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Journal of Neuroscience, Vol 14, 368-383, Copyright © 1994 by Society for Neuroscience
Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor neuron synapses in isolated cell culture
LS Eliot, RD Hawkins, ER Kandel and S Schacher
Center for Neurobiology and Behavior, College of Physicians and Surgeons of Columbia University, New York, New York 10032.
Synapses made by Aplysia sensory neurons onto motor- and interneuron
followers in the intact nervous system exhibit an associative form of
synaptic facilitation that is thought to contribute to classical
conditioning of the animal's gill and siphon withdrawal reflex (Hawkins et
al., 1983; Walters and Byrne, 1983). Here we demonstrate that a similar
associative facilitation can be induced between individual sensory and
motor neurons isolated in culture. Pairing tetanic stimulation with either
of two facilitatory transmitters, 5-HT or small cardioactive peptide,
considerably prolongs facilitation compared to either tetanus or
transmitter alone. When corrected for the depression that occurs simply in
response to low-frequency testing, the facilitation produced by one pairing
trial does not decay for more than 20 min after training. This facilitation
requires the temporal pairing (0.5 sec forward interstimulus interval) of
the two stimuli, tetanus and 5-HT. Delivering the same two stimuli in an
unpaired fashion (1 min forward interval) fails to produce the long-lasting
effect. Measurements of spontaneous transmitter release during either
paired or unpaired training reveal no changes in unitary mEPSP or mEPSC
("mini") amplitude, indicating that the facilitation involves a presynaptic
mechanism. While both forms of training dramatically increase the initial
frequency of spontaneous release, mini frequency does not remain elevated
as long as the evoked EPSP following paired training, nor does paired
training specifically enhance spontaneous release frequency.
Pairing-specific facilitation was not blocked by the protein kinase C
inhibitor H7. In contrast, the same training procedure produced
pairing-specific increases of sensory neuron excitability and action
potential width, suggesting that cAMP-mediated processes are involved in
the paired effect. Although Ca2+ influx is necessary for the associative
effect (Abrams, 1985), we find that the facilitation does not require
influx through L-type voltage-gated Ca2+ channels, since the effect was not
blocked by the dihydropyridine antagonist nitrendipine. Together, these
findings indicate that the mechanism underlying associative,
activity-dependent facilitation is intrinsic to the sensory neuron synapse,
that it is presynaptically mediated by processes unique to evoked synaptic
transmission, and that it appears to involve a pairing-specific broadening
of the presynaptic action potential, allowing enhanced Ca2+ influx through
the dihydropyridine- insensitive channels responsible for release.
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