Development of short-term heterosynaptic facilitation at Aplysia sensorimotor synapses in vitro is accompanied by changes in the functional expression of presynaptic serotonin receptors

Journal of Neurophysiology

Volumn 76, Issue 4, 1996, Pages 2250-2261

  Sun, Zhong Yi ^a   Schacher, Samuel ^a  

^a New York State Psychiatric Institute ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYPROHEPTADINE; METITEPINE; PHORBOL ESTER; PRESYNAPTIC RECEPTOR; PROTEIN KINASE C; SEROTONIN; SEROTONIN RECEPTOR;

ANIMAL CELL; APLYSIA; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; FACILITATION; MOTOR NERVE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SYNAPSE; SYNAPTIC POTENTIAL;

EID: 0029907564     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.4.2250     Document Type: Article

References (62)

1. ANDERSON, M. J. AND COHEN, M. W.Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J. Physiol. Lond. 268: 757-773, 1977.
2. BACKSAI, B. J., HOCHNER, B., MAHAUT-SMITH, M., ADAMS, S. R., KAANG, B., KANDEL, E. R., AND TSIEN, R. Y. Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science Wash. DC 260: 222-226, 1993.
3. BAIRD, D. H., BAPTISTA, C. A., WANG, L. C., AND MASON, C. A. Specificity of a target-derived stop signal for afferent axon growth. J. Neurobiol. 23: 579-591, 1992.
4. BANK, M. AND SCHACHER, S. Segregation of presynaptic inputs on an identified target neuron in vitro: structural remodeling visualized over time. J. Neurosci. 12: 2960-2972, 1992.
5. BAXTER, D. A. AND BYRNE, J. H. Differential effects of cAMP and serotonin on membrane current, action potential duration, and excitability in somata of pleural sensory neurons of Aplysia. J. Neurophysiol. 64: 978-990, 1990.
6. BELARDETTI, F., SCHACHER, S., KANDEL, E. R., AND SIEGELBAUM, S. A. The growth cones of Aplysia sensory neurons: modulation by serotonin of action potential duration and single potassium channel currents. Proc. Natl. Acad. Sci. USA 83: 7094-7098, 1986.
7. BERNIER, L., CASTELLUCCI, V. F., KANDEL, E. R., AND SCHWARTZ, J. H. Facilitatory transmitter causes a selective and prolonged increase in cyclic AMP in sensory neurons mediating the gill and siphon withdrawal reflex in Aplysia. J. Neurosci. 2: 1682-1691, 1982.
8. 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. USA 87: 2040-2044, 1990.
9. BRUNELLI, M., CASTELLUCCI, V. F., AND KANDEL, E. R. Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science Wash. DC 194: 1178-1181, 1976.
10. BYRNE, J. Analysis of synaptic depression contributing to habituation of gill-withdrawal reflex in Aplysia californica. J. Neurophysiol. 48: 431-438, 1982.
11. BYRNE, J. AND KANDEL E. R. Presynaptic facilitation revisited: state and time dependence. J. Neurosci. 16: 425-435, 1996.
12. CASTELLUCCI, V. F. AND KANDEL, E. R. A quantal analysis of synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. Proc. Natl. Acad. Sci. USA 71: 5004-5008, 1974.
13. CASTELLUCCI, V. F. AND KANDEL, E. R. Presynaptic facilitation as a mechanism for behavioral sensitization in Aplysia. Science Wash. DC 194: 1176-1178, 1976.
14. CASTELLUCCI, V. F., KANDEL, E. R., SCHWARTZ, J. H., WILSON, A. C., NAIRN, A., AND GREENGARD, P. Intracellular injection of the catalytic subunit of cyclic AMP-dependent protein kinase stimulates facilitation of transmitter release underlying behavioral sensitization in Aplysia. Proc. Natl. Acad. Sci. USA 11: 7492-7496, 1980.
15. CASTELLUCCI, V. F., NAIRN, A. C., GREENGARD, P., SCHWARTZ, J. H., AND KANDEL, E. R. Inhibitor of cAMP-dependent protein kinase blocks presynaptic facilitation in Aplysia. J. Neurosci. 2: 1673-1681, 1982.
16. CASTELLUCCI, V. F., PINSKER, H., KUPFERMANN, I., AND KANDEL, E. R. Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science Wash. DC 167: 1745-1748, 1970.
17. CLARK, G. A. AND KANDEL, E. R. Branch-specific heterosynaptic faciltation in Aplysia siphon sensory cells. Proc. Natl. Acad. Sci. USA 81: 2577-2581, 1984.
18. CLARK, G. A. AND KANDEL, E. R. Induction of long-term facilitation in Aplysia sensory neurons by local application of serotonin to remote synapses. Proc. Natl. Acad. Sci. USA 90: 11411-11415, 1993.
19. DALE, N. AND KANDEL, E. R. Facilitatory and inhibitory transmitters modulate spontaneous transmitter release at cultured Aplysia sensorimotor synapses. J. Physiol. Lond. 421: 203-222, 1990.
20. EMPTAGE, N. J. AND CAREW, T. J. Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. Science Wash. DC 262: 253-256, 1993.
21. FRANK, E. AND FISCHBACH, G. D. Early events in neuromuscular junction formation in vitro: induction of acetylcholine receptor clusters in the postsynaptic membrane and morphology of newly formed synapses. J. Cell Biol. 83: 143-158, 1979.
22. 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: 1-20, 1992.
23. GINGRICH, K. J. AND BYRNE, J. H. Simulation of synaptic depression, posttetanic potentiation and presynaptic facilitation of synaptic potentials from sensory neurons mediating the gill withdrawal reflex in Aplysia. J. Neurophysiol. 53: 652-669, 1985.
24. GLANZMAN, D. L., KANDEL, E. R., AND SCHACHER, S. Identified target motor neuron regulates neurite outgrowth and synapse formation of Aplysia sensory neurons in vitro. Neuron 3: 441-450, 1989a.
25. GLANZMAN, D. L., MACKEY, S. L., HAWKINS, R. D., DYKE, A. M., LLOYD, P. E., AND KANDEL, E. R. Depletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock. J. Neurosci. 9: 4200-4213, 1989b.
26. GOLDSMITH, B. A. AND ABRAMS, T. W. Reversal of synaptic depression by serotonin at Aplysia sensory neuron synapses involves activation of adenylate cyclase. Proc. Natl. Acad. Sci. USA 88: 9021-9025, 1991.
27. GOODMAN, C. S. AND SHATZ, C. J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72/Neuron 10: 77-98, 1993.
28. HAWVER, D. B. AND SCHACHER, S. Selective fasciculation as a mechanism for the formation of specific chemical connections between Aplysia neurons in vitro. J. Neurobiol. 24: 368-383, 1993.
29. HOCHNER, B., KLEIN, M., SCHACHER, S., AND KANDEL, E. R. Action potential duration and the modulation of transmitter release from the sensory neurons of Aplysia in presynaptic facilitation. Proc. Natl. Acad. Sci. USA 83: 8410-8414, 1986a.
30. HOCHNER, B., KLEIN, M., SCHACHER, S., AND KANDEL, E. R. Additional components in the cellular mechanism of presynaptic facilitation contributes to behavioral dishabituation in Aplysia. Proc. Natl. Acad. Sci. USA 83: 8794-8798, 1986b.
31. JESSELL, T. M. AND KANDEL, E. R. Synaptic transmission: a bidirectional and self-modifiable form of cell-cell communication. Cell 72/Neuron 10: 1-30, 1993.
32. KANDEL, E. R. AND SCHWARTZ, J. H. Molecular biology of learning : modulation of transmitter release. Science Wash. DC 218: 433-443, 1982.
33. 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: 3793-3801, 1993.
34. KLEIN, M. Synaptic augmentation by 5-HT at rested Aplysia sensorimotor synapses: independence of action potential prolongation. Neuron 13: 159-166, 1994.
35. KLEIN, M., HOCHNER, B., AND KANDEL, E. R. Facilitatory transmitters and cAMP can modulate accommodation as well as transmitter release in Aplysia sensory neurons: evidence for parallel processing in a single cell. Proc. Natl. Acad. Sci. USA 83: 7994-7998, 1986.
36. KUPFERMANN, I., CASTELLUCCI, V. F., PINSKER, H., AND KANDEL, E. R. Neuronal correlates of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science Wash. DC 167: 1743-1745, 1970.
37. LI, X.-C., GIOT, J.-F., KUHL, D., HEN, R., AND KANDEL, E. R. Cloning and characterization of two related serotonergic receptors from the brain and the reproductive system of Aplysia that activate phospholipase C. J. Neurosci. 15: 7585-7591, 1995.
38. MACKEY, S. L., KANDEL, E. R., AND HAWKINS, R. D. Identified serotonergic neurons LCB1 and RCB1 in the cerebral ganglion of Aplysia produce presynaptic facilitation of siphon sensory neurons. J. Neuroci. 9: 4227-4235, 1989.
39. MARCUS, E. A., NOLEN, T. G., RANKIN, C. H., AND CAREW, T. J. Behavioral dissociation of dishabituation, sensitization, and inhibition in Aplysia. Science Wash. DC 241: 210-213, 1988.
40. MERCER, A. R., EMPTAGE, N. J., AND CAREW, T. J. Pharmacological dissociation of modulatory effects of serotonin in Aplysia sensory neurons. Science Wash DC 254: 1811-1813, 1991.
41. MERZ, D. C. AND DRAPEAU, P. Cell-specific contact selects transmitter responses in an identified leech neuron. Proc. Roy. Soc. Lond. B Biol. Sci. 248: 129-133, 1992.
42. MONTAROLO, P. G., GOELET, P., CASTELLUCCI, V. F., MORGAN, J., KANDEL, E. R., AND SCHACHER, S. A critical time window for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science Wash. DC 234: 1249-1254, 1986.
43. MONTAROLO, P. G., KANDEL, E. R., AND SCHACHER, S. Long-term heterosynaptic inhibition in Aplysia. Nature Lond. 333: 171-174, 1988.
44. NOLEN, T. G. AND CAREW, T. J. The cellular analog of sensitization in Aplysia emerges at the same time in development as behavioral sensitization. J. Neurosci. 8: 212-222, 1988.
45. NOLEN, T. G. AND CAREW, T. J. Ontogeny of serotonin-immunoreactive neurons in juvenile Aplysia California: implications for the development of learning. Behav. Neural Biol. 61: 282-295, 1994.
46. RANKIN, C. H. AND CAREW, T. J. Dishabituation and sensitization emerge as separate processes during development in Aplysia. J. Neurosci. 8: 197-211, 1988.
47. RAYPORT, S. G. AND SCHACHER, S. Synaptic plasticity in vitro: cell culture of identified Aplysia neurons mediating short-term habituation and sensitization. J. Neurosci. 6: 759-763, 1986.
48. SAKTOR, T. C. AND SCHWARTZ, J. H. Sensitizing stimuli cause translocation of protein kinase C in Aplysia sensory neurons. Proc. Natl. Acad. Sci. USA 87: 2036-2039, 1990.
49. SCHACHER, S., KANDEL, E. R., AND MONTAROLO, P. G. cAMP and arachidonic acid simulate long-term structural and functional changes produced by neurotransmitters in Aplysia sensory neurons. Neuron 10: 1079-1088, 1993.
50. SCHACHER, S. AND MONTAROLO, P. G. Target-dependent structural changes in sensory neurons of Aplysia accompany long-term heterosynaptic inhibition. Neuron 6: 679-690, 1991.
51. SCHACHER, S., MONTAROLO, P. G., 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: 3286-3294, 1990.
52. SCHOLZ, K. P. AND BYRNE, J. H. Intracellular injection of cAMP induces a long-term reduction of neuronal potassium currents. Science Wash. DC 240: 1664-1667, 1988.
53. SCHOTZINGER, R. J. AND LANDIS, S. C. Acquisition fo cholinergic and peptidergic properties by sympathetic innervation of rat sweat glands requires interaction with normal target. Neuron 5: 91-100, 1990.
54. SOSSIN, W. S. AND SCHWARTZ, J. H. Selective activation of calcium-activated PKCs in Aplysia neurons by 5-HT. J. Neurosci. 9: 3218-3229, 1992.
55. SUGITA, S., GOLDSMITH, J. R., BAXTER, D. A., AND BYRNE, J. H. Involvement of protein kinase C in serotonin-induced spike broadening and synaptic facilitation of sensorimotor connections in Aplysia. J. Neurophysiol. 68: 643-651, 1992.
56. SUN, Z.-Y. AND SCHACHER, S. Tetanic stimulation and cAMP regulate segregation of presynaptic inputs on a common postsynaptic target neuron in vitro. J. Neurobiol. 29: 183-201, 1996.
57. WALTERS, E. T. AND BYRNE, J. H. Posttetanic potentiation in Aplysia sensory neurons. Brain Res. 293: 377-380, 1984.
58. WU, F., FRIEDMAN, L., AND SCHACHER, S. Transient versus persistent functional and structural changes associated with facilitation of Aplysia sensorymotor synaspes are second messenger dependent. J. Neurosci. 15: 7517-7527, 1995.
59. YAMORI, T., FUKADA, K., AEBERSOLD, R., KORSCHING, S., FANN, M. J., AND PATTERSON, P. H. The cholinergic neuronal differentiating factor from heart cells is identical to leukemia inhibitory factor. Science Wash. DC 246: 1412-1416, 1989.
60. ZHU, H., WU, F., AND SCHACHER, S. Aplysia cell adhesion molecules and serotonin regulate sensory cell-motor cell interactions during early stages of synapse formation in vitro. J. Neurosci. 14: 6886-6900, 1994.
61. ZORAN, M. J., DOYLE, R. T., AND HAYDON, P. G. Target-dependent induction of secretory capabilities in an identified motoneuron during synaptogenesis. Dev. Biol. 138: 202-213, 1990.
62. ZORAN, M. J., DOYLE, R. T., AND HAYDON, P. G. Target contact regulates the calcium responsiveness of the secretory machinery during synaptogenesis. Neuron 6: 145-151, 1991.