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Science 6 February 1987:
Vol. 235. no. 4789, pp. 685 - 687
DOI: 10.1126/science.2433766
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Articles

Science, Vol 235, Issue 4789, 685-687
Copyright © 1987 by American Association for the Advancement of Science

articles

Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons

KP Scholz and JH Byrne

A fundamental problem in the cellular analysis of learning and memory is the identification of the neuronal substrates of long-term information storage and their relation to short-term cellular alterations. In this report, biophysical correlates of long-term sensitization of a simple withdrawal reflex in the mollusc Aplysia were examined. A voltage-clamp analysis of the sensory neurons that control the reflex, 24 hours after sensitization training, revealed a significant reduction in net outward current. The results indicate that one mechanism for the storage of long-term sensitization is the regulation of membrane currents that influence the characteristics of the action potential and the excitability of individual neurons. The results also provide insights into the relation between short- and long-term sensitization in that the biophysical loci involved in the storage of long-term sensitization appear similar to those involved in short-term sensitization.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Long-Term Sensitization Training Produces Spike Narrowing in Aplysia Sensory Neurons.
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Regulation of Behavioral and Synaptic Plasticity by Serotonin Release within Local Modulatory Fields in the CNS of Aplysia.
S. Marinesco, N. Wickremasinghe, and T. J. Carew (2006)
J. Neurosci. 26, 12682-12693
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Non-Ocular Circadian Oscillators and Photoreceptors Modulate Long Term Memory Formation in Aplysia.
L. C. Lyons, O. Rawashdeh, and A. Eskin (2006)
J Biol Rhythms 21, 245-255
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Long-term sensitization training primes Aplysia for further learning.
E. G. Antzoulatos, M. L. Wainwright, L. J. Cleary, and J. H. Byrne (2006)
Learn. Mem. 13, 422-425
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Latent memory for sensitization in Aplysia..
G. T. Philips, E. I. Tzvetkova, S. Marinesco, and T. J. Carew (2006)
Learn. Mem. 13, 224-229
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Evidence That Long-Term Hyperexcitability of the Sensory Neuron Soma Induced by Nerve Injury in Aplysia Is Adaptive.
X. Gasull, X. Liao, M. F. Dulin, C. Phelps, and E. T. Walters (2005)
J Neurophysiol 94, 2218-2230
   Abstract »    Full Text »    PDF »
Memory-Like Alterations in Aplysia Axons after Nerve Injury or Localized Depolarization.
R. M. S. Weragoda, E. Ferrer, and E. T. Walters (2004)
J. Neurosci. 24, 10393-10401
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Coregulation of Glutamate Uptake and Long-Term Sensitization in Aplysia.
O. Khabour, J. Levenson, L. C. Lyons, L. S. Kategaya, J. Chin, J. H. Byrne, and A. Eskin (2004)
J. Neurosci. 24, 8829-8837
   Abstract »    Full Text »    PDF »
Serotonergic Modulation in Aplysia. I. Distributed Serotonergic Network Persistently Activated by Sensitizing Stimuli.
S. Marinesco, K. E. Kolkman, and T. J. Carew (2004)
J Neurophysiol 92, 2468-2486
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Serotonergic Modulation in Aplysia. II. Cellular and Behavioral Consequences of Increased Serotonergic Tone.
S. Marinesco, N. Wickremasinghe, K. E. Kolkman, and T. J. Carew (2004)
J Neurophysiol 92, 2487-2496
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Dissociation of Morphological and Physiological Changes Associated With Long-Term Memory in Aplysia.
M. L. Wainwright, J. H. Byrne, and L. J. Cleary (2004)
J Neurophysiol 92, 2628-2632
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Long-Term Memory Requires PolyADP-ribosylation.
M. Cohen-Armon, L. Visochek, A. Katzoff, D. Levitan, A. J. Susswein, R. Klein, M. Valbrun, and J. H. Schwartz (2004)
Science 304, 1820-1822
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Intermediate-Term Memory for Site-Specific Sensitization in Aplysia Is Maintained by Persistent Activation of Protein Kinase C.
M. A. Sutton, M. W. Bagnall, S. K. Sharma, J. Shobe, and T. J. Carew (2004)
J. Neurosci. 24, 3600-3609
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Neural Circuit of Tail-Elicited Siphon Withdrawal in Aplysia. I. Differential Lateralization of Sensitization and Dishabituation.
A. S. Bristol, M. A. Sutton, and T. J. Carew (2004)
J Neurophysiol 91, 666-677
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Neural Circuit of Tail-Elicited Siphon Withdrawal in Aplysia. II. Role of Gated Inhibition in Differential Lateralization of Sensitization and Dishabituation.
A. S. Bristol, S. Marinesco, and T. J. Carew (2004)
J Neurophysiol 91, 678-692
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Circadian modulation of long-term sensitization in Aplysia.
R. I. Fernandez, L. C. Lyons, J. Levenson, O. Khabour, and A. Eskin (2003)
PNAS 100, 14415-14420
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Long-Term Plasticity of Intrinsic Excitability: Learning Rules and Mechanisms.
G. Daoudal and D. Debanne (2003)
Learn. Mem. 10, 456-465
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Burst-Induced Synaptic Depression and Its Modulation Contribute to Information Transfer at Aplysia Sensorimotor Synapses: Empirical and Computational Analyses.
G. A. Phares, E. G. Antzoulatos, D. A. Baxter, and J. H. Byrne (2003)
J. Neurosci. 23, 8392-8401
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Multiple Serotonergic Mechanisms Contributing to Sensitization in Aplysia: Evidence of Diverse Serotonin Receptor Subtypes.
D. Barbas, L. DesGroseillers, V. F. Castellucci, T. J. Carew, and S. Marinesco (2003)
Learn. Mem. 10, 373-386
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Quantitation of Contacts Among Sensory, Motor, and Serotonergic Neurons in the Pedal Ganglion of Aplysia.
H. Zhang, M. Wainwright, J. H. Byrne, and L. J. Cleary (2003)
Learn. Mem. 10, 387-393
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Localized Neuronal Outgrowth Induced by Long-Term Sensitization Training in Aplysia.
M. L. Wainwright, H. Zhang, J. H. Byrne, and L. J. Cleary (2002)
J. Neurosci. 22, 4132-4141
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Long-Term Alteration of S-Type Potassium Current and Passive Membrane Properties in Aplysia Sensory Neurons Following Axotomy.
M. A. Ungless, X. Gasull, and E. T. Walters (2002)
J Neurophysiol 87, 2408-2420
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Serotonin Release Evoked by Tail Nerve Stimulation in the CNS of Aplysia: Characterization and Relationship to Heterosynaptic Plasticity.
S. Marinesco and T. J. Carew (2002)
J. Neurosci. 22, 2299-2312
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Interaction between Amount and Pattern of Training in the Induction of Intermediate- and Long-Term Memory for Sensitization in Aplysia.
M. A. Sutton, J. Ide, S. E. Masters, and T. J. Carew (2002)
Learn. Mem. 9, 29-40
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Axonal Rejoining Inhibits Injury-Induced Long-Term Changes in Aplysia Sensory Neurons In Vitro.
S. S. Bedi and D. L. Glanzman (2001)
J. Neurosci. 21, 9667-9677
   Abstract »    Full Text »    PDF »
Limited Contributions of Serotonin to Long-Term Hyperexcitability of Aplysia Sensory Neurons.
X. Liao, C. G. Brou, and E. T. Walters (1999)
J Neurophysiol 82, 3223-3235
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
Activation of Protein Kinase A Contributes to the Expression But Not the Induction of Long-Term Hyperexcitability Caused by Axotomy of Aplysia Sensory Neurons.
X. Liao, J. D. Gunstream, M. R. Lewin, R. T. Ambron, and E. T. Walters (1999)
J. Neurosci. 19, 1247-1256
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Separate Effects of a Classical Conditioning Procedure on Respiratory Pumping, Swimming, and Inking in Aplysia fasciata.
M. Levy and A. J. Susswein (1999)
Learn. Mem. 6, 21-36
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Cellular Correlates of Long-Term Sensitization in Aplysia.
L. J. Cleary, W. L. Lee, and J. H. Byrne (1998)
J. Neurosci. 18, 5988-5998
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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 »
Identification of specific mRNAs affected by treatments producing long-term facilitation in Aplysia..
R E Zwartjes, H West, S Hattar, X Ren, F Noel, M Nunez-Regueiro, K MacPhee, R Homayouni, M T Crow, J H Byrne, et al. (1998)
Learn. Mem. 4, 478-495
   Abstract »    PDF »
Modulation of a cAMP/Protein Kinase A Cascade by Protein Kinase C in Sensory Neurons of Aplysia.
S. Sugita, D. A. Baxter, and J. H. Byrne (1997)
J. Neurosci. 17, 7237-7244
   Abstract »    Full Text »    PDF »
A Developmental Gene (Tolloid/BMP-1) Is Regulated in Aplysia Neurons by Treatments that Induce Long-Term Sensitization.
Q.-R Liu, S. Hattar, S. Endo, K. MacPhee, H. Zhang, L. J. Cleary, J. H. Byrne, and A. Eskin (1997)
J. Neurosci. 17, 755-764
   Abstract »    Full Text »    PDF »
Prostaglandins Suppress an Outward Potassium Current in Embryonic Rat Sensory Neurons.
G. D. Nicol, M. R. Vasko, and A. R. Evans (1997)
J Neurophysiol 77, 167-176
   Abstract »    Full Text »    PDF »
Nonassociative and associative modification of head-waving produced by aversive tentacular stimuli in Aplysia..
K K Fitzgerald, C A Takacs, and T J Carew (1997)
Learn. Mem. 3, 366-375
   Abstract »    PDF »
An autonomous kinase generated during long-term facilitation in Aplysia is related to the Ca(2+)-independent protein kinase C Apl II..
W S Sossin (1997)
Learn. Mem. 3, 389-401
   Abstract »    PDF »
Toward a molecular definition of long-term memory storage.
C. H. Bailey, D. Bartsch, and E. R. Kandel (1996)
PNAS 93, 13445-13452
   Abstract »    Full Text »    PDF »
Trace Eyeblink Conditioning Increases CA1 Excitability in a Transient and Learning-Specific Manner.
J. R. Moyer Jr., L. T. Thompson, and J. F. Disterhoft (1996)
J. Neurosci. 16, 5536-5546
   Abstract »    Full Text »    PDF »
Site Specificity of Short-Term and Long-Term Habituation in the Tail-Elicited Siphon Withdrawal Reflex of Aplysia.
M. Stopfer, X. Chen, Y.-T. Tai, G. S. Huang, and T. J. Carew (1996)
J. Neurosci. 16, 4923-4932
   Abstract »    Full Text »    PDF »
Heterosynaptic Facilitation of Tail Sensory Neuron Synaptic Transmission during Habituation in Tail-Induced Tail and Siphon Withdrawal Reflexes of Aplysia.
M. Stopfer and T. J. Carew (1996)
J. Neurosci. 16, 4933-4948
   Abstract »    Full Text »    PDF »
Persistent activation of protein kinase C during the development of long-term facilitation in Aplysia..
W S Sossin, T C Sacktor, and J H Schwartz (1994)
Learn. Mem. 1, 189-202
   Abstract »    PDF »
Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons.
N. Emptage and T. Carew (1993)
Science 262, 253-256
   Abstract »    PDF »
Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons.
B. Bacskai, B Hochner, M Mahaut-Smith, Adams SR, B. Kaang, E. Kandel, and R. Tsien (1993)
Science 260, 222-226
   Abstract »    PDF »
Pharmacological dissociation of modulatory effects of serotonin in Aplysia sensory neurons.
A. Mercer, N. Emptage, and T. Carew (1991)
Science 254, 1811-1813
   Abstract »    PDF »
Similar neuronal alterations induced by axonal injury and learning in Aplysia.
E. Walters, H Alizadeh, and G. Castro (1991)
Science 253, 797-799
   Abstract »    PDF »
Identification of a peptide specific for Aplysia sensory neurons by PCR-based differential screening.
J. Brunet, E Shapiro, S. Foster, E. Kandel, and Y Iino (1991)
Science 252, 856-859
   Abstract »    PDF »
Long-term synaptic changes produced by a cellular analog of classical conditioning in Aplysia.
D. Buonomano and J. Byrne (1990)
Science 249, 420-423
   Abstract »    PDF »
Long-term Facilitation in Aplysia: Persistent Phosphorylation and Structural Changes.
S. Schacher, D. Glanzman, A. Barzilai, P. Dash, S.G.N. Grant, F. Keller, M. Mayford, and E.R. Kandel (1990)
Cold Spring Harb Symp Quant Biol 55, 187-202
   Abstract »    PDF »
Intracellular injection of cAMP induces a long-term reduction of neuronal K+ currents.
K. Scholz and J. Byrne (1988)
Science 240, 1664-1666
   Abstract »    PDF »
cAMP evokes long-term facilitation in Aplysia sensory neurons that requires new protein synthesis.
S Schacher, V. Castellucci, and E. Kandel (1988)
Science 240, 1667-1669
   Abstract »    PDF »
Long-term regulation of neuronal high-affinity glutamate and glutamine uptake in Aplysia.
J. Levenson, S. Endo, L. S. Kategaya, R. I. Fernandez, D. G. Brabham, J. Chin, J. H. Byrne, and A. Eskin (2000)
PNAS 97, 12858-12863
   Abstract »    Full Text »    PDF »


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