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Science 20 December 1991:
Vol. 254. no. 5039, pp. 1811 - 1813
DOI: 10.1126/science.1662413
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Articles

Science, Vol 254, Issue 5039, 1811-1813
Copyright © 1991 by American Association for the Advancement of Science

articles

Pharmacological dissociation of modulatory effects of serotonin in Aplysia sensory neurons

AR Mercer, NJ Emptage, and TJ Carew

Yale University, Department of Psychology, New Haven, CT 06520.

In the mollusk Aplysia the neurotransmitter serotonin (5HT) has a fundamental modulatory role in several forms of learning and memory that involve an increase in the efficacy of synaptic transmission between tail sensory neurons (SNs) and motor neurons. The classical 5HT antagonist cyproheptadine (CYP) permits dissociation of three forms of serotonergic modulation in these SNs: (i) CYP reversibly blocks spike-broadening induced either by exogenous application of 5HT or by sensitizing stimulation of a tail nerve. (ii) CYP does not block 5HT-induced or tail input-induced increases in SN somatic excitability. (iii) Concomitant with its block of spike-broadening, CYP reversibly blocks 5HT-induced facilitation of synaptic transmission from SNs. These results suggest that endogenously released 5HT may act at different receptor subtypes that are coupled to different forms of neuromodulation in tail SNs of Aplysia.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
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
   Abstract »    Full Text »    PDF »
Serotonin Receptor Antagonists Discriminate Between PKA- and PKC-Mediated Plasticity in Aplysia Sensory Neurons.
B. Dumitriu, J. E. Cohen, Q. Wan, A. M. Negroiu, and T. W. Abrams (2006)
J Neurophysiol 95, 2713-2720
   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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
Parallel somatic and synaptic processing in the induction of intermediate-term and long-term synaptic facilitation in Aplysia.
C. M. Sherff and T. J. Carew (2004)
PNAS 101, 7463-7468
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
Spike Timing-Dependent Serotonergic Neuromodulation of Synaptic Strength Intrinsic to a Central Pattern Generator Circuit.
A. Sakurai and P. S. Katz (2003)
J. Neurosci. 23, 10745-10755
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
Evolution of learning in three aplysiid species: differences in heterosynaptic plasticity contrast with conservation in serotonergic pathways.
S. Marinesco, K. L Duran, and W. G Wright (2003)
J. Physiol. 550, 241-253
   Abstract »    Full Text »    PDF »
Pharmacological Characterization of an Adenylyl Cyclase-Coupled 5-HT Receptor in Aplysia: Comparison With Mammalian 5-HT Receptors.
J. E. Cohen, C. U. Onyike, V. L. McElroy, A. H. Lin, and T. W. Abrams (2003)
J Neurophysiol 89, 1440-1455
   Abstract »    Full Text »    PDF »
Behavioral, Cellular, and Molecular Analysis of Memory in Aplysia I: Intermediate-Term Memory.
M. A. Sutton and T. J. Carew (2002)
Integr. Comp. Biol. 42, 725-735
   Abstract »    Full Text »    PDF »
Mechanisms Involved in Persistent Facilitation of Neuromuscular Synapses in Aplysia.
L. E. Fox and P. E. Lloyd (2002)
J Neurophysiol 87, 2018-2030
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
Combined Effects of Intrinsic Facilitation and Modulatory Inhibition of Identified Interneurons in the Siphon Withdrawal Circuitry of Aplysia.
A. S. Bristol, T. M. Fischer, and T. J. Carew (2001)
J. Neurosci. 21, 8990-9000
   Abstract »    Full Text »    PDF »
Activation of a heterologously expressed octopamine receptor coupled only to adenylyl cyclase produces all the features of presynaptic facilitation in Aplysia sensory neurons.
D.-J. Chang, X.-C. Li, Y.-S. Lee, H.-K. Kim, U. S. Kim, N. J. Cho, X. Lo, K. R. Weiss, E. R. Kandel, and B.-K. Kaang (2000)
PNAS 97, 1829-1834
   Abstract »    Full Text »    PDF »
Computational Model of the Serotonergic Modulation of Sensory Neurons in Aplysia.
D. A. Baxter, C. C. Canavier, J. W. Clark Jr., and J. H. Byrne (1999)
J Neurophysiol 82, 2914-2935
   Abstract »    Full Text »    PDF »
Developmental Dissociation of Serotonin-Induced Spike Broadening and Synaptic Facilitation in Aplysia Sensory Neurons.
L. L. Stark and T. J. Carew (1999)
J. Neurosci. 19, 334-346
   Abstract »    Full Text »    PDF »
Cloning and Functional Expression of an Aplysia 5-HT Receptor Negatively Coupled to Adenylate Cyclase.
A. Angers, M. V. Storozhuk, T. Duchaine, V. F. Castellucci, and L. DesGroseillers (1998)
J. Neurosci. 18, 5586-5593
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »
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 »
Developmental emergence of different forms of neuromodulation in Aplysia sensory neurons.
E. A. Marcus and T. J. Carew (1998)
PNAS 95, 4726-4731
   Abstract »    Full Text »    PDF »
Conopressin Affects Excitability, Firing, and Action Potential Shape Through Stimulation of Transient and Persistent Inward Currents in Mulluscan Neurons.
P. F. van Soest and K. S. Kits (1998)
J Neurophysiol 79, 1619-1632
   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 »
Role of Calcium-Calmodulin-Dependent Protein Kinase II in Modulation of Sensorimotor Synapses in Aplysia.
K. Nakanishi, F. Zhang, D. A. Baxter, A. Eskin, and J. H. Byrne (1997)
J Neurophysiol 78, 409-416
   Abstract »    Full Text »    PDF »
Differential Distribution of Functional Receptors for Neuromodulators Evoking Short-Term Heterosynaptic Plasticity in Aplysia Sensory Neurons.
Z.-Y. Sun, B. Kauderer, and S. Schacher (1996)
J. Neurosci. 16, 7540-7549
   Abstract »    Full Text »    PDF »
Dynamics of Induction and Expression of Long-Term Synaptic Facilitation in Aplysia.
J. Mauelshagen, G. R. Parker, and T. J. Carew (1996)
J. Neurosci. 16, 7099-7108
   Abstract »    Full Text »    PDF »
Direct comparison of serotonin effects on siphon versus tail sensory neurons in Aplysia..
W G Wright and D Kirschman (1995)
Learn. Mem. 2, 178-184
   Abstract »    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 »
Activity-dependent enhancement of presynaptic facilitation provides a cellular mechanism for the temporal specificity of classical conditioning in Aplysia..
G A Clark, R D Hawkins, and E R Kandel (1994)
Learn. Mem. 1, 243-257
   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 »


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