Different correlations among physiological and morphological properties at single glutamatergic synapses in the rat hippocampus and the cerebellum

Synapse

Volumn 65, Issue 5, 2011, Pages 412-423

  Miyawaki, Hiroyuki ^a   Hirano, Tomoo ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Culture; Presynaptic varicosity; Quantal EPSC; Spine

Indexed keywords

FLUORESCENT DYE;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL STRUCTURE; CEREBELLUM; ELECTRODE; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; NERVE CELL CULTURE; NONHUMAN; PHYSIOLOGY; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PURKINJE CELL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION; VARICOSIS;

ANIMALS; CELLS, CULTURED; CEREBELLUM; EMBRYO, MAMMALIAN; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; NEURONS; PATCH-CLAMP TECHNIQUES; PREGNANCY; PRESYNAPTIC TERMINALS; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; SYNAPSES; TRANSFECTION;

EID: 79952225572     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20860     Document Type: Article

References (60)

1. Allen C, Stevens CF. 1994. An evaluation of causes for unreliability of synaptic transmission. Proc Natl Acad Sci USA 91: 10380-10383.
2. Andrasfalvy BK, Magee JC. 2001. Distance-dependent increase in AMPA receptor number in the dendrites of adult hippocampal CA1 pyramidal neurons. J Neurosci 21: 9151-9159.
3. 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.
4. Belmeguenai A, Botta P, Weber JT, Carta M, De Ruiter M, De Zeeuw CI, Valenzuela CF, Hansel C. 2008. Alcohol impairs long-term depression at the cerebellar parallel fiber-Purkinje cell synapse. J Neurophysiol 100: 3167-3174.
5. Brewer GJ, Torricelli JR, Evege EK, Price PJ. 1993. Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serum-free medium combination. J Neurosci Res 35: 567-576.
6. Chen G, Harata NC, Tsien RW. 2004. Paired-pulse depression of unitary quantal amplitude at single hippocampal synapses. Proc Natl Acad Sci USA 101: 1063-1068.
7. Christie JM, Jahr CE. 2006. Multivesicular release at Schaffer collateral-CA1 hippocampal synapses. J Neurosci 26: 210-216.
8. 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.
9. Denk W, Sugimori M, Llinas R. 1995. Two types of calcium response limited to single spines in cerebellar Purkinje cells. Proc Natl Acad Sci USA 92: 8279-8282.
10. Dobrunz LE, Stevens CF. 1997. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008.
11. Fedulova SA, Vasilyev DV, Isaeva EV, Romanyuk SG, Veselovsky NS. 1999. Possibility of multiquantal transmission at single inhibitory synapse in cultured rat hippocampal neurons. Neuroscience 92: 1217-1230.
12. Foster TC, McNaughton BL. 1991. Long-term enhancement of CA1 synaptic transmission is due to increased quantal size, not quantal content. Hippocampus 1: 79-91.
13. Foster KA, Crowley JJ, Regehr WG. 2005. The influence of multivesicular release and postsynaptic receptor saturation on transmission at granule cell to Purkinje cell synapses. J Neurosci 25: 11655-11665.
14. Furuya S, Makino A, Hirabayashi Y. 1998. An improved method for culturing cerebellar Purkinje cells with differentiated dendrites under a mixed monolayer setting. Brain Res Brain Res Protoc 3: 192-198.
15. Futai K, Kim MJ, Hashikawa T, Scheiffele P, Sheng M, Hayashi Y. 2007. Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Nat Neurosci 10: 186-195.
16. Gundappa-Sulur G, De Schutter E, Bower JM. 1999. Ascending granule cell axon: An important component of cerebellar cortical circuitry. J Comp Neurol 408: 580-596.
17. Harris KM, Landis DM. 1986. Membrane structure at synaptic junctions in area CA1 of the rat hippocampus. Neuroscience 19: 857-872.
18. Harris KM, Stevens JK. 1988. Dendritic spines of rat cerebellar Purkinje cells: Serial electron microscopy with reference to their biophysical characteristics. J Neurosci 8: 4455-4469.
19. Harris KM, Stevens JK. 1989. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: Serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9: 2982-2997.
20. Hirano T, Hagiwara S. 1988. Synaptic transmission between rat cerebellar granule and Purkinje cells in dissociated cell culture: Effects of excitatory-amino acid transmitter antagonists. Proc Natl Acad Sci USA 85: 934-938.
21. Hirano T, Kasono K. 1993. Spatial distribution of excitatory and inhibitory synapses on a Purkinje cell in a rat cerebellar culture. J Neurophysiol 70: 1316-1325.
22. Horikawa K, Takeichi M. 2001. Requirement of the juxtamembrane domain of the cadherin cytoplasmic tail for morphogenetic cell rearrangement during myotome development. J Cell Biol 155: 1297-1306.
23. Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y, Aizawa S, Mishina M. 1995. Impairment of motor coordination. Purkinje cell synapse formation, and cerebellar long-term depression in GluRδ2 mutant mice. Cell 81: 245-252.
24. Kawaguchi SY, Hirano T. 2006. Integrin α3β1 suppresses long-term potentiation at inhibitory synapses on the cerebellar Purkinje neuron. Mol Cell Neurosci 31: 416-426.
25. Kirischuk S, Veselovsky N, Grantyn R. 1999. Relationship between presynaptic calcium transients and postsynaptic currents at single gamma-aminobutyric acid (GABA)ergic boutons. Proc Natl Acad Sci USA 96: 7520-7525.
26. Kullmann DM, Nicoll RA. 1992. Long-term potentiation is associated with increases in quantal content and quantal amplitude. Nature 357: 240-244.
27. Kuroyanagi T, Yokoyama M, Hirano T. 2009. Postsynaptic glutamate receptor δ family contributes to presynaptic terminal differentiation and establishment of synaptic transmission. Proc Natl Acad Sci USA 106: 4912-4916.
28. Lee KJ, Kim H, Kim TS, Park SH, Rhyu IJ. 2004. Morphological analysis of spine shapes of Purkinje cell dendrites in the rat cerebellum using high-voltage electron microscopy. Neurosci Lett 359: 21-24.
29. Liao D, Jones A, Malinow R. 1992. Direct measurement of quantal changes underlying long-term potentiation in CA1 hippocampus. Neuron 9: 1089-1097.
30. Liu G. 2003. Presynaptic control of quantal size: Kinetic mechanisms and implications for synaptic transmission and plasticity. Curr Opin Neurobiol 13: 324-331.
31. Liu G, Tsien RW. 1995. Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 375: 404-408.
32. Magee JC, Cook EP. 2000. Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci 3: 895-903.
33. Martin LJ, Blackstone CD, Levey AI, Huganir RL, Price DL. 1993. AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53: 327-358.
34. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429: 761-766.
35. McAllister AK, Stevens CF. 2000. Nonsaturation of AMPA and NMDA receptors at hippocampal synapses. Proc Natl Acad Sci USA 97: 6173-6178.
36. Mizuno H, Hirano T, Tagawa Y. 2007. Evidence for activity-dependent cortical wiring: Formation of interhemispheric connections in neonatal mouse visual cortex requires projection neuron activity. J Neurosci 27: 6760-6770.
37. Mizuno H, Hirano T, Tagawa Y. 2010. Pre- and postsynaptic neuron activity supports the axon development of callosal projection neurons during different postnatal periods in the cerebral cortex. Eur J Neurosci 31: 410-424.
38. Murnick JG, Dube G, Krupa B, Liu G. 2002. High-resolution iontophoresis for single-synapse stimulation. J Neurosci Methods 116: 65-75.
39. Murphy TH, Baraban JM, Wier WG. 1995. Mapping miniature synaptic currents to single synapses using calcium imaging reveals heterogeneity in postsynaptic output. Neuron 15: 159-168.
40. Murthy VN, Sejnowski TJ, Stevens CF. 1997. Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18: 599-612.
41. Nicholson DA, Trana R, Katz Y, Kath WL, Spruston N, Geinisman Y. 2006. Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron 50: 431-442.
42. 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.
43. 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.
44. Okamoto K, Nagai T, Miyawaki A, Hayashi Y. 2004. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7: 1104-1112.
45. Redman S. 1990. Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol Rev 70: 165-198.
46. Schikorski T, Stevens CF. 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17: 5858-5867.
47. Sdrulla AD, Linden DJ. 2007. Double dissociation between long-term depression and dendritic spine morphology in cerebellar Purkinje cells. Nat Neurosci 10: 546-548.
48. Shi S, Hayashi Y, Esteban JA, Malinow R. 2001. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105: 331-343.
49. 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 548(Pt 1): 245-258.
50. Spruston N, Jaffe DB, Johnston D. 1994. Dendritic attenuation of synaptic potentials and currents: The role of passive membrane properties. Trends Neurosci 17: 161-166.
51. Stevens CF, Tsujimoto T. 1995. Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc Natl Acad Sci USA 92: 846-849.
52. Stevens CF, Williams JH. 2000. "Kiss and run" exocytosis at hippocampal synapses. Proc Natl Acad Sci USA 97: 12828-12833.
53. Stevens CF, Williams JH. 2007. Discharge of the readily releasable pool with action potentials at hippocampal synapses. J Neurophysiol 98: 3221-3229.
54. Stricker C, Field AC, Redman SJ. 1996. Statistical analysis of amplitude fluctuations in EPSCs evoked in rat CA1 pyramidal neurones in vitro. J Physiol 490(Pt 2): 419-441.
55. Takeuchi T, Miyazaki T, Watanabe M, Mori H, Sakimura K, Mishina M. 2005. Control of synaptic connection by glutamate receptor δ2 in the adult cerebellum. J Neurosci 25: 2146-2156.
56. 2+ requirements for cerebellar long-term synaptic depression: Role for a postsynaptic leaky integrator. Neuron 54: 787-800.
57. Tong G, Jahr CE. 1994. Multivesicular release from excitatory synapses of cultured hippocampal neurons. Neuron 12: 51-59.
58. Ward JH. 1963. Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58: 236-244.
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. Zhou Q, Homma KJ, Poo MM. 2004. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44: 749-757.