Binding of serotonin to receptors at multiple sites is required for structural plasticity accompanying long-term facilitation of Aplysia sensorimotor synapses

Journal of Neuroscience

Volumn 18, Issue 11, 1998, Pages 3991-4000

  Sun, Zhong Yi ^a   Schacher, Samuel ^a  

^a The New York Presbyterian Hospital   (United States)

Author keywords

5 HT; Activity dependent plasticity; Aplysia; Long term; Sensory neuron; Structure function relationships; Synaptic plasticity

Indexed keywords

ANIMAL CELL; APLYSIA; ARTICLE; BEHAVIOR; BINDING SITE; CONDITIONING; DRUG RECEPTOR BINDING; FACILITATION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SECOND MESSENGER; SENSORIMOTOR CORTEX; SENSORY NERVE CELL; STRUCTURE ACTIVITY RELATION;

EID: 0032101319     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-11-03991.1998     Document Type: Article

References (78)

1. Abrams TW, Castellucci VF, Camardo JS, Kandel ER, Lloyd P (1984) Two endogenous neuropeptides modulate the gill- and siphonwithdrawal reflex in Aplysia by presynaptic facilitation involving cAMP-dependent closure of a serotonin-sensitive potassium channel. Proc Natl Acad Sci USA 81:7956-7960.
2. Abrams TW, Karl KA, Kandel ER (1991) Biochemical studies of stim- ulus convergence during classical conditioning in Aplysia: dual regulation of adenylate cyclase by calcium/calmodulin and transmitter. J Neurosci 11:2655-2665.
3. Alberini CM, Ghirardi M, Metz R, Kandel ER (1994) C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76:1099-1114.
4. 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.
5. Bailey CH, Chen M (1983) Morphological basis of long-term habituation and sensitization. Science 220:91-93.
6. Bailey CH, Chen M (1988) Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. Proc Natl Acad Sci USA 85:2373-2377.
7. Bailey CH, Kandel ER (1993) Structural changes accompanying memory storage. Annu Rev Physiol 55:397-426.
8. Bailey CH, Chen M, Montarolo PG, Kandel ER, Schacher S (1992) Inhibitors of protein and RNA synthesis block structural and functional changes accompanying long-term synaptic facilitation and inhibition in Aplysia sensory neurons. Neuron 9:749-758.
9. 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.
10. Bao JX, Kandel ER, Hawkins RD (1997) Involvement of pre- and postsynaptic mechanisms in posttetanic potentiation at Aplysia synapses. Science 275:969-973.
11. Bartsch D, Ghirardi M, Skehel PA, Karl KA, Herder SP, Chen M, Bailey CH, Kandel ER (1995) Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 83:979-992.
12. Barzilai A, Kennedy TE, Sweatt JD, Kandel ER (1989) 5-HT modulates protein synthesis and the expression of specific proteins during long-term facilitation in Aplysia sensory neurons. Neuron 2:1577-1586.
13. Buonomano DV, Byrne JH (1990) Long-term synaptic changes produced by a cellular analog of classical conditioning in Aplysia. Science 249:420-423.
14. Byrne JH, Zwartjes R, Homayouni R, Critz SD, Erskin A (1993) Roles of second messenger pathways in neuronal plasticity and in learning and memory. In: Advances in second messenger and phosphoprotein research, Vol 27 (Shennolikar S, Nairn AC, eds), pp 47-108. New York: Raven.
15. Castellucci VF, Kandel ER (1976) Presynaptic facilitation as a mechanism for behavioral sensitization in Aplysia. Science 194:1176-1178.
16. Clark GA, Kandel ER (1984) Branch-specific heterosynaptic facilitation in Aplysia siphon sensory cells. Proc Natl Acad Sci USA 81:2577-2581.
17. Clark GA, Kandel ER (1993) 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.
18. 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.
19. Dale N, Schacher S, Kandel ER (1988) Long-term facilitation in Aplysia involves increase in transmitter release. Science 239:282-285.
20. Dash P, Hochner B, Kandel ER (1990) Injection of cAMP responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345:718-721.
21. Eliot LS, Hawkins RD, Kandel ER, Schacher S (1994) Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor synapses in isolated cell culture. J Neurosci 14:368-383.
22. Emptage NJ, Carew TJ (1993) Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. Science 262:253-256.
23. Frost WN, Castellucci VF, Hawkins RD, Kandel ER (1985) Monosynaptic connections made by the sensory neurons of the gill- and siphonwithdrawal reflex in Aplysia participate in the storage of long-term memory for sensitization. Proc Natl Acad Sci USA 82:8266-8269.
24. Ghirardi M, Braha O, Hochner B, Montarolo PG, Kandel ER, Dale N (1992) Roles of PKA and PKC in facilitation of evoked and spontaneous transmitter release at depressed and non-depressed synapses in Aplysia sensory neurons. Neuron 9:1-20.
25. Ghirardi M, Montarolo PG, Kandel ER (1995) A novel intermediate stage in the transition between short- and long-term facilitation in the sensory to motor neuron synapse of Aplysia. Neuron 14:413-420.
26. Glanzman DL, Kandel ER, Schacher S (1989) Identified target motor neuron regulates neurite outgrowth and synapse formation of Aplysia sensory neurons in vitro. Neuron 3:441-450.
27. Glanzman DL, Kandel ER, Schacher S (1990) Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science 249:799-802.
28. Goelet P, Castellucci VF, Schacher S, Kandel ER (1986) The long and short of long-term memory. Nature 322:419-422.
29. Goldsmith BA, Abrams TW (1991) Reversal of synaptic depression by serotonin at Aplysia sensory neuron synapses involves activation of adenylate cyclase. Proc Natl Acad Sci USA 88:9021-9025.
30. Greenberg SM, Castellucci VF, Bayley H, Schwanz JH (1987) A molecular mechanism for long-term sensitization in Aplysia. Nature 329:62-65.
31. 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.
32. Hawkins RD, Castellucci VF, Kandel ER (1981) Interneurons involved in mediation and modulation of gill-withdrawal reflex in Aplysia. II. Identified neurons produce heterosynaptic facilitation contributing to behavioral sensitization. J Neurophysiol 45:315-326.
33. Hawkins RD, Abrams TW, Carew TJ, Kandel ER (1983) A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science 219:400-405.
34. Hegde AN, Inokuchi K, Pei W, Casadio A, Ghirardi M, Chain DG, Martin KC, Kandel ER, Schwartz JH (1997) Ubiquitin C-terminal hydrolase is an intermediate-early gene essential for long-term facilitation in Aplysia. Cell 89:115-126.
35. Hu Y, Barzilai A, Chen M, Bailey CH, Kandel ER (1993) 5-HT and cAMP induce the formation of coated pits and vesicles and increase the expression of clathrin light chain in sensory neurons of Aplysia. Neuron 10:921-929.
36. Kaang B-K, Kandel ER, Grant SGN (1993) Stimuli that produce long-term facilitation in Aplysia sensory neurons activate the transcription of cAMP-responsive genes. Neuron 10:427-435.
37. Kandel ER, Schwartz JH (1982) Molecular biology of learning: modulation of transmitter release. Science 218:433-443.
38. Kistler HB, Hawkins RD, Koester J, Steinbusch HWM, Kandel ER, Schwartz JH (1985) Distribution of serotonin-immunorcactive cell bodies and processes in the abdominal ganglion of mature Aplysia. J Neurosci 5:72-80.
39. Kuhl D, Kennedy TE, Barzilai A, Kandel ER (1992) Long-term sensitization training in Aplysia leads to an increase in the expression of Bip, the major protein chaperone of the endoplasmic reticulum. J Cell Biol 119:1069-1076.
40. 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.
41. Liu QR, Hattar S, Endo S, MacPhee K, Zhang H, Cleary LJ, Byrne JH, Eskin A (1997) A developmental gene (Tolloid/BMP-1) is regulated in Aplysia neurons by treatments that induce long-term sensitization. J Neurosci 17:755-764.
42. Malenka RC, Kauer JA, Perkel DJ, Mark MD, Keily PT, Nicholl RA, Waxham NN (1989) An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature 340:554-557.
43. Martin KC, Casadio A, Bailey CH, Chen M, Zhu H, Kandel ER (1997a) Synapse-specific, transcription-dependent long-term facilitation can be reconstituted in a novel Aplysia sensory-motor neuron culture system. Soc Neurosci Abstr 23:233.
44. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER (1997b) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18:899-912.
45. Mercer AR, Emptage NJ, Carew TJ (1991) Pharmacological dissociation of modulatory effects of serotonin in Aplysia sensory neurons. Science 254:1811-1813.
46. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S (1986) A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234:1249-1254.
47. Montarolo PG, Kandel ER, Schacher S (1988) Long-term heterosynaptic inhibition in Aplysia. Nature 333:171-174.
48. Nazif FA, Byrne JH, Cleary LJ (1991) cAMP induces long-term mor- phological changes in sensory neurons of Aplysia. Brain Res 539:324-327.
49. Occor KA, Walters ET, Byrne JH (1985) Associative conditioning analog selectively increases cAMP levels of tail sensory neurons in Aplvsia. Proc Natl Acad Sci USA 82:2548-2552.
50. O'Leary FA, Byrne JH, Cleary LJ (1995) Long-term structural remodeling in Aplysia sensory neurons requires de novo protein synthesis during a critical time period. J Neurosci 15:3519-3525.
51. 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.
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. SaktorTC, Schwartz JH (1990) Sensitizing stimuli cause translocation of protein kinase C in Aplysia sensory neurons. Proc Natl Acad Sci USA 87:2036-2039.
54. Schacher S (1985) Differential synapse formation and neuritic outgrowth at two branches of the metacerebral cell of Aplysia in dissociated cell culture. J Neurosci 5:2028-2034.
55. Schacher S, Montarolo PG (1991) Target-dependent structural changes in sensory neurons of Aplysia accompany long-term heterosynaptic inhibition. Neuron 6:679-690.
56. 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.
57. Schacher S, Castellucci VF, Kandel ER (1988) Cyclic AMP evokes long-term facilitation in Aplysia sensory neurons that requires new protein synthesis. Science 240:1667-1669.
58. Schacher S, Glanzman DL, Barzilai A, Dash P, Grant SGN, Keller F, Mayford M, Kandel ER (1990a) Long-term facilitation in Aplysia: persistent phosphorylation and structural changes. Cold Spring Harb Symp Quant Biol 55:187-202.
59. Schacher S, Montarolo PG, Kandel ER (1990b) 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, 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.
61. Schacher S, Wu F, Sun ZY (1997) Pathway-specific synaptic plasticity: activity-dependent enhancement and suppression of long-term heterosynaptic facilitation at converging inputs on a single target. J Neurosci 17:597-606.
62. Scholz KP, Byrne JH (1987) Long-term sensitizalion in Aplysia: biophysical correlates in tail sensory neurons. Science 235:685-687.
63. Scholz KP, Byrne JH (1988) Intracellular injection of cAMP induces a long-term reduction of neuronal potassium currents. Science 240:1664-1667.
64. Schuster CM, Davis GW, Fetter RD, Goodman CS (1996) Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17:655-667.
65. 2+-activated PKCs in Aplysia neurons by 5-HT. J Neurosci 12:1160-1168.
66. Stewart BA, Schuster CM, Goodman CS, Atwood HL (1996) Homeostasis of synaptic transmission in Drosophila with genetically altered nerve terminal morphology. J Neurosci 16:3887-3895.
67. Stoup R, Poo MM (1995) Potentiation of transmitter release by ciliary neurotrophic factor requires somatic signaling. Science 267:695-699.
68. 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.
69. Sun Z-Y, 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 76:2250-2261.
70. Sun Z-Y, Kauderer B, Schacher S (1996) Differential distribution of functional receptors for neuromodulators evoking short-term heterosynaptic plasticity in Aplysia sensory neurons. J Neurosci 16:7540-7549.
71. Trudeau L-E, Castellucci VF (1995) Postsynaptic modifications in long-term facilitation in Aplysia: upregulation of excitatory amino acid receptors. J Neurosci 15:1275-1284.
72. Walters ET, Byrne JH (1983) Associative conditioning of single sensory neurons suggests a cellular mechanism for learning. Science 219:405-408.
73. Wu F, Friedman L, Schacher S (1995) Transient versus persistent functional and structural changes associated with facilitation of Aplysia sensory-motor synapses are second messenger-dependent. J Neurosci 15:7517-7527.
74. Yin JCP, Del Vecchio M, Zhou H, Tully T (1995) CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81:107-115.
75. Zhang F, Encio S, Cleary LJ, Eskin A, Byrne JH (1997) Role of transforming growth factor-β in long-term synaptic facilitation in Aplysia. Science 275:1277-1279.
76. 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.
77. Zhu H, Wu F, Schacher S (1995) Changes in expression and distribution of Aplysia cell adhesion molecules can influence synapse formation and elimination in vitro. J Neurosci 15:4173-4183.
78. Zhu H, Wu F, Schacher S (1997) Site-specific and sensory neurondependent increases in postsynaptic glutamate sensitivity accompany serotonin-induced long-term facilitation at Aplysia sensorimotor synapses. J Neurosci 17:4976-4986.