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Science 5 December 1986:
Vol. 234. no. 4781, pp. 1249 - 1254
DOI: 10.1126/science.3775383
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Articles

Science, Vol 234, Issue 4781, 1249-1254
Copyright © 1986 by American Association for the Advancement of Science

articles

A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia

PG Montarolo, P Goelet, VF Castellucci, J Morgan, ER Kandel, and S Schacher

Both long-term and short-term sensitization of the gill and siphon withdrawal reflex in Aplysia involve facilitation of the monosynaptic connections between the sensory and motor neurons. To analyze the relationship between these two forms of synaptic facilitation at the cellular and molecular level, this monosynaptic sensorimotor component of the gill-withdrawal reflex of Aplysia can be reconstituted in dissociated cell culture. Whereas one brief application of 1 microM serotonin produced short-term facilitation in the sensorimotor connection that lasted minutes, five applications over 1.5 hours resulted in long-term facilitation that lasted more than 24 hours. Inhibitors of protein synthesis or RNA synthesis selectively blocked long-term facilitation, but not short-term facilitation, indicating that long-term facilitation requires the expression of gene products not essential for short-term facilitation. Moreover, the inhibitors only blocked long-term facilitation when given during the serotonin applications; the inhibitors did not block the facilitation when given either before or after serotonin application. These results parallel those for behavioral performance in vertebrates and indicate that the critical time window characteristic of the requirement for macromolecular synthesis in long-term heterosynaptic facilitation is not a property of complex circuitry, but an intrinsic characteristic of specific nerve cells and synaptic connections involved in the long-term storage of information.


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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L. Karachot, Y. Shirai, R. Vigot, T. Yamamori, and M. Ito (2001)
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Overexpression of and RNA Interference with the CCAAT Enhancer-Binding Protein on Long-Term Facilitation of Aplysia Sensory to Motor Synapses.
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   Abstract »    Full Text »    PDF »
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Non-Associative Learning and Serotonin Induce Similar Bi-Directional Changes in Excitability of a Neuron Critical for Learning in the Medicinal Leech.
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J. Neurosci. 21, 1401-1412
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Blockade of NGF-Induced Neurite Outgrowth by a Dominant-Negative Inhibitor of the Egr Family of Transcription Regulatory Factors.
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C. H. Bailey, M. Giustetto, H. Zhu, M. Chen, and E. R. Kandel (2000)
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Transition to Endogenous Bursting After Long-Term Decentralization Requires De Novo Transcription in a Critical Time Window.
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J. Neurosci. 20, 2944-2953
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cAMP-Dependent Plasticity at Excitatory Cholinergic Synapses in Drosophila Neurons: Alterations in the Memory Mutant Dunce.
D. Lee and D. K. O'Dowd (2000)
J. Neurosci. 20, 2104-2111
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Limited Contributions of Serotonin to Long-Term Hyperexcitability of Aplysia Sensory Neurons.
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J Neurophysiol 82, 3223-3235
   Abstract »    Full Text »    PDF »
Learning Induces a CDC2-Related Protein Kinase, KKIAMRE.
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C. M. Sherff and T. J. Carew (1999)
Science 285, 1911-1914
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Levels of Serotonin in the Hemolymph of Aplysia Are Modulated by Light/Dark Cycles and Sensitization Training.
J. Levenson, J. H. Byrne, and A. Eskin (1999)
J. Neurosci. 19, 8094-8103
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Entire Course and Distinct Phases of Day-Lasting Depression of Miniature EPSC Amplitudes in Cultured Purkinje Neurons.
M. Murashima and T. Hirano (1999)
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Expression and Branch-Specific Export of mRNA Are Regulated by Synapse Formation and Interaction with Specific Postsynaptic Targets.
S. Schacher, F. Wu, J. D. Panyko, Z.-Y. Sun, and D. Wang (1999)
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Memory Consolidation for Contextual and Auditory Fear Conditioning Is Dependent on Protein Synthesis, PKA, and MAP Kinase.
G. E. Schafe, N. V. Nadel, G. M. Sullivan, A. Harris, and J. E. LeDoux (1999)
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X. Liao, J. D. Gunstream, M. R. Lewin, R. T. Ambron, and E. T. Walters (1999)
J. Neurosci. 19, 1247-1256
   Abstract »    Full Text »    PDF »
Genes to remember.
C. Alberini (1999)
J. Exp. Biol. 202, 2887-2891
   Abstract »    PDF »
Serotonergic Neurons Differentially Modulate the Efficacy of Two Motor Neurons Innervating the Same Muscle Fibers in Aplysia.
L. E. Fox and P. E. Lloyd (1998)
J Neurophysiol 80, 647-655
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Requirement of Protein Synthesis for Group I mGluR-Mediated Induction of Epileptiform Discharges.
L. R. Merlin, P. J. Bergold, and R. K. S. Wong (1998)
J Neurophysiol 80, 989-993
   Abstract »    Full Text »    PDF »
Cellular Correlates of Long-Term Sensitization in Aplysia.
L. J. Cleary, W. L. Lee, and J. H. Byrne (1998)
J. Neurosci. 18, 5988-5998
   Abstract »    Full Text »    PDF »
Multiple Memory Processes Following Training That a Food Is Inedible in Aplysia.
D. Botzer, S. Markovich, and A. J. Susswein (1998)
Learn. Mem. 5, 204-219
   Abstract »    Full Text »
Differential Induction of Long-Term Synaptic Facilitation by Spaced and Massed Applications of Serotonin at Sensory Neuron Synapses of Aplysia californica.
J. Mauelshagen, C. M. Sherff, and T. J. Carew (1998)
Learn. Mem. 5, 246-256
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Substance P Modulates NMDA Responses and Causes Long-Term Protein Synthesis-Dependent Modulation of the Lamprey Locomotor Network.
D. Parker, W. Zhang, and S. Grillner (1998)
J. Neurosci. 18, 4800-4813
   Abstract »    Full Text »    PDF »
Binding of Serotonin to Receptors at Multiple Sites Is Required for Structural Plasticity Accompanying Long-Term Facilitation of Aplysia Sensorimotor Synapses.
Z.-Y. Sun and S. Schacher (1998)
J. Neurosci. 18, 3991-4000
   Abstract »    Full Text »    PDF »
Long-Term Changes in Excitability Induced by Protein Kinase C Activation in Aplysia Sensory Neurons.
F. Manseau, W. S. Sossin, and V. F. Castellucci (1998)
J Neurophysiol 79, 1210-1218
   Abstract »    Full Text »    PDF »
Long-Term Effects of Axotomy on Excitability and Growth of Isolated Aplysia Sensory Neurons in Cell Culture: Potential Role of cAMP.
S. S. Bedi, A. Salim, S. Chen, and D. L. Glanzman (1998)
J Neurophysiol 79, 1371-1383
   Abstract »    Full Text »    PDF »
Repeated pulses of serotonin required for long-term facilitation activate mitogen-activated protein kinase in sensory neurons of Aplysia.
D. Michael, K. C. Martin, R. Seger, M.-M. Ning, R. Baston, and E. R. Kandel (1998)
PNAS 95, 1864-1869
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Mapping of interneurons that contribute to food aversive conditioning in the slug brain..
T Kimura, H Suzuki, E Kono, and T Sekiguchi (1998)
Learn. Mem. 4, 376-388
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Protein synthesis-dependent memory and neuronal enhancement in Hermissenda are contingent on param