Home LiteratureArticle Details
PMID: 11027355 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A novel function for serotonin-mediated short-term facilitation in aplysia: conversion of a transient, cell-wide homosynaptic hebbian plasticity into a persistent, protein synthesis-independent synapse-specific enhancement.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 97 ·No. 21 ·2000-10-10 ·Pages 11581-6

Bailey CH, Giustetto M, Zhu H, Chen M, Kandel ER

Abstract

Studies of sensitization and classical conditioning of the gill-withdrawal reflex in Aplysia have shown that the synaptic connections between identified glutamatergic sensory neurons and motor neurons can be enhanced in one of two ways: by a heterosynaptic (modulatory input-dependent) mechanism that gives rise with repetition to long-term facilitation and by a homosynaptic (activity-dependent) mechanism that gives rise with repetition to a facilitation that is partially blocked by 2-amino-5-phosphonovaleric acid and by injection of 1,2-bis(2-aminophenoxy)ethane-N,N,N', N'-tetraacetate (BAPTA) into the postsynaptic cell and is similar to long-term potentiation in the hippocampus. We here have examined how these two forms of facilitation interact at the level of an individual synaptic connection by using a culture preparation consisting of a single bifurcated sensory neuron that forms independent synaptic contacts with each of two spatially separated motor neurons. We find that the homosynaptic facilitation produced by a train of action potentials is cell wide and is evident at all of the terminals of the sensory neuron. By contrast, the heterosynaptic facilitation mediated by the modulatory transmitter serotonin (5-HT) can operate at the level of a single synapse. Homosynaptic activation gives rise to only a transient facilitation lasting a few hours, even when repeated in a spaced manner. The heterosynaptic facilitation produced by a single pulse of 5-HT, applied to one terminal of the sensory neuron, also lasts only minutes. However, when one or more homosynaptic trains of spike activity are paired with even a single pulse of 5-HT applied to one of the two branches of the sensory neuron, the combined actions lead to a selective enhancement in synaptic strength only at the 5-HT-treated branch that now lasts more than a day, and thus amplifies, by more than 20-fold, the duration of the individually produced homo- and heterosynaptic facilitation. This form of synapse-specific facilitation has unusual long-term properties. It does not require protein synthesis, nor is it accompanied by synaptic growth.

MeSH Terms
Animals Aplysia/physiology Nerve Tissue Proteins/biosynthesis Neuronal Plasticity Serotonin/physiology Synapses/physiology
Chemicals
Nerve Tissue Proteins Serotonin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Bailey C H
Howard Hughes Medical Institute, and Center for Neurobiology and Behavior, College of Physicians and Surgeons of Columbia University, New York State Psychiatric Institute, New York, NY 10032, USA.
Giustetto M
Zhu H
Chen M
Kandel E R
References (51)
51 references, click to expand
  1. Time course of structural changes at identified sensory neuron synapses during long-term sensitization in Aplysia.
    J Neurosci. 1989 May;9(5):1774-80 PMID: 2723749
  2. Intracellular injection of cAMP induces a long-term reduction of neuronal K+ currents.
    Science. 1988 Jun 17;240(4859):1664-6 PMID: 2837826
  3. Cellular analysis of associative learning.
    Physiol Rev. 1987 Apr;67(2):329-439 PMID: 3550838
  4. Long-term sensitization of a defensive withdrawal reflex in Aplysia.
    Science. 1973 Dec 7;182(4116):1039-42 PMID: 4748675
  5. cAMP evokes long-term facilitation in Aplysia sensory neurons that requires new protein synthesis.
    Science. 1988 Jun 17;240(4859):1667-9 PMID: 2454509
  6. Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons.
    Science. 1993 Apr 9;260(5105):222-6 PMID: 7682336
  7. Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica.
    Learn Mem. 1998 Jul-Aug;5(3):246-56 PMID: 10454368
  8. Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons.
    Neuron. 1998 Dec;21(6):1423-34 PMID: 9883734
  9. Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons.
    Proc Natl Acad Sci U S A. 1988 Apr;85(7):2373-7 PMID: 3353385
  10. Fear and the brain: where have we been, and where are we going?
    Biol Psychiatry. 1998 Dec 15;44(12):1229-38 PMID: 9861466
  11. A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation.
    Science. 1983 Jan 28;219(4583):400-5 PMID: 6294833
  12. Involvement of presynaptic and postsynaptic mechanisms in a cellular analog of classical conditioning at Aplysia sensory-motor neuron synapses in isolated cell culture.
    J Neurosci. 1998 Jan 1;18(1):458-66 PMID: 9412522
  13. Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage.
    Cell. 1997 Dec 26;91(7):927-38 PMID: 9428516
  14. Coincident induction of long-term facilitation in Aplysia: cooperativity between cell bodies and remote synapses.
    Science. 1999 Sep 17;285(5435):1911-4 PMID: 10489370
  15. D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus.
    Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2446-50 PMID: 7708662
  16. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia.
    Science. 1986 Dec 5;234(4781):1249-54 PMID: 3775383
  17. Parallel molecular pathways mediate expression of distinct forms of intermediate-term facilitation at tail sensory-motor synapses in Aplysia.
    Neuron. 2000 Apr;26(1):219-31 PMID: 10798406
  18. Inhibitor of protein synthesis blocks long-term behavioral sensitization in the isolated gill-withdrawal reflex of Aplysia.
    J Neurobiol. 1989 Jan;20(1):1-9 PMID: 2921606
  19. Modulation of both the early and the late phase of mossy fiber LTP by the activation of beta-adrenergic receptors.
    Neuron. 1996 Mar;16(3):611-7 PMID: 8785058
  20. Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation.
    Nature. 1990 Jun 21;345(6277):718-21 PMID: 2141668
  21. Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons.
    Science. 1990 Aug 17;249(4970):799-802 PMID: 2389145
  22. Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia.
    Neuron. 1992 Oct;9(4):749-58 PMID: 1356372
  23. Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change.
    Cell. 1995 Dec 15;83(6):979-92 PMID: 8521521
  24. Roles of PKA and PKC in facilitation of evoked and spontaneous transmitter release at depressed and nondepressed synapses in Aplysia sensory neurons.
    Neuron. 1992 Sep;9(3):479-89 PMID: 1355977
  25. L-glutamate may be the fast excitatory transmitter of Aplysia sensory neurons.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7163-7 PMID: 8102205
  26. MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia.
    Neuron. 1997 Jun;18(6):899-912 PMID: 9208858
  27. Morphological basis of long-term habituation and sensitization in Aplysia.
    Science. 1983 Apr 1;220(4592):91-3 PMID: 6828885
  28. Associative conditioning of single sensory neurons suggests a cellular mechanism for learning.
    Science. 1983 Jan 28;219(4583):405-8 PMID: 6294834
  29. Learning to modulate transmitter release: themes and variations in synaptic plasticity.
    Annu Rev Neurosci. 1993;16:625-65 PMID: 8096376
  30. Hebbian induction of long-term potentiation of Aplysia sensorimotor synapses: partial requirement for activation of an NMDA-related receptor.
    Proc Biol Sci. 1994 Mar 22;255(1344):215-21 PMID: 7912832
  31. CREB and the formation of long-term memory.
    Curr Opin Neurobiol. 1996 Apr;6(2):264-8 PMID: 8725970
  32. Long-term enhancement produced by activity-dependent modulation of Aplysia sensory neurons.
    J Neurosci. 1985 Mar;5(3):662-72 PMID: 3973691
  33. Synaptic plasticity in vitro: cell culture of identified Aplysia neurons mediating short-term habituation and sensitization.
    J Neurosci. 1986 Mar;6(3):759-63 PMID: 3958793
  34. Monosynaptic connections made by the sensory neurons of the gill- and siphon-withdrawal reflex in Aplysia participate in the storage of long-term memory for sensitization.
    Proc Natl Acad Sci U S A. 1985 Dec;82(23):8266-9 PMID: 16593630
  35. Presynaptic facilitation revisited: state and time dependence.
    J Neurosci. 1996 Jan 15;16(2):425-35 PMID: 8551327
  36. Invertebrate learning and memory: from behavior to molecules.
    Annu Rev Neurosci. 1986;9:435-87 PMID: 2423010
  37. CREB1 encodes a nuclear activator, a repressor, and a cytoplasmic modulator that form a regulatory unit critical for long-term facilitation.
    Cell. 1998 Oct 16;95(2):211-23 PMID: 9790528
  38. A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis.
    Cell. 1999 Oct 15;99(2):221-37 PMID: 10535740
  39. Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia.
    Science. 1970 Mar 27;167(3926):1745-8 PMID: 5416543
  40. Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP.
    Science. 1976 Dec 10;194(4270):1178-81 PMID: 186870
  41. The long and the short of long-term memory--a molecular framework.
    Nature. 1986 Jul 31-Aug 6;322(6078):419-22 PMID: 2874497
  42. Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons.
    Science. 1993 Oct 8;262(5131):253-6 PMID: 8211146
  43. Differential classical conditioning of a defensive withdrawal reflex in Aplysia californica.
    Science. 1983 Jan 28;219(4583):397-400 PMID: 6681571
  44. Long-lasting forms of synaptic potentiation in the mammalian hippocampus.
    Learn Mem. 1996 Sep-Oct;3(2-3):74-85 PMID: 10456078
  45. Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons.
    Neuron. 1993 Mar;10(3):427-35 PMID: 8384857
  46. Molecular enhancement of memory formation.
    Neuron. 1996 Jan;16(1):5-8 PMID: 8562090
  47. Mediation of classical conditioning in Aplysia californica by long-term potentiation of sensorimotor synapses.
    Science. 1997 Oct 17;278(5337):467-71 PMID: 9334306
  48. The control of short-term memory.
    Sci Am. 1971 Aug;225(2):82-90 PMID: 5089457
  49. Involvement of pre- and postsynaptic mechanisms in posttetanic potentiation at Aplysia synapses.
    Science. 1997 Feb 14;275(5302):969-73 PMID: 9020078
  50. C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia.
    Cell. 1994 Mar 25;76(6):1099-114 PMID: 8137425
  51. Pathway-specific synaptic plasticity: activity-dependent enhancement and suppression of long-term heterosynaptic facilitation at converging inputs on a single target.
    J Neurosci. 1997 Jan 15;17(2):597-606 PMID: 8987782
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.97.21.11581
Published
2000-10-10
Pages
11581-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC17243
Subset
IM
Grants
NIMH NIH HHS · R01 MH037134 · United States
NIMH NIH HHS · MH37134 · United States
External Links
PubMed source DOI: 10.1073/pnas.97.21.11581 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2