms for synaptic transmission and plasticity. Curr Opin Neurobiol 13:324-331.
25. Losonczy A, Biró AA, Nusser Z (2004) Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons. Proc Natl Acad Sci USA 101:1362-1367.
26. A receptors. J Neurosci 19:2474-2488.
27. 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.
28. Nusser Z (2002) Release-independent short-term facilitation at GABAergic synapses in the olfactory bulb. Neuropharmacology 43:573-583.
29. A receptor number underlie variation in GABA mini amplitude. Neuron 19:697-709.
30. A receptors in synapses of hippocampal pyramidal cells of the rat. Eur J Neurosci 13:428-442.
31. Oertner TG, Sabatini BL, Nimchinsky EA, Svoboda K (2002) Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 5:657-964.
32. Overstreet LS, Westbrook GL, Jones M V (2002) Measuring and modeling the spatiotemporal profile of GABA at the synapse. In: Transmembrane transporters (Quick MW, ed), pp 259-275. Hoboken, NJ: Wiley-Liss.
33. Perrais D, Ropert N (1999) Effect of zolpidem on miniature IPSCs and occupancy of postsynaptic GABAA receptors in central synapses. J Neurosci 19:578-588.
34. Perrais D, Ropert N (2000) Altering the concentration of GABA in the synaptic cleft potentiates miniature IPSCs in rat occipital cortex. Eur J Neurosci 12:400-404.
35. Reid CA, Clements JD (1999) Postsynaptic expression of long-term potentiation in the rat dentate gyrus demonstrated by variance-mean analysis. J Physiol (Lond) 518:121-130.
36. Saviane C, Silver RA (2006) Errors in the estimation of the variance: implications for multiple probability fluctuation analysis. J Neurosci Methods 153:250-260.
37. 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.
38. Scheuss V, Neher E (2001) Estimating synaptic parameters from mean, variance, and covariance in trains of synaptic responses. Biophys J 81:1970-1989.
39. Scheuss V, Schneggenburger R, Neher E (2002) Separation of presynaptic and postsynaptic contributions to depression by covariance analysis of successive EPSCs at the calyx of held synapse. J Neurosci 22:728-739.
40. Silver RA (2003) Estimation of nonuniform quantal parameters with multiple-probability fluctuation analysis: theory, application and limitations. J Neurosci Methods 130:127-141.
41. 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.
42. Silver RA, Momiyama A, Cull-Candy SG (1998) Locus of frequency-dependent depression identified with multiple- probability fluctuation analysis at rat climbing fibre-Purkinje cell synapses. J Physiol (Lond) 510:881-902.
43. Silver RA, Lubke J, Sakmann B, Feldmeyer D (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302:1981-1984.
44. Sloviter RS, Ali-Akbarian L, Horvath KD, Menkens KA (2001) Substance P receptor expression by inhibitory interneurons of the rat hippocampus: enhanced detection using improved immunocytochemical methods for the preservation and colocalization of GABA and other neuronal markers. J Comp Neurol 430:283-305.
45. Tong G, Jahr CE (1994) Multivesicular release from excitatory synapses of cultured hippocampal neurons. Neuron 12:51-59.
46. Wadiche JI, Jahr CE (2001) Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32:301-313.
47. Watanabe J, Rozov A, Wollmuth LP (2005) Target-specific regulation of synaptic amplitudes in the neocortex. J Neurosci 25:1024-1033.
48. Zador AM, Dobrunz LE (1997) Dynamic synapses in the cortex. Neuron 19:1-4.