Differential distribution of functional receptors for neuromodulators evoking short-term heterosynaptic plasticity in Aplysia sensory neurons

Journal of Neuroscience

Volumn 16, Issue 23, 1996, Pages 7540-7549

  Sun, Zhong Yi ^a   Kauderer, Beth ^a   Schacher, Samuel ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

Aplysia; excitability; FMRFamide receptors; sensory neuron; serotonin receptors; short term; synaptic plasticity

Indexed keywords

NEUROTRANSMITTER RECEPTOR; PHENYLALANYLMETHIONYLARGINYLPHENYLALANINAMIDE; SEROTONIN;

ANIMAL CELL; APLYSIA; ARTICLE; CONTROLLED STUDY; MOTONEURON; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SENSORY NERVE CELL;

EID: 0029912646     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-23-07540.1996     Document Type: Article

References (73)

1. Anderson MJ, Cohen MW (1977) Nerve-induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells. J Physiol (Lond) 268:757-773.
2. Backsai BJ, Hochner B, Mahaut-Smith M, Adams SR, Kaang B, Kandel ER, Tsien RY (1993) Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science 260:222-226.
3. Bank M, Schacher S (1992) Segregation of presynaptic inputs on an identified target neuron in vitro: structural remodeling visualized over time. J Neurosci 12:2960-2972.
4. 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.
5. Belardetti F, Schacher S, Kandel ER, Siegelbaum SA (1986) 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.
6. Belardetti F, Kandel ER, Siegelbaum SA (1987) Neuronal inhibition by the peptide FMRFamide involves opening of S-potassium channels. Nature 325:153-156.
7. Bernier L, Castellucci VF, Kandel ER, Schwartz JH (1982) 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.
8. 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.
9. Brunelli M, Castellucci VF, Kandel ER (1976) Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science 194:1178-1181.
10. Brown RO, Gusman D, Basbaum AI, Mayeri E (1985) Identification of Aplysia neurons containing immunoreactive FMRFamide. Neuropeptides 6:517-526.
11. Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci 16:425-435.
12. Buttner N, Siegelbaum SA, Volterra A (1989) Direct modulation of Aplysia S-potassium channels by a 12-lipoxygenase metabolite of arachidonic acid. Nature 342:553-555.
13. Castellucci VF, Kandel ER, Schwartz JH, Wilson AC, Nairn A, Greengard P (1980) 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 77:7492-7496.
14. Clark GA, Cooper J (1993) Synapse-specific inhibition by FMRFamide at Aplysia sensorimotor connections. Soc Neurosci Abstr 19:18.
15. Clark GA, Kandel ER (1984) Branch-specific heterosynaptic facilitation in Aplysia siphon sensory cells. Proc Nail Acad Sci USA 81:2577-2581.
16. Critz SD, Baxter DA, Byrne JH (1991) Modulatory effects of serotonin, FMRFamide, and myomodulin on the duration of action potentials, excitability, and membrane currents in tail sensory neurons of Aplysia. J Neurophysiol 66:1912-1926.
17. Dale N, Kandel ER (1990) Facilitatory and inhibitory transmitters modulate spontaneous transmitter release at cultured Aplysia sensorimotor synapses. J Physiol (Lond) 421:203-222.
18. Dale N, Kandel ER (1993) L-Glutamate may be the fast excitatory transmitter of Aplysia sensory neurons. Proc Natl Acad Sci USA 90:7163-7167.
19. Dale N, Kandel ER, Schacher S (1987) Serotonin produces long-term changes in the excitability of Aplysia sensory neurons in culture that depend on new protein synthesis. J Neurosci 7:2232-2238.
20. Dale N, Schacher S, Kandel ER (1988) Long-term facilitation in Aplysia involves increase in transmitter release. Science 239:282-285.
21. Dan Y, Poo MM (1994) Retrograde interactions during formation and elimination of neuromuscular synapses. Curr Opin Neurobiol 4:95-100.
22. Davenport RW, Dou P, Rehder V, Kater SB (1993) A sensory role for neuronal growth cone filopodia. Nature 361:721-724.
23. Drapeau P, Catarsi S, Merz DC (1995) Signaling synapse formation between identified neurons. J Physiol (Paris) 89:115-123.
24. Emptage NJ, Carew TJ (1993) Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. Science 262:253-256.
25. Falls DL, Harris DA, Johnson FA, Morgan MM, Corfas G, Fischbach GD (1990) ARIA: a protein that may regulate the accumulation of acetylcholine receptors at developing chick neuromuscular junction. Cold Spring Harb Symp Quant Biol 50:397-406.
26. Frank E, Fischbach GD (1979) 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.
27. Gapon S, Kupfermann I (1996) Evidence for transmitter similarity of two classes of mechanoreceptor neurons in the cerebral ganglion of Aplysia. Neurosci Lett 205:157-160.
28. Glanzman DL, Kandel ER, Schacher S (1989a) Identified target motor neuron regulates neurite outgrowth and synapse formation of Aplysia sensory neurons in vitro. Neuron 3:441-450.
29. Glanzman DL, Mackey SL, Hawkins RD, Dyke AM, Lloyd PE, Kandel ER (1989b) 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.
30. Glanzman DL, Kandel ER, Schacher S (1990) Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science 249:799-802.
31. Goldberg DJ, Schacher S (1996) Culturing the large identified neurons of Aplysia. In: Culturing nerve cells, 2nd Ed (Banker G, Goslin K, eds). Cambridge, MA: MIT, in press.
32. Goldberg JI, Mills LR, Kater SB (1991) Novel effects of serotonin on neurite outgrowth in neurons cultured from embryos of Helisoma trivolvis. J Neurobiol 22:182-194.
33. Hall ZW, Sanes JR (1993) Synaptic structure and development: the neuromuscular junction. Neuron 10:99-122.
34. Hammer M, Cleary LJ, Byrne JH (1989) Serotonin acts in the synaptic region of sensory neurons in Aplysia to enhance transmitter release. Neurosci Lett 104:235-240.
35. Haydon PG, McCobb DP, Kater SB (1984) Serotonin selectively inhibits growth cone motility and synaptogenesis of specific identified neurons. Science 226:561-564.
36. Hochner B, Klein M, Schacher S, Kandel ER (1986) Additional components in the cellular mechanism of presynaptic facilitation contributes to behavioral dishabituation in Aplysia. Proc Natl Acad Sci USA 83:8794-8798.
37. Kater SB, Rehder V (1995) The sensory-motor role of growth cone filopodia. Curr Opin Neurobiol 5:68-74.
38. Kistler HB, Hawkins RD, Koester J, Steinbusch HWM, Kandel ER, Schwartz JH (1985) Distribution of serotonin-immunoreactive cell bodies and processes in the abdominal ganglion of mature Aplysia. J Neurosci 5:72-80.
39. Klein M, Schapiro E, Kandel ER (1980) Synaptic plasticity and modulation of the calcium current. J Exp Biol 89:117-157.
40. Klein M, Hochner B, Kandel ER (1986) 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.
41. Li XC, Giot JF, Kuhl D, Hen R, Kandel ER (1995) 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.
42. Lloyd PE, Frankfurt M, Stevens P, Kupfermann I, Weiss KR (1987) Biochemical and immunocytochemical localization of the neuropeptides FMRFamide, SCPA, SCPB, to neurons involved in the regulation of feeding in Aplysia. J Neurosci 7:1123-1132.
43. Lohof AM, Quillan M, Day Y, Poo MM (1992) Asymmetric modulation of cytosolic cAMP activity induces growth cone turning. J Neurosci 12:1253-1261.
44. Mackey SL, Kandel ER, Hawkins RD (1989) Identified serotonergic neurons LCB1 and RCB1 in the cerebral ganglion of Aplysia produce presynaptic facilitation of siphon sensory neurons. J Neurosci 9:4227-4235.
45. McMahan UJ, Wallace BG (1989) Molecules in the basal lamina that direct the formation of synaptic specializations at neuromuscular junctions. Dev Neurosci 11:227-247.
46. Mercer AR, Emptage NJ, Carew TJ (1991) Pharmacological dissociation of modulatory effects of serotonin in Aplysia sensory neurons. Science 254:1811-1813.
47. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S (1986) A critical time window for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234:1249-1254.
48. Montarolo PG, Kandel ER, Schacher S (1988) Long-term heterosynaptic inhibition in Aplysia. Nature 333:171-174.
49. Occor KA, Byrne JH (1985) Membrane responses and changes in cyclic AMP levels in Aplysia neurons by serotonin, tryptamine, FMRFamide, and small cardioactive peptide (SCPb). Neurosci Lett 55:113-118.
50. Pieroni JP, Byrne JH (1992) Differential effects of serotonin, FMRF-amide, and small cardioactive peptide on multiple, distributed processes modulating sensorimotor synaptic transmission in Aplysia. J Neurosci 12:2633-2647.
51. Piomelli D, Volterra A, Dale N, Siegelbaum SA, Kandel ER, Schwartz JH, Belardetti F (1987) Lipoxygenase metabolites of arachidonic acid as second messengers for presynaptic inhibition of Aplysia sensory cells. Nature 328:38-43.
52. Rayport SG, Schacher S (1986) Synaptic plasticity in vitro: cell culture of identified Aplysia neurons mediating short-term habituation and sensitization. J Neurosci 6:759-763.
53. Rosen SC, Susswein AJ, Cropper EC, Weiss KR, Kupfermann I (1989) Selective modulation of spike duration by serotonin and the neuropeptides, FMRFamide, SCPb, buccalin and myomodulin in different classes of mechanoafferent neurons in the cerebral ganglion of Aplysia. J Neurosci 9:390-402.
54. Saktor TC, Schwartz JH (1990) Sensitizing stimuli cause translocation of protein kinase C in Aplysia sensory neurons. Proc Natl Acad Sci USA 87:2036-2039.
55. Schacher S (1985) Differential synapse formation and neuritic outgrowth at two branches of the metacerebral cell of Aplysia in dissociated cell culture. J Neuiosci 5:2028-2034.
56. Schacher S, Montarolo PG (1991) Target-dependent structural changes in sensory neurons of Aplysia accompany long-term heterosynaptic inhibition. Neuron 6:679-690.
57. Schacher S, Proshansky E (1983) Neurite regeneration by Aplysia neurons in dissociated cell culture: modulation by Aplysia hemolymph and the presence of the initial axon segment. J Neurosci 3:2403-2413.
58. Schaefer M, Piccioto M, Kreiner T, Kaldany RR, Taussig R, Sheller RH (1985) Aplysia neurons express a gene encoding multiple FMRFamide neuropeptides. Cell 41:467-467.
59. Schacher S, Montarolo PG, Kandel ER (1990) 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.
60. Schacher S, Glanzman DL, Barzilai A, Dash P, Grant SON, Keller F, Mayford M, Kandel ER (1991) Long-term facilitation in Aplysia: persistent phosphorylation and structural changes. Cold Spring Harb Symp Quant Biol 55:187-202.
61. Schacher S, Kandel ER, Montarolo PG (1993) cAMP and arachidonic acid simulate long-term structural and functional changes produced by neurotransmitters in Aplysia sensory neurons. Neuron 10:1079-1088.
62. + channels in Aplysia sensory neurons. Nature 299:413-417.
63. Small SA, Cohen TE, Kandel ER, Hawkins RD (1992) Identified FMRFamide-immunoreactive neuron LPL16 in the left pleural ganglion of Aplysia produces presynaptic inhibition of siphon sensory neu-rons. J Neurosci 12:1616-1627.
64. Sossin WS, Schwartz JH (1992) Selective activation of calcium-activated PKCs in Aplysia neurons by 5-HT. J Neurosci 9:3218-3229.
65. Stoop R, Poo MM (1995) Potentiation of transmitter release by ciliary neurotrophic factor requires somatic signaling. Science 267:695-699.
66. Sugita S, Goldsmith JR, Baxter DA, Byrne JH (1992) Involvement of protein kinase C in serotonin-induced spike broadening and synaptic facilitation of sensorimotor connections in Aplysia. J Neurophysiol 68:643-651.
67. Sun ZY, Schacher S (1996) Development of short-term heterosynaptic facilitation at Aplysia sensorimotor synapses in vitro is accompanied by changes in the functional expression of presynaptic serotonin receptors. J Neurophysiol, in press.
68. Trudeau LE, Castellucci VF (1993) Excitatory amino acid neurotrans-mission at sensory-motor and interneuronal synapses of Aplysia californica. J Neurophysiol 70:1221-1230.
69. Xu Y, Cleary LJ, Byrne JH (1994) Identification and characterization of pleural neurons that inhibit tail sensory neurons and motor neurons in Aplysia: correlation with FMRFamide immunoreactivity. J Neurosci 14:3565-3577.
70. Zhang ZS, Fang B, Marshak DW, Byrne JH, Cleary LJ (1991) Serotonergic varicosities make synaptic contacts with pleural sensory neurons of Aplysia. J Comp Neurol 311:259-270.
71. Zheng JQ, Felder M Connor JA, Poo MM (1994) Turning of nerve growth cones induced by neurotransmitters. Nature 368:140-144.
72. Zhu H, Wu F, Schacher S (1994) 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.
73. Zoran MJ, Doyle RT, Haydon PG (1990) Target-dependent induction of secretory capabilities in an identified motoneuron during synaptogenesis. Dev Biol 138:202-13.