Presynaptic facilitation revisited: state and time dependence

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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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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]

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]

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.
[Abstract] [PDF]

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]

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]

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]

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]

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]

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]

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]

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]

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]

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]

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]

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]

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]