Tetanic stimulation and cyclic adenosine monophosphate regulate segregation of presynaptic inputs on a common postsynaptic target neuron in vitro

Journal of Neurobiology

Volumn 29, Issue 2, 1996, Pages 183-201

  Sun, Zhong Yi ^a   Schacher, Samuel ^a  

^a Department of Neurology and the Taub Institute for Research on Alzheimer's Disease and the Aging Brain   (United States)

Author keywords

Aplysia; competition; synapse elimination; synapse formation; tetanus

Indexed keywords

CYCLIC AMP;

ANIMAL CELL; APLYSIA; ARTICLE; COMPETITIVE INHIBITION; EVOKED RESPONSE; FACILITATION; GENE SEGREGATION; GENETIC REGULATION; MUSCLE TETANIC CONTRACTION; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION; TARGET CELL; TETANUS; VARICOSIS;

ANIMALS; APLYSIA; AXONS; CELLS, CULTURED; CYCLIC AMP; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; MOTOR NEURONS; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; SYNAPSES;

EID: 0030033834     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199602)29:2<183::AID-NEU5>3.0.CO;2-6     Document Type: Article

References (81)

1. ALBERINI, C. M., GHIRARDI, M., METZ, R., and KANDEL, E. R. (1994). C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76:1099-1114.
2. ANTONINI, A. and STRYKER, M. P. (1993a). Rapid remodeling of axonal arbors in the visual cortex. Science 260:1819-1821.
3. ANTONINI, A. and STRYKER, M. P. (1993b). Development of individual geniculcortical arbors in cat striate cortex and effects of binocular impulse blockade. J. Neurosci. 13:3549-3573.
4. ARTOLA, A. and SINGER, W. (1987). Long-term potentiation and NMDA receptors in rat visual cortex. Nature 330:649-652.
5. BAILEY, C. H. and CHEN, M. (1983). Morphological basis of long-term habituation and sensitization in Aplysia. Science 220:91-93.
6. BAILEY, C. H. and 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, C. H., MONTAROLO, P. G., CHEN, M., KANDEL, E. R., and SCHACHER, S. (1992). Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia Neuron 9:749-758.
8. BALICE-GORDON, R. J. and LICHTMAN, J. W. (1993). In vivo observations of pre- and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. J. Neurosci. 13:834-855.
9. BALICE-GORDON, R. J. and LICHTMAN, J. W. (1994). Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372:519-524.
10. BANK, M. and SCHACHER, S. (1992). Segregation of presynaptic inputs on an identified target neuron in vitro: structural remodeling visualized over time. J. Neurosci. 12:2960-2972.
11. BEAR, M. F. and MALENKA, R. C. (1994). Synaptic plasticity: LTP and LTD. Curr. Opin. Neurobiol. 4: 389-399.
12. BLISS, T. V. P. and COLLINGRIDGE, G. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
13. BUONOMANO, D. V. and BYRNE, J. H. (1990). Long-term synaptic changes produced by a cellular analog of classical conditioning in Aplysia. Science 249:420-423.
14. CASTELLUCCI, V. F., KANDEL, E. R., SCHWARTZ, J. H., WILSON, A. C., NAIRN, A., and GREENGARD, P. (1980). Intracellular injection of the catalytic subunit of cAMP-dependent protein kinase stimulates facilitation of transmitter release underlying behavioral sensitization in Aplysia Proc. Natl Acad. Sci. USA 77: 7492-7496.
15. CHANGEAUX, J. P. and DANCHIN, A. (1976). Selective stabilization of developing synapses as a mechanism for the specification of neural networks. Nature 264: 705-712.
16. CLARK, G. A. and KANDEL, E. R. (1984). Branch-specific heterosynaptic facilitation in Aplysia siphon sensory cells. Proc. Natl. Acad. Sci. USA 81:2577-2581.
17. CLINE, H. T., DEBSKI, E. A., and CONSTANTINE-PATON, M. (1987). NMDA receptor antagonist desegregates eye-specific stripes. Proc. Natl Acad. Sci. USA 84: 4342-4345.
18. CONSTANTINE-PATON, M., CLINE, H. T., and DEBSKI, E. A. (1990). Patterned activity, synaptic convergence and the NMDA receptor in developing visual pathways. Annu. Rev. Neurosci. 13:129-154.
19. DALE, N. and KANDEL, E. R. (1993). L-glutamate may be the fast excitatory transmitter of Aplysia sensory neurons. Proc. Natl. Acad. Sci. USA 90:7163-7167.
20. DAN, Y. and POO, M.-M. (1992). Hebbian depression of isolated neuromuscular synapses in vitro. Science 256:1570-1573.
21. DAN, Y. and POO, M.-M. (1994). Retrograde interactions during formation and elimination of neuromuscular synapses. Curr. Opin. Neurobiol. 4:95-100.
22. DASH, P. K., HOCHNER, B., and KANDEL, E. R. (1990). Injection of the cAMP-responsive element into the nucleus of the Aplysia sensory neurons blocks long-term facilitation. Nature 345:718-721.
23. DIXON, D. and ATWOOD, H. L. (1989). Adenylate cyclase system is essential for long-term facilitation at the crayfish neuromuscuiar junction. J. Neurosci. 9: 4246-4252.
24. ELIOT, L. S., HAWKINS, R. D., KANDEL, E. R., and SCHACHER, S. (1994). Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor neuron synapses in isolated cell culture. J. Neurosci. 14:368-383.
25. EMPTAGE, N. J. and CAREW, T. J. (1993). Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. Science 262:253-256.
26. FORSCHER, P. and SMITH, S. J. (1988). Actions of cytochalasin on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107:1505-1516.
27. FORSCHER, P., KACZMAREK, L. K., BUCHANAN, J., and SMITH, S. J. (1987). Cyclic AMP induces changes in distribution and transport of organelles within growth cones of Aplysia bag cell neurons. J. Neurosci 7:3600-3611.
28. FUNTE, L. R. and HAYDON, P. G. (1993). Synaptic target contact enhances presynaptic calcium influx by activating cAMP-dependent protein kinase during synaptogenesis. Neuron 10:1069-1078.
29. GLANZMAN, D. L. (1994). Postsynaptic regulation of the development and long-term plasticity of Aplysia sensorimotor synapses in cell culture. J. Neurobiol. 25: 666-693.
30. GLANZMAN, D. L., KANDEL, E. R., and SCHACHER, S. (1989). Identified target motor neuron regulates neurite outgrowth and synapse formation of Aplysia sensory neurons in vitro. Neuron 3:441-450.
31. GLANZMAN, D. L., KANDEL, E. R., and SCHACHER, S. (1990). Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science 249:799-802.
32. GLANZMAN, D. L., KANDEL, E. R., and SCHACHER, S. (1991). Target-dependent morphological segregation of Aplysia sensory outgrowth in vitro. Neuron 7:903-913.
33. GOLDBERG, D. J. and SCHACHER, S. (1987). Differential growth of the two branches of a regenerating bifurcate axon is associated with differential axonal transport of organelles. Dev. Biol. 124:35-40.
34. GOODMAN, C. S. and SHATZ, C. J. (1993). Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72/Neuron 10:77-98.
35. GU, X. and MULLER, K. J. (1990). Competitive interactions between neurons making axosomatic contacts in the leech. J. Neurosci. 10:3814-3822.
36. HATA, Y. and STRYKER, M. P. (1994). Control of thalamocortical afferent rearrangement by postsynaptic activity in developing visual cortex. Science 265:1732-1735.
37. HEBB, D. O. (1949). The Organization of Behavior: A Neurophysiological Theory. Wiley Press, New York.
38. HUBEL, D. H. and WIESEL, T. N. (1970). The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol (Lond) 206:419-436.
39. ITO, M. (1989). Long-term depression. Annu. Rev. Neurosci 12:85-102.
40. KAANG, B.-K., KANDEL, E. R., and GRANT, S. G. N. (1993). Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons. Neuron 10:427-435.
41. KIRKWOOD, A., DUDEK, S. M., GOLD, J. T., AIZENMAN, C. D., and BEAR, M. F. (1993). Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. Science 260:1518-1521.
42. KLEINSCHMIDT, A., BEAR, M. F., and SINGER, W. (1987). Blockade of NMDA receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238:355-358.
43. LEVAY, S., WIESEL, T. N., and HUBEL, D. H. (1980). The development of ocular dominance columns in normal and visually deprived monkeys. J Comp. Neurol. 191:1-51.
44. LIN, C.-H. and FORSCHER, P. (1993). Cytoskeletal remodeling during growth cone-target interactions. J. Cell Biol. 121:1369-1383.
45. LIN, X. Y. and GLANZMAN, D. L. (1994a). Long-term potentiation of Aplysia sensorimotor synapses in cell culture: regulation by postsynaptic voltage. Proc. R Soc. Lond B 255:113-118.
46. LIN, X. Y. and GLANZMAN, D. L. (1994b). Hebbian induction of long-term potentiation of Aplysia sensorimotor synapses: partial requirement for activation of an NMDA-related receptor. Proc. R. Soc. Lond. B 255: 215-221.
47. LIU, Y., FIELDS, R. D., FITZGERALD, S., FESTOFF, B. W., and NELSON, P. G. (1994). Proteolytic activity, synapse elimination, and the Hebb synapse. J. Neurobiol. 25:325-335.
48. LO, Y.-J. and POO, M.-M. (1991). Activity-dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses. Science 254:1019-1022.
49. LO, Y.-J. and POO, M.-M. (1994). Heterosynaptic suppression of developing neuromuscular synapses in culture. J. Neurosci. 14:4684-4693.
50. LO, Y.-J., LIN, Y. C., SANES, D. H., and POO, M.-M. (1994). Depression of developing neuromuscular synapses induced by repetitive postsynaptic depolarizations. J. Neurosci. 14:4694-4704.
51. MONTAROLO, P. G., GOELET, P., CASTELLUCCI, V. F., MORGAN, J., KANDEL, E. R., and SCHACHER, S. (1986). A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234:1249-1254.
52. MONTAROLO, P. G., KANDEL, E. R., and SCHACHER, S. (1988). Long-term heterosynaptic inhibition in Aplysia. Nature 333:171-174.
53. MURPHEY, R. K. (1986). Competition and the dynamics of axon arbor growth in the cricket. J Comp. Neurol 251:100-110.
54. NAZIF, F. A., BYRNE, J. H., and CLEARY, L. J. (1991). cAMP induces long-term morphological changes in sensory neurons of Aplysia. Brain Res. 539:324-327.
55. O'DELL, T. J., HAWKINS, R. D., KANDEL, E. R., and ARANCIO, O. (1991). Test of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl Acad. Sci. USA 88:11285-11289.
56. PETER, N., ARONOFF, B., WU, F., and SCHACHER, S. (1994). Decrease in growth cone-neurite fasciculation by sensory or motor cells in vitro accompanies modulation of Aplysia cell adhesion molecule by 5-HT or FMRFamide. J Neurosci. 14:1413-1421.
57. PURVES, D. and LICHTMAN, J. W. (1985). Principles of Neuronal Development Sinauer Press, Sunderland, MA.
58. RABACCHI, S., BAILLY, Y., DELHAYE-BOUCHAUD, N., and MARIANI, J. (1992). Involvement of the NMDA receptor in synapse elimination during cerebellar development. Science 256:1823-1825.
59. RAMOA, A. S., CAMPBELL, G., and SHATZ, C. J. (1988). Dendritic growth and remodeling of cat retinal ganglion cells during fetal and postnatal development. J. Neurosci. 8:4239-4261.
60. RAYPORT, S. G. and SCHACHER, S. (1986). Synaptic plasticity in vitro: cell culture of identified Aplysia neurons mediating short-term habituation and sensitization. J Neurosci. 6:759-763.
61. SCHACHER, S. (1985). Differential synapse formation and neurite outgrowth at two branches of the metacerebral cell of Aplysia in dissociated cell culture. J. Neurosci. 5:2028-2034.
62. SCHACHER, S. and MONTAROLO, P. G. (1991). Target-dependent structural changes in sensory neurons of Aplysia accompany long-term heterosynaptic inhibition. Neuron 6:679-690.
63. SCHACHER, S., CASTELLUCCI, V. F., and KANDEL, E. R. (1988). Cyclic AMP evokes long-term facilitation in Aplysia sensory neurons that requires new protein synthesis. Science 240:1667-1669.
64. SCHACHER, S., MONTAROLO, P. G., and KANDEL, E. R. (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.
65. SCHACHER, S., GLANZMAN, D. L., BARZILAI, A., DASH, P., GRANT, S. G. N., KELLER, F., MAYFORD, M., and KANDEL, E. R. (1991). Long-term facilitation in Aplysia: persistent phosphorylation and structural changes. Cold Spring Harbor Symp. Quant. Biol. 55: 187-202.
66. SCHACHER, S., MONTAROLO, P. G., and KANDEL, E. R. (1993). cAMP and arachidonic acid simulate long-term structural and functional changes produced by neurotransmitters in Aplysia sensory neurons. Neuron 10:1079-1088.
67. SCHLAGGAR, B. L., FOX, K., and O'LEARY, D. M. (1993). Postsynaptic control of plasticity in developing somatosensory cortex. Nature 364:623-626.
68. SCHOLZ, K. P. and BYRNE, J. H. (1987). Long-term sensitization in Aplysia, biophysical correlates in tail sensory neurons. Science 235:685-687.
69. SCHOLZ, K. P. and BYRNE, J. H. (1988). Intracellular injection of cAMP induces a long-term reduction of neuronal potassium currents. Science 240:1664-1667.
70. SCHUMAN, E. M. and MADISON, D. V. (1991). A requirement for the intracellular messenger nitric oxide in long-term potentiation. Science 254:1503-1506.
71. STENT, G. S. (1973). A physiological mechanism for Hebb's postulate of learning. Proc Natl. Acad. Sci. USA 70:997-1001.
72. STRYKER, M. P. and HARRIS, W. A. (1986). Binocular impulse blockade prevents the formation of occular dominance columns in cat visual cortex. J. Neurosci. 6:2117-2133.
73. TRIFARO, J.-M. and VITALE, M. L. (1993). Cytoskeleton dynamics during neurotransmitter release. Trends Neurosci. 16:466-472.
74. WALTERS, E. T. and BYRNE, J. H. (1984). Posttetanic potentiation in Aplysia sensory neurons. Brain. Res. 293:377-380.
75. WANG, J., RENGER, J. J., GRIFFITH, L. C., GREENSPAN, R. J., and WU, C.-F. (1994). Concomitant alterations of physiological and developmental plasticity in Drosophila CaM kinase II-inhibited synapses. Neuron 13: 1373-1384.
76. WILLIAMS, J. H., ERRINGTON, M. L., LYNCH, M. A., and BLISS, T. V. P. (1989). Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus. Nature 341: 739-742.
77. WU, F. and SCHACHER, S. (1994). Pre- and postsynaptic changes mediated by two second messengers contribute to the expression of long-term heterosynaptic inhibition in Aplysia. Neuron 12:407-421.
78. WU, H. H., WILLIAMS, C. V., and MCLOON, S. C. (1994). Involvement of nitric oxide in the elimination of a transient retinotectal projection in development. Science 265:1593-1596.
79. ZHONG, Y., BUDNIK, V., and WU, C.-F. (1992). Synaptic plasticity in Drosophila memory and hyperexcitable mutants: role of cAMP cascade. J. Neurosci. 12: 644-65
80. ZHU, H., WU, F., and SCHACHER, S. (1994a). 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.
81. ZHU, H., WU, F., and SCHACHER, S. (1994b). Changes in expression and distribution of Aplysia cell adhesion molecules can influence synapse formation and elimination in vitro. J. Neurosci. 15:4173-4183.