Direct enhancement of presynaptic calcium influx in presynaptic facilitation at Aplysia sensorimotor synapses

Molecular and Cellular Neuroscience

Volumn 41, Issue 2, 2009, Pages 247-257

  Leal, Karina ^a   Klein, Marc ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; SEROTONIN;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; APLYSIA; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL CULTURE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EVOKED RESPONSE; FLUORESCENCE; LEARNING; MODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; REFLEX; SENSITIZATION; SENSORIMOTOR FUNCTION; SENSORY NERVE CELL;

ACTION POTENTIALS; ANIMALS; APLYSIA; CALCIUM; CALCIUM CHANNEL BLOCKERS; CELLS, CULTURED; ELECTROPHYSIOLOGY; NITRENDIPINE; SENSORY RECEPTOR CELLS; SEROTONIN; SYNAPSES; SYNAPTIC POTENTIALS; SYNAPTIC TRANSMISSION;

APLYSIA;

EID: 67349195982     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2009.03.004     Document Type: Article

References (60)

1. Ahn S., Ginty D.D., and Linden D.J. A late phase of cerebellar long-term depression requires activation of CaMKIV and CREB. Neuron 23 (1999) 559-568
2. Armitage B.A., and Siegelbaum S.A. Presynaptic induction and expression of homosynaptic depression at Aplysia sensorimotor neuron synapses. J. Neurosci. 18 (1998) 8770-8779
3. Augustine G.J. Regulation of transmitter release at the squid giant synapse by presynaptic delayed rectifier potassium current. J. Physiol. 431 (1990) 343-364
4. Augustine G.J., and Charlton M.P. Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse. J. Physiol. 381 (1986) 619-640
5. Bailey C.H., Thompson E.B., Castellucci V.F., and Kandel E.R. Ultrastructure of the synapses of sensory neurons that mediate the gill-withdrawal reflex in Aplysia. J. Neurocytol. 8 (1979) 415-444
6. Baxter D.A., and Byrne J.H. Serotonergic modulation of two potassium currents in the pleural sensory neurons of Aplysia. J. Neurophysiol. 62 (1989) 665-679
7. Beique J.C., Chapin-Penick E.M., Mladenovic L., and Andrade R. Serotonergic facilitation of synaptic activity in the developing rat prefrontal cortex. J. Physiol. 556 (2004) 739-754
8. Blumenfeld H., Spira M.E., Kandel E.R., and Siegelbaum S.A. Facilitatory and inhibitory transmitters modulate calcium influx during action potentials in Aplysia sensory neurons. Neuron 5 (1990) 487-499
9. Borst J.G., and Sakmann B. Calcium influx and transmitter release in a fast CNS synapse. Nature 383 (1996) 431-434
10. Borst J.G., and Sakmann B. 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 (1999) 347-355
11. Boyle M.B., Klein M., Smith S.J., and Kandel E.R. Serotonin increases intracellular Ca2+ transients in voltage-clamped sensory neurons of Aplysia californica. Proc. Natl. Acad. Sci. U. S. A. 81 (1984) 7642-7646
12. Braha O., Dale N., Hochner B., Klein M., Abrams T.W., and Kandel E.R. Second messengers involved in the two processes of presynaptic facilitation that contribute to sensitization and dishabituation in Aplysia sensory neurons. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 2040-2044
13. Braha O., Edmonds B., Sacktor T., Kandel E.R., and Klein M. The contributions of protein kinase A and protein kinase C to the actions of 5-HT on the L-type Ca2+ current of the sensory neurons in Aplysia. J. Neurosci. 13 (1993) 1839-1851
14. Brette F., Lacampagne A., Salle L., Findlay I., and Le Guennec J.Y. Intracellular Cs+ activates the PKA pathway, revealing a fast, reversible, Ca2+-dependent inactivation of L-type Ca2+ current. Am. J. Physiol. Cell Physiol. 285 (2003) C310-C318
15. Byrne J.H., and Kandel E.R. Presynaptic facilitation revisited: state and time dependence. Review. J. Neurosci. 16 (1996) 425-435
16. Chen G., and van den Pol A.N. Presynaptic GABAB autoreceptor modulation of P/Q-type calcium channels and GABA release in rat suprachiasmatic nucleus neurons. J. Neurosci. 18 (1998) 1913-1922
17. Christie B.R., Eliot L.S., Ito K., Miyakawa H., and Johnston D. Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx. J. Neurophysiol. 73 (1995) 2553-2557
18. Coulson R.L., and Klein M. Rapid development of synaptic connections and plasticity between sensory neurons and motor neurons of Aplysia in cell culture: implications for learning and regulation of synaptic strength. J. Neurophysiol. 77 (1997) 2316-2327
19. Czesnik D., Nezlin L., Rabba J., Muller B., and Schild D. Noradrenergic modulation of calcium currents and synaptic transmission in the olfactory bulb of Xenopus laevis tadpoles. Eur. J. Neurosci. 13 (2001) 1093-1100
20. Deisseroth K., Bito H., and Tsien R.W. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16 (1996) 89-101
21. Dodge Jr. F.A., and Rahamimoff R. Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193 (1967) 419-432
22. Dunlap K., and Fischbach G.D. Neurotransmitters decrease the calcium component of sensory neurone action potentials. Nature 276 (1978) 837-839
23. Edmonds B., Klein M., Dale N., and Kandel E.R. Contributions of two types of calcium channels to synaptic transmission and plasticity. Science 250 (1990) 1142-1147
24. Eliot L.S., Kandel E.R., Siegelbaum S.A., and Blumenfeld H. Imaging terminals of Aplysia sensory neurons demonstrates role of enhanced Ca2+ influx in presynaptic facilitation. Nature 361 (1993) 634-637
25. Fedchyshyn M.J., and Wang L.Y. Developmental transformation of the release modality at the calyx of Held synapse. J. Neurosci. 25 (2005) 4131-4140
26. Fernandez-Chacon R., Konigstorfer A., Gerber S.H., Garcia J., Matos M.F., Stevens C.F., Brose N., Rizo J., Rosenmund C., and Sudhof T.C. Synaptotagmin I functions as a calcium regulator of release probability. Nature 410 (2001) 41-49
27. Fossier P., Baux G., and Tauc L. N- and P-type Ca2+ channels are involved in acetylcholine release at a neuroneuronal synapse: only the N-type channel is the target of neuromodulators. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 4771-4775
28. Ghirardi M., Braha O., Hochner B., Montarolo P.G., Kandel E.R., and Dale N. Roles of PKA and PKC in facilitation of evoked and spontaneous transmitter release at depressed and nondepressed synapses in Aplysia sensory neurons. Neuron 9 (1992) 479-489
29. Graef I.A., Mermelstein P.G., Stankunas K., Neilson J.R., Deisseroth K., Tsien R.W., and Crabtree G.R. L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons. Nature 401 (1999) 703-708
30. Hawkins R.D., Abrams T.W., Carew T.J., and Kandel E.R. A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science 219 (1983) 400-405
31. Haydon P.G., Henderson E., and Stanley E.F. Localization of individual calcium channels at the release face of a presynaptic nerve terminal. Neuron 13 (1994) 1275-1280
32. Hochner B., and Kandel E.R. Modulation of a transient K+ current in the pleural sensory neurons of Aplysia by serotonin and cAMP: implications for spike broadening. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 11476-11480
33. Huang C.C., Wang S.J., and Gean P.W. Selective enhancement of P-type calcium currents by isoproterenol in the rat amygdala. J. Neurosci. 18 (1998) 2276-2282
34. Huang Y.Y., and Kandel E.R. 5-Hydroxytryptamine induces a protein kinase A/mitogen-activated protein kinase-mediated and macromolecular synthesis-dependent late phase of long-term potentiation in the amygdala. J. Neurosci. 27 (2007) 3111-3119
35. Isaacson J.S. GABAB receptor-mediated modulation of presynaptic currents and excitatory transmission at a fast central synapse. J. Neurophysiol. 80 (1998) 1571-1576
36. Klein M. Differential cyclic AMP dependence of facilitation at Aplysia sensorimotor synapses as a function of prior stimulation: augmentation versus restoration of transmitter release. J. Neurosci. 13 (1993) 3793-3801
37. Klein M. Synaptic augmentation by 5-HT at rested Aplysia sensorimotor synapses: independence of action potential prolongation. Neuron 13 (1994) 159-166
38. Klein M., and Kandel E.R. Mechanism of calcium current modulation underlying presynaptic facilitation and behavioral sensitization in Aplysia. Proc. Natl. Acad. Sci. U. S. A. 77 (1980) 6912-6916
39. Lando L., and Zucker R.S. Ca2+ cooperativity in neurosecretion measured using photolabile Ca2+ chelators. J. Neurophysiol. 72 (1994) 825-830
40. Llinas R., Sugimori M., and Silver R.B. Microdomains of high calcium concentration in a presynaptic terminal. Science 256 (1992) 677-679
41. Marinesco S., and Carew T.J. Serotonin release evoked by tail nerve stimulation in the CNS of Aplysia: characterization and relationship to heterosynaptic plasticity. J. Neurosci. 22 (2002) 2299-2312
42. Mckernan M.G., and Shinnickgallagher P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390 (1997) 607-611
43. Nair S.G., and Gudelsky G.A. Activation of 5-HT2 receptors enhances the release of acetylcholine in the prefrontal cortex and hippocampus of the rat. Synapse 53 (2004) 202-207
44. Pisani A., Bonsi P., Catania M.V., Giuffrida R., Morari M., Marti M., Centonze D., Bernardi G., Kingston A.E., and Calabresi P. Metabotropic glutamate 2 receptors modulate synaptic inputs and calcium signals in striatal cholinergic interneurons. J. Neurosci. 22 (2002) 6176-6185
45. Robitaille R., Adler E.M., and Charlton M.P. Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses. Neuron 5 (1990) 773-779
46. Royer S., Coulson R.L., and Klein M. Switching off and on of synaptic sites at Aplysia sensorimotor synapses. J. Neurosci. 20 (2000) 626-638
47. Sakaba T., and Neher E. Quantitative relationship between transmitter release and calcium current at the calyx of Held synapse. J. Neurosci. 21 (2001) 462-476
48. Schacher S., Montarolo P., and Kandel E.R. Selective short- and long-term effects of serotonin, small cardioactive peptide, and tetanic stimulation on sensorimotor synapses of Aplysia in culture. J. Neurosci. 10 (1990) 3286-3294
49. Schacher S., and Proshansky E. Neurite regeneration by Aplysia neurons in dissociated cell culture: modulation by Aplysia hemolymph and the presence of the initial axonal segment. J. Neurosci. 3 (1983) 2403-2413
50. Shahrezaei V., Cao A., and Delaney K.R. Ca2+ from one or two channels controls fusion of a single vesicle at the frog neuromuscular junction. J. Neurosci. 26 (2006) 13240-13249
51. Sherff C.M., and Carew T.J. Coincident induction of long-term facilitation at sensory-motor synapses in Aplysia: presynaptic and postsynaptic factors. Neurobiol. Learn. Mem. 78 (2002) 498-507
52. Smith S.J., Buchanan J., Osses L.R., Charlton M.P., and Augustine G.J. The spatial distribution of calcium signals in squid presynaptic terminals. J. Physiol. 472 (1993) 573-593
53. Spafford J.D., Munno D.W., Van Nierop P., Feng Z.P., Jarvis S.E., Gallin W.J., Smit A.B., Zamponi G.W., and Syed N.I. Calcium channel structural determinants of synaptic transmission between identified invertebrate neurons. J. Biol. Chem. 278 (2003) 4258-4267
54. Stanley E.F. Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 11 (1993) 1007-1011
55. Sun Z.Y., Kauderer B., and Schacher S. Differential distribution of functional receptors for neuromodulators evoking short-term heterosynaptic plasticity in Aplysia sensory neurons. J. Neurosci. 16 (1996) 7540-7549
56. Vargas G., Yeh T.Y., Blumenthal D.K., and Lucero M.T. Common components of patch-clamp internal recording solutions can significantly affect protein kinase A activity. Brain Res. 828 (1999) 169-173
57. Wang B.W., Liao W.N., Chang C.T., and Wang S.J. Facilitation of glutamate release by nicotine involves the activation of a Ca2+/calmodulin signaling pathway in rat prefrontal cortex nerve terminals. Synapse 59 (2006) 491-501
58. Westenbroek R.E., Hoskins L., and Catterall W.A. Localization of Ca2+ channel subtypes on rat spinal motor neurons, interneurons, and nerve terminals. J. Neurosci. 18 (1998) 6319-6330
59. Williams G.V., Rao S.G., and Goldman-Rakic P.S. The physiological role of 5-HT2A receptors in working memory. J. Neurosci. 22 (2002) 2843-2854
60. Wu L.G., and Saggau P. Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci. 20 (1997) 204-212