Short-term plasticity constrains spatial organization of a hippocampal presynaptic terminal

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 36, 2012, Pages 14657-14662

  Nadkarni, Suhita ^a,b   Bartol, Thomas M ^a,b   Stevens, Charles F ^b   Sejnowski, Terrence J ^a,b,c   Levine, Herbert ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

MCell; Paired pulse facilitation; Synaptic depression; Vesicle

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; NEUROTRANSMITTER; CALCIUM;

ACTION POTENTIAL; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; IN VITRO STUDY; NERVE CELL PLASTICITY; NERVE ENDING; NEUROTRANSMITTER RELEASE; POST TETANIC POTENTIATION; PRIORITY JOURNAL; SYNAPSE; BIOLOGICAL MODEL; BIOPHYSICS; COMPUTER SIMULATION; CYTOLOGY; HUMAN; METABOLISM; PHYSIOLOGY; SYNAPTOSOME; ULTRASTRUCTURE;

BIOPHYSICS; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; CALCIUM; CALCIUM CHANNELS; COMPUTER SIMULATION; HUMANS; MODELS, BIOLOGICAL; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS;

EID: 84871002619     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1211971109     Document Type: Article

References (47)

1. Katz B, Miledi R (1970) Further study of the role of calcium in synaptic transmission. J Physiol 207:789–801.
2. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355–405.
3. Lisman JE, Raghavachari S, Tsien RW (2007) The sequence of events that underlie quantal transmission at central glutamatergic synapses. Nat Rev Neurosci 8:597–609.
4. Augustine GJ, Santamaria F, Tanaka K (2003) Local calcium signaling in neurons. Neuron 40:331–346.
5. Stanley EF (1997) The calcium channel and the organization of the presynaptic transmitter release face. Trends Neurosci 20:404–409.
6. Brandt A, Khimich D, Moser T (2005) Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 25:11577–11585.
7. Shahrezaei V, Cao A, Delaney KR (2006) Ca2+ from one or two channels controls fusion of a single vesicle at the frog neuromuscular junction. J Neurosci 26: 13240–13249.
8. Bucurenciu I, Bischofberger J, Jonas P (2010) A small number of open Ca2+ channels trigger transmitter release at a central GABAergic synapse. Nat Neurosci 13:19–21.
9. Mintz IM, Sabatini BL, Regehr WG (1995) Calcium control of transmitter release at a cerebellar synapse. Neuron 15:675–688.
10. Borst JG, Sakmann B (1996) Calcium influx and transmitter release in a fast CNS synapse. Nature 383:431–434.
11. Wu LG, Westenbroek RE, Borst JG, Catterall WA, Sakmann B (1999) Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses. J Neurosci 19:726–736.
12. Bucurenciu I, Kulik A, Schwaller B, Frotscher M, Jonas P (2008) Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 57:536–545.
13. Eggermann E, Bucurenciu I, Goswami SP, Jonas P (2012) Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses. Nat Rev Neurosci 13:7–21.
14. Nadkarni S, Bartol TM, Sejnowski TJ, Levine H (2010) Modelling vesicular release at hippocampal synapses. PLOS Comput Biol 6:e1000983.
15. Coggan JS, et al. (2005) Evidence for ectopic neurotransmission at a neuronal synapse. Science 309:446–451.
16. 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.
17. Bertram R, Sherman A, Stanley EF (1996) Single-domain/bound calcium hypothesis of transmitter release and facilitation. J Neurophysiol 75:1919–1931.
18. Murthy VN, Sejnowski TJ, Stevens CF (1997) Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18:599–612.
19. Koester HJ, Sakmann B (2000) Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. J Physiol 529:625–646.
20. Goda Y, Stevens CF (1994) Two components of transmitter release at a central synapse. Proc Natl Acad Sci USA 91:12942–12946.
21. Stevens CF, Sullivan JM (2003) The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron 39:299–308.
22. Sun J, et al. (2007) A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 450:676–682.
23. Nagy G, Kim J, Pang Z, Matti U (2006) Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J Neurosci 26:632–643.
24. Xu J, Mashimo T, Südhof TC (2007) Synaptotagmin-1, -2, and -9: Ca(2+) sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54:567–581.
25. Modchang C, et al. (2010) A comparison of deterministic and stochastic simulations of neuronal vesicle release models. Phys Biol 7:026008.
26. Allbritton NL, Meyer T, Stryer L (1992) Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258:1812–1815.
27. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18:995–1008.
28. Pfister J-P, Dayan P, Lengyel M (2010) Synapses with short-term plasticity are optimal estimators of presynaptic membrane potentials. Nat Neurosci 13:1271–1275.
29. Dobrunz LE, Huang EP, Stevens CF (1997) Very short-term plasticity in hippocampal synapses. Proc Natl Acad Sci USA 94:14843–14847.
30. Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673–682.
31. Edelman GM, Gall WE, Cowan WM; Neurosciences Institute (1987) Synaptic Function (Wiley, New York).
32. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197–1207.
33. Thomson AM (2000) Facilitation, augmentation and potentiation at central synapses. Trends Neurosci 23:305–312.
34. Kraushaar U, Jonas P (2000) Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20:5594–5607.
35. Chen Y, Chad JE, Wheal HV (1996) Synaptic release rather than failure in the conditioning pulse results in paired-pulse facilitation during minimal synaptic stimulation in the rat hippocampal CA1 neurones. Neurosci Lett 218:204–208.
36. Hanse E, Gustafsson B (2002) Release dependence to a paired stimulus at a synaptic release site with a small variable pool of immediately releasable vesicles. J Neurosci 22:4381–4387.
37. Hjelmstad GO, Nicoll RA, Malenka RC (1997) Synaptic refractory period provides a measure of probability of release in the hippocampus. Neuron 19:1309–1318.
38. Isaac JT, Hjelmstad GO, Nicoll RA, Malenka RC (1996) Long-term potentiation at single fiber inputs to hippocampal CA1 pyramidal cells. Proc Natl Acad Sci USA 93:8710–8715.
39. Stevens CF, Wang Y (1994) Changes in reliability of synaptic function as a mechanism for plasticity. Nature 371:704–707.
40. Volynski KE, Rusakov DA, Kullmann DM (2006) Presynaptic fluctuations and release-independent depression. Nat Neurosci 9:1091–1093.
41. Thomson AM, Bannister AP (1999) Release-independent depression at pyramidal inputs onto specific cell targets: Dual recordings in slices of rat cortex. J Physiol 519:57–70.
42. Zhang C, et al. (2009) Presenilins are essential for regulating neurotransmitter release. Nature 460:632–636.
43. Ribrault C, Sekimoto K, Triller A (2011) From the stochasticity of molecular processes to the variability of synaptic transmission. Nat Rev Neurosci 12:375–387.
44. Kerr RA, et al. (2008) Fast Monte Carlo simulation methods for biological reaction-diffusion systems in solution and on surfaces. SIAM J Sci Comput 30:3126.
45. Dodge FA, Jr., Rahamimoff R (1967) Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol 193:419–432.
46. Otsu Y, Murphy TH (2003) Miniature transmitter release: Accident of nature or careful design? Sci STKE 2003:pe54.
47. Reid CA, Bekkers JM, Clements JD (2003) Presynaptic Ca2+ channels: A functional patchwork. Trends Neurosci 26:683–687.