Presynaptic calcium influx controls neurotransmitter release in part by regulating the effective size of the readily releasable pool

Journal of Neuroscience

Volumn 33, Issue 11, 2013, Pages 4625-4633

  Thanawala, Monica S ^a   Regehr, Wade G ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; SIMULATION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; BACLOFEN; BIOPHYSICS; CALCIUM; CALCIUM CHANNEL BLOCKERS; COMPUTER SIMULATION; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GABA ANTAGONISTS; GABA-B RECEPTOR AGONISTS; MALE; MICE; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; NEURONS; NEUROTRANSMITTER AGENTS; NICKEL; OMEGA-AGATOXIN IVA; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; PONS; PRESYNAPTIC TERMINALS; PROPANOLAMINES;

EID: 84874843974     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4031-12.2013     Document Type: Article

References (42)

1. Ariel P, Ryan TA (2010) Optical mapping of release properties in synapses. Front Neural Circuits 4, pii: 18. CrossRef Medline
2. Augustine GJ (2001) How does calcium trigger neurotransmitter release? Curr Opin Neurobiol 11:320-326. CrossRef Medline
3. Beaumont V, Llobet A, Lagnado L (2005) Expansion of calcium microdomains regulates fast exocytosis at a ribbon synapse. Proc Natl Acad Sci U S A 102:10700-10705. CrossRef Medline
4. Borst JG, Sakmann B (1996) Calcium influx and transmitter release in a fast CNS synapse. Nature 383:431-434. CrossRef Medline
5. Borst JG, Sakmann B (1999) Effect of changes in action potential shape on calcium currents and transmitter release in a calyx-type synapse of the rat auditory brainstem. Philos Trans R Soc Lond B Biol Sci 354:347-355. CrossRef Medline
6. Cooper RL, Winslow JL, Govind CK, Atwood HL (1996) Synaptic structural complexity as a factor enhancing probability of calcium-mediated transmitter release. J Neurophysiol 75:2451-2466. Medline
7. Cuttle MF, Tsujimoto T, Forsythe ID, Takahashi T (1998) Facilitation of the presynaptic calcium current at an auditory synapse in rat brainstem. J Physiol 512:723-729. CrossRef Medline
8. Dittman JS, Regehr WG (1998) Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18:6147-6162. Medline
9. Dodge FA Jr, Rahamimoff R (1967) Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol 193: 419-432. Medline
10. Elmqvist D, Quastel DM (1965) A quantitative study of end-plate potentials in isolated human muscle. J Physiol 178:505-529. Medline
11. Fogelson AL, Zucker RS (1985) Presynaptic calcium diffusion from various arrays of single channels. Implications for transmitter release and synaptic facilitation. Biophys J 48:1003-1017. CrossRef Medline
12. Forsythe ID, Tsujimoto T, Barnes-Davies M, Cuttle MF, Takahashi T (1998) Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20:797-807. CrossRef Medline
13. Iwasaki S, Takahashi T (1998) Developmental changes in calcium channel types mediating synaptic transmission in rat auditory brainstem. J Physiol 509:419-423. CrossRef Medline
14. Jenkinson DH (1957) The nature of the antagonism between calcium and magnesium ions at the neuromuscular junction. J Physiol 138:434-444. Medline
15. Kushmerick C, Renden R, von Gersdorff H (2006) Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment. J Neurosci 26:1366-1377. CrossRef Medline
16. Lou X, Korogod N, Brose N, Schneggenburger R (2008) Phorbol esters modulate spontaneous and Ca2+-evoked transmitter release via acting on both Munc13 and protein kinase C. J Neurosci 28:8257-8267. CrossRef Medline
17. Meinrenken CJ, Borst JG, Sakmann B (2002) Calcium secretion coupling at calyx of held governed by nonuniform channel-vesicle topography. J Neurosci 22:1648-1667. Medline
18. Mintz IM, Sabatini BL, Regehr WG (1995) Calcium control of transmitter release at a cerebellar synapse. Neuron 15:675-688. CrossRef Medline
19. Moulder KL, Mennerick S (2005) Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons. J Neurosci 25:3842-3850. CrossRef Medline
20. Pan B, Zucker RS (2009) A general model of synaptic transmission and short-term plasticity. Neuron 62:539-554. CrossRef Medline
21. Rizzoli SO, Betz WJ (2005) Synaptic vesicle pools. Nat Rev Neurosci 6:57-69. CrossRef Medline
22. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1207. CrossRef Medline
23. Sakaba T, Neher E (2001a) Calmodulin mediates rapid recruitment of fastreleasing synaptic vesicles at a calyx-type synapse. Neuron 32:1119-1131. CrossRef Medline
24. Sakaba T, Neher E (2001b) Quantitative relationship between transmitter release and calcium current at the calyx of held synapse. J Neurosci 21: 462-476. Medline
25. Schneggenburger R, Neher E (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889-893. CrossRef Medline
26. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23:399-409. CrossRef Medline
27. Schneider T, Wei X, Olcese R, Costantin JL, Neely A, Palade P, Perez-Reyes E, Qin N, Zhou J, Crawford GD. (1994) Molecular analysis and functional expression of the human type E neuronal Ca2+ channel alpha 1 subunit. Receptors Channels 2:255-270. Medline
28. Shahrezaei V, Delaney KR (2004) Consequences of molecular-level Ca2+ channel and synaptic vesicle colocalization for the Ca2+ microdomain and neurotransmitter exocytosis: a Monte Carlo study. Biophys J 87:2352-2364. CrossRef Medline
29. Simon SM, Llinás RR (1985) Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys J 48:485-498. CrossRef Medline
30. Smith SJ, Augustine GJ, Charlton MP (1985) Transmission at voltageclamped giant synapse of the squid: evidence for cooperativity of presynaptic calcium action. Proc Natl Acad Sci U S A 82:622-625. CrossRef Medline
31. Soong TW, Stea A, Hodson CD, Dubel SJ, Vincent SR, Snutch TP (1993) Structure and functional expression of a member of the low voltageactivated calcium channel family. Science 260:1133-1136. CrossRef Medline
32. Stevens CF, Wesseling JF (1998) Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 21:415-424. CrossRef Medline
33. Stevens CF, Williams JH (2007) Discharge of the readily releasable pool with action potentials at hippocampal synapses. J Neurophysiol 98:3221-3229. CrossRef Medline
34. Takahashi T, Kajikawa Y, Tsujimoto T (1998). G-Protein-coupled modulation of presynaptic calcium currents and transmitter release by a GABAB receptor. J Neurosci 18:3138-3146. Medline
35. Taschenberger H, Scheuss V, Neher E (2005) Release kinetics, quantal parameters and their modulation during short-term depression at a developing synapse in the rat CNS. J Physiol 568:513-537. CrossRef Medline
36. Wadel K, Neher E, Sakaba T (2007) The coupling between synaptic vesicles and Ca2+ channels determines fast neurotransmitter release. Neuron 53:563-575. CrossRef Medline
37. Wang LY, Kaczmarek LK (1998) High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394:384-388. CrossRef Medline
38. Wu LG, Saggau P (1994) Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. J Neurosci 14:5613-5622. Medline
39. Wu LG, Borst JG, Sakmann B (1998) R-type Ca2+ currents evoke transmitter release at a rat central synapse. Proc Natl Acad Sci U S A 95: 4720-4725. CrossRef Medline
40. 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. Medline
41. Zamponi GW, Bourinet E, Snutch TP (1996) Nickel block of a family of neuronal calcium channels: subtype-and subunit-dependent action at multiple sites. J Membr Biol 151:77-90. CrossRef Medline
42. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405. CrossRef Medline