Potentiation Phase of Spike Timing-Dependent Neuromodulation by a Serotonergic Interneuron Involves an Increase in the Fraction of Transmitter Release

Author:

Sakurai Akira,Calin-Jageman Robert J.,Katz Paul S.

Abstract

In the mollusk, Tritonia diomedea, the serotonergic dorsal swim interneuron (DSI) produces spike timing-dependent neuromodulation (STDN) of the synaptic output of ventral swim interneuron B (VSI) resulting in a biphasic, bidirectional change of synaptic strength characterized by a rapid heterosynaptic potentiation followed by a more prolonged heterosynaptic depression. This study examined the mechanism underlying the potentiation phase of STDN. In the presence of 4-aminopyridine, which blocks the depression phase and enhances transmitter release from VSI, rapidly stimulating VSI led to a steady-state level of transmitter depletion during which potentiation by DSI or serotonin (5-HT) was eliminated. Cumulative plots of excitatory postsynaptic currents were used to estimate changes in the size and replenishment rate of the readily releasable pool (RRP) and the fraction of release. 5-HT application increased transmitter release without altering replenishment rate. The magnitude of 5-HT-evoked potentiation correlated with the increase in the fraction of release. A phenomenological model of the synapse further supported the hypothesis that 5-HT-induced potentiation was caused by an increase in the fraction of release and correctly predicted no change in frequency facilitation. A dynamic version of the model correctly predicted the effect of DSI stimulation under a variety of conditions. Finally, depletion of internal Ca2+ stores with cyclopiazonic acid showed that Ca2+ from internal stores is necessary for the 5-HT-induced potentiation. The data indicate that 5-HT released from DSI increases the fraction of the RRP discharged during VSI action potentials using a mechanism that involves Ca2+ extrusion from internal stores, resulting in time- and state-dependent neuromodulation.

Publisher

American Physiological Society

Subject

Physiology,General Neuroscience

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1. Homology and Variation in Neural Control of Swimming in Nudipleura Mollusks;Hikaku seiri seikagaku(Comparative Physiology and Biochemistry);2018-08-01

2. Use of the Aplysia feeding network to study repetition priming of an episodic behavior;Journal of Neurophysiology;2017-09-01

3. Nonassociative Learning in Invertebrates;Cold Spring Harbor Perspectives in Biology;2015-02-26

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