Developmental dissociation of serotonin-induced spike broadening and synaptic facilitation in Aplysia sensory neurons

Journal of Neuroscience

Volumn 19, Issue 1, 1999, Pages 334-346

  Stark, Laura L ^a,b   Carew, Thomas J ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Developmental plasticity; Serotonin; Spike duration dependent facilitation; Spike duration independent facilitation; Synaptic transmission; Tail withdrawal reflex

Indexed keywords

4 AMINOPYRIDINE; CYPROHEPTADINE; SEROTONIN; SEROTONIN RECEPTOR;

ADOLESCENT; AGED; ANIMAL EXPERIMENT; APLYSIA; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SYNAPTIC TRANSMISSION;

EID: 0032958760     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-01-00334.1999     Document Type: Article

References (51)

1. Barrett EF, Barrett JN (1976) Separation of two voltage-sensitive potassium currents, and demonstration of a tetrodotoxin-resistant calcium current in frog motoneurones. J Physiol (Lond) 255:737-774.
2. Baxter DA, Byrne JH (1989) Serotonergic modulation of two potassium currents in the pleural sensory neurons of Aplysia. J Neurophysiol 62:665-679.
3. Baxter DA, Byrne JH (1990) 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.
4. Blumenfeld H, Spira ME, Kandel ER, Siegelbaum SA (1990) Facilitatory and inhibitory transmitters modulate calcium influx during action potentials in Aplysia sensory neurons. Neuron 5:487-499.
5. Braha O, Dale N, Hochner B, Klein M, Abrams TW, Kandel ER (1990) 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.
6. Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci 16:425-435.
7. Carmignoto G, Vicini S (1992) Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258:1007-1011.
8. Castellucci VF, Pinsker H, Kupfermann I, Kandel ER (1970) Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167:1745-1748.
9. Crair MC, Malenka RC (1995) A critical period for long-term potentiation at thalamocortical synapses. Nature 375:325-328.
10. Edmonds B, Klein M, Kandel ER (1990) Contributions of two types of calcium channels to synaptic transmission and plasticity. Science 250:1142-1147.
11. 2+ influx in presynaptic facilitation. Nature 361:634-637.
12. Emptage NJ, Mauelshagen J, Carew TJ (1996) Threshold serotonin concentration required to produce synaptic facilitation differs for depressed and nondepressed synapses in Aplysia sensory neurons. J Neurophysiol 75:843-854.
13. Ghirardi M, Braha O, Hochner B, Montarolo PG, Kandel ER, Dale NE (1992) Roles of PKA and PKC in facilitation of evoked and spontaneous transmitter release at depressed and nondepressed synapses in Aplysia sensory neurons. Neuron 9:479-489.
14. Gingrich KJ, Byrne JH (1985) Simulation of synaptic depression, posttetanic potentiation, and presynaptic facilitation of synaptic potentials from sensory neurons mediating gill-withdrawal reflex in Aplysia. J Neurophysiol 53:652-669.
15. Gingrich KJ, Baxter DA, Byrne JH (1988) Mathematical model of cellular mechanisms contributing to presynaptic facilitation. Brain Res Bull 21:513-520.
16. + currents, increasing spike duration and excitability in Aplysia sensory neurons. Proc Natl Acad Sci USA 89:11481-11485.
17. + current development. J Neurosci 16:3287-3295.
18. Hestrin S (1992) Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 357:686-689.
19. + current in the pleural sensory neurons of Aplysia by serotonin and cAMP: implications for spike broadening. Proc Natl Acad Sci USA 89:11476-11480.
20. Hochner B, Klein M, Schacher S, Kandel ER (1986a) Action potential duration and the modulation of transmitter release from sensory neurons of Aplysia in presynaptic facilitation and behavioral sensitization. Proc Natl Acad Sci USA 83:8410-8414.
21. Hochner B, Klein M, Schacher S, Kandel ER (1986b) Additional component in the cellular mechanism of presynaptic facilitation contributes to behavioral dishabituation in Aplysia. Proc Natl Acad Sci USA 83:8794-8798.
22. Hofer M, Constantine-Paton M (1994) Regulation of N-methyl-D-aspartate (NMDA) receptor function during the rearrangement of developing neuronal connections. Prog Brain Res 102:277-285.
23. Illes P, Thesleff S (1978) 4-Aminopyridine and evoked transmitter release from motor nerve endings. Br J Pharmacol 64:623-629.
24. Katz B, Miledi R (1967) The timing of calcium action during neuromuscular transmission. J Physiol (Lond) 189:535-544.
25. Klein M (1994) Synaptic augmentation by 5-HT at rested Aplysia sensorimotor synapses: independence of action potential prolongation. Neuron 13:159-166.
26. 2+ current: mechanism for behavioral sensitization in Aplysia californica. Proc Natl Acad Sci USA 75:3512-3516.
27. Klein M, Camardo J, Kandel ER (1982) Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation in Aplysia. Proc Natl Acad Sci USA 79:5713-5717.
28. Kriegstein AR (1977) Stages of post-hatching development of Aplysia californica. J Exp Zool 199:275-288.
29. Levitan IB, Kaczmarek LK (1996) The neuron. New York: Oxford UP.
30. Marcus EA, Carew TJ (1998) Developmental emergence of biophysical plasticity in sensory neurons of juvenile Aplysia. Proc Natl Acad Sci USA 95:4726-4731.
31. Mauelshagen J, Parker GR, Carew TJ (1996) Dynamics of induction and expression of long-term synaptic facilitation in Aplysia. J Neurosci 16:7099-7108.
32. Mercer AR, Emptage NJ, Carew TJ (1991) Pharmacological dissociation of modulatory effects of serotonin in Aplysia sensory neurons. Science 254:1811-1813.
33. Mishina M, Takai T, Imoto K, Noda M, Takahashi T, Numa S, Methfessel C, Sakmann B (1986) Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature 321:406-411.
34. Nolen TG, Marcus EA, Carew TJ (1987) Development of learning and memory in Aplysia. III. Central neuronal correlates. J Neurosci 7:144-153.
35. Pieroni JP, Byrne JH (1992) Differential effects of serotonin, FMRF-amide, and small cardioactive peptide on multiple, distributed processes modulating scnsorimotor synaptic transmission in Aplysia. J Neurosci 12:2633-2647.
36. Rankin CH, Carew TJ (1987) Development of learning and memory in Aplysia. II. Habituation and dishabituation. J Neurosci 7:133-143.
37. Rayport SG, Camardo JS (1984) Differential emergence of cellular mechanisms mediating habituation and sensitization in the developing Aplysia nervous system. J Neurosci 4:2528-2532.
38. Shuster MJ, Siegelbaum SA (1987) Pharmacological characterization of the serotonin-sensitive potassium channel of Aplysia sensory neurons. J Gen Physiol 90:587-608.
39. + channels in Aplysia sensory neurones. Nature 299:413-417.
40. Spitzer NC (1991) A developmental handshake: neuronal control of ionic currents and their control of neuronal differentiation. J Neurobiol 22:659-673.
41. Stark LL (1997) Development of synaptic plasticity in Aplysia californica. PhD thesis, Yale University.
42. Stark LL, Carew TJ (1994) Serotonergic facilitation of synaptic transmission in juvenile Aplysia. Soc Neurosci Abstr 20:814.
43. Stark LL, Carew TJ (1996) Synaptic facilitation is independent of spike duration in sensory neurons of juvenile Aplysia. Soc Neurosci Abstr 22:695.
44. Stark LL, Mercer AR, Emptage NJ, Carew TJ (1996) Pharmacological and kinetic characterization of two functional classes of serotonergic modulation in Aplysia sensory neurons. J Neurophysiol 75:855-866.
45. Stopfer M, Carew TJ (1996) Heterosynaptic facilitation of tail sensory neuron synaptic transmission during habituation in tail-induced tail and siphon withdrawal reflexes of Aplysia. J Neurosci 16:4933-4948.
46. Sugita S, Goldsmith JR, Baxter DA, Byrne JH (1992) Involvement of protein kinase C in serotonin-induced spike broadening and synaptic facilitation in sensorimotor connections of Aplysia. J Neurophysiol 68:643-651.
47. Sugita S, Baxter DA, Byrne JH (1994) Activators of protein kinase C mimic serotonin-induced modulation of a voltage-dependent potassium current in pleural sensory neurons of Aplysia. J Neurophysiol 72:1240-1249.
48. Sugita S, Baxter DA, Byrne JH (1997) Differential effects of 4-aminopyridine, serotonin, and phorbol esters on facilitation of sensorimotor connections in Aplysia. J Neurophysiol 77:177-185.
49. Walters ET, Byrne JH, Carew TJ, Kandel ER (1983a) Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. J Neurophysiol 50:1522-1542.
50. Walters ET, Byrne JH, Carew TJ, Kandel ER (1983b) Mechanoafferent neurons innervating tail of Aplysia. II. Modulation by sensitizing stimulation. J Neurophysiol 50:1543-1559.
51. 2+ channels in rat hippocampus. J Neurosci 16:2226-2237.