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Journal of Neuroscience, Vol 16, 425-435, Copyright © 1996 by Society for Neuroscience


ARTICLE

Presynaptic facilitation revisited: state and time dependence

JH Byrne and ER Kandel
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston 77030, USA.

The mechanisms underlying short-term presynaptic facilitation, the enhancement of transmitter release from sensory neurons in Aplysia, induced by serotonin (5-HT), can be divided into two categories: (1) changes in ionic conductances leading to spike broadening and enhancement of Ca2+ influx; and (2) actions on the machinery for transmitter release that are independent of spike broadening and the resulting increases in Ca2+ influx. Spike broadening and the associated enhancement of excitability are induced by the modulation of K+ conductances in the sensory neuron. The cellular mechanisms that contribute to the enhancement of release that is independent of spike broadening are not known and may involve vesicle mobilization or other steps in exocytotic release. These two facilitatory actions of 5-HT are mediated by at least two second-messenger-activated protein kinase systems, protein kinase A (PKA) and protein kinase C (PKC). These two second-messenger cascades overlap in their contributions to synaptic facilitation. However, their relative contributions to enhancement of transmitter release are not simply synergistic but are state- and time- dependent. The state dependence is a reflection of the synapse's previous history of activity. When the synapse is rested (and not depressed), a brief pulse of 5-HT (lasting from 10 sec to 5 min) produces its actions primarily through PKA via both spike broadening- dependent and -independent mechanisms. The broadening primarily involves the modulation of a voltage-dependent K+ current, IKV, with a small contribution by a voltage-independent K+ current, IKS. By contrast, the enhancement of excitability is mediated primarily by the modulation of IKS. As the synapse becomes depressed with repeated activity, the contribution of PKC becomes progressively more important. As is the case with PKA, PKC produces its action both by broadening the spike via modulation of IKV and by a spike broadening-independent mechanism. In addition to being state-dependent, the mechanisms of facilitation are time-dependent. There are differences in the response to 5-HT when it is given briefly to produce short-term facilitation or when the exposure is prolonged. When exposure is brief (< or = 5 min), PKA dominates. When exposure is prolonged (10-20 min), PKC becomes dominant as it is with depressed synapses. Thus, synaptic plasticity appears to be expressed in several overlapping time domains, and the transition between very short-term facilitation and various intermediate duration phases seems to involve interactive processes between the kinases.


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Serotonin Stimulates Phosphorylation of Aplysia Synapsin and Alters Its Subcellular Distribution in Sensory Neurons
J. Neurosci., July 1, 2002; 22(13): 5412 - 5422.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
M. A. Ungless, X. Gasull, and E. T. Walters
Long-Term Alteration of S-Type Potassium Current and Passive Membrane Properties in Aplysia Sensory Neurons Following Axotomy
J Neurophysiol, May 1, 2002; 87(5): 2408 - 2420.
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J. Neurophysiol.Home page
L. E. Fox and P. E. Lloyd
Mechanisms Involved in Persistent Facilitation of Neuromuscular Synapses in Aplysia
J Neurophysiol, April 1, 2002; 87(4): 2018 - 2030.
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J. Neurosci.Home page
S. Marinesco and T. J. Carew
Serotonin Release Evoked by Tail Nerve Stimulation in the CNS of Aplysia: Characterization and Relationship to Heterosynaptic Plasticity
J. Neurosci., March 15, 2002; 22(6): 2299 - 2312.
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J. Neurosci.Home page
T. D. Gover, X.-Y. Jiang, and T. W. Abrams
Persistent, Exocytosis-Independent Silencing of Release Sites Underlies Homosynaptic Depression at Sensory Synapses in Aplysia
J. Neurosci., March 1, 2002; 22(5): 1942 - 1955.
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J. Neurophysiol.Home page
L. E. Fox and P. E. Lloyd
Evidence That Post-Tetanic Potentiation Is Mediated by Neuropeptide Release in Aplysia
J Neurophysiol, December 1, 2001; 86(6): 2845 - 2855.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
A. S. Bristol, T. M. Fischer, and T. J. Carew
Combined Effects of Intrinsic Facilitation and Modulatory Inhibition of Identified Interneurons in the Siphon Withdrawal Circuitry of Aplysia
J. Neurosci., November 15, 2001; 21(22): 8990 - 9000.
[Abstract] [Full Text] [PDF]


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ScienceHome page
E. R. Kandel
The Molecular Biology of Memory Storage: A Dialogue Between Genes and Synapses
Science, November 2, 2001; 294(5544): 1030 - 1038.
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J. Neurosci.Home page
X.-S. Wu and L.-G. Wu
Protein Kinase C Increases the Apparent Affinity of the Release Machinery to Ca2+ by Enhancing the Release Machinery Downstream of the Ca2+ Sensor
J. Neurosci., October 15, 2001; 21(20): 7928 - 7936.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
R. A Chitwood, Q. Li, and D. L Glanzman
Serotonin facilitates AMPA-type responses in isolated siphon motor neurons of Aplysia in culture
J. Physiol., July 15, 2001; 534(2): 501 - 510.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
A. L. Purcell and T. J. Carew
Modulation of Excitability in Aplysia Tail Sensory Neurons by Tyrosine Kinases
J Neurophysiol, June 1, 2001; 85(6): 2398 - 2411.
[Abstract] [Full Text] [PDF]


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J. Appl. Physiol.Home page
G. S. Mitchell, T. L. Baker, S. A. Nanda, D. D. Fuller, A. G. Zabka, B. A. Hodgeman, R. W. Bavis, K. J. Mack, and E. B. Olson Jr.
Physiological and Genomic Consequences of Intermittent Hypoxia: Invited Review: Intermittent hypoxia and respiratory plasticity
J Appl Physiol, June 1, 2001; 90(6): 2466 - 2475.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
W.-D. Yao and C.-F. Wu
Distinct Roles of CaMKII and PKA in Regulation of Firing Patterns and K+ Currents in Drosophila Neurons
J Neurophysiol, April 1, 2001; 85(4): 1384 - 1394.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
J. W. Barclay and R. M. Robertson
Enhancement of Short-Term Synaptic Plasticity by Prior Environmental Stress
J Neurophysiol, March 1, 2001; 85(3): 1332 - 1335.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
J. H. Schaffhausen, T. M. Fischer, and T. J. Carew
Contirbution of Postsynaptic Ca2+ to the Induction of Posttetanic Potentiation in the Neural Circuit for Siphon Withdrawal in Aplysia
J. Neurosci., March 1, 2001; 21(5): 1739 - 1749.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
F. Manseau, X. Fan, T. Hueftlein, W. S. Sossin, and V. F. Castellucci
Ca2+-Independent Protein Kinase C Apl II Mediates the Serotonin-Induced Facilitation at Depressed Aplysia Sensorimotor Synapses
J. Neurosci., February 15, 2001; 21(4): 1247 - 1256.
[Abstract] [Full Text] [PDF]


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J. Exp. Biol.Home page
E Walters, P Illich, J Weeks, and M Lewin
Defensive responses of larval Manduca sexta and their sensitization by noxious stimuli in the laboratory and field
J. Exp. Biol., January 2, 2001; 204(3): 457 - 469.
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Proc. Natl. Acad. Sci. USAHome page
T. Sakaba and E. Neher
Preferential potentiation of fast-releasing synaptic vesicles by cAMP at the calyx of Held
PNAS, December 22, 2000; (2000) 21541098.
[Abstract] [Full Text]


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J. Neurosci.Home page
M. Yoshihara, K. Suzuki, and Y. Kidokoro
Two Independent Pathways Mediated by cAMP and Protein Kinase A Enhance Spontaneous Transmitter Release at Drosophila Neuromuscular Junctions
J. Neurosci., November 15, 2000; 20(22): 8315 - 8322.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
C. H. Bailey, M. Giustetto, H. Zhu, M. Chen, and E. R. Kandel
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
PNAS, October 10, 2000; 97(21): 11581 - 11586.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
E. J. Weeber, C. M. Atkins, J. C. Selcher, A. W. Varga, B. Mirnikjoo, R. Paylor, M. Leitges, and J. D. Sweatt
A Role for the beta Isoform of Protein Kinase C in Fear Conditioning
J. Neurosci., August 15, 2000; 20(16): 5906 - 5914.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
J. J. Renger, A. Ueda, H. L. Atwood, C. K. Govind, and C.-F. Wu
Role of cAMP Cascade in Synaptic Stability and Plasticity: Ultrastructural and Physiological Analyses of Individual Synaptic Boutons in Drosophila Memory Mutants
J. Neurosci., June 1, 2000; 20(11): 3980 - 3992.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
R. A. Satterlie, T. P. Norekian, and T. J. Pirtle
Serotonin-Induced Spike Narrowing in a Locomotor Pattern Generator Permits Increases in Cycle Frequency During Accelerations
J Neurophysiol, April 1, 2000; 83(4): 2163 - 2170.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
D. Lee and D. K. O'Dowd
cAMP-Dependent Plasticity at Excitatory Cholinergic Synapses in Drosophila Neurons: Alterations in the Memory Mutant Dunce
J. Neurosci., March 15, 2000; 20(6): 2104 - 2111.
[Abstract] [Full Text] [PDF]


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J. Appl. Physiol.Home page
M. E. Crider and R. L. Cooper
Differential facilitation of high- and low-output nerve terminals from a single motoneuron
J Appl Physiol, March 1, 2000; 88(3): 987 - 996.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
L. E. Fox and P. E. Lloyd
Role of cAMP in the Short-Term Modulation of a Neuromuscular System in Aplysia
J Neurophysiol, March 1, 2000; 83(3): 1567 - 1579.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
S. C. Rosen, M. W. Miller, C. G. Evans, E. C. Cropper, and I. Kupfermann
Diverse Synaptic Connections Between Peptidergic Radula Mechanoafferent Neurons and Neurons in the Feeding System of Aplysia
J Neurophysiol, March 1, 2000; 83(3): 1605 - 1620.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
S. C. Rosen, M. W. Miller, E. C. Cropper, and I. Kupfermann
Outputs of Radula Mechanoafferent Neurons in Aplysia are Modulated by Motor Neurons, Interneurons, and Sensory Neurons
J Neurophysiol, March 1, 2000; 83(3): 1621 - 1636.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
C. C. Gandhi and L. D. Matzel
Modulation of Presynaptic Action Potential Kinetics Underlies Synaptic Facilitation of Type B Photoreceptors after Associative Conditioning in Hermissenda
J. Neurosci., March 1, 2000; 20(5): 2022 - 2035.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
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
Activation of a heterologously expressed octopamine receptor coupled only to adenylyl cyclase produces all the features of presynaptic facilitation in Aplysia sensory neurons
PNAS, February 15, 2000; 97(4): 1829 - 1834.
[Abstract] [Full Text] [PDF]



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