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The Journal of Neuroscience, February 15, 2006, 26(7):2010-2021; doi:10.1523/JNEUROSCI.2599-05.2006

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Behavioral/Systems/Cognitive
Serotonergic Enhancement of a 4-AP-Sensitive Current Mediates the Synaptic Depression Phase of Spike Timing-Dependent Neuromodulation

Akira Sakurai,¹ Naïm R. Darghouth,^1,2 Robert J. Butera,² and Paul S. Katz¹

¹Department of Biology, Georgia State University, Atlanta, Georgia 30302-4010, and ²School of Electrical and Computer Engineering, Georgia Institute of Technology, Atlanta, Georgia 30332-0160

Correspondence should be addressed to Akira Sakurai, Department of Biology, Georgia State University, P.O. Box 4010, Atlanta, GA 30302-4010. Email: akira{at}gsu.edu

The mechanism underlying spike timing-dependent neuromodulation (STDN) was investigated in the opisthobranch mollusc Tritonia diomedea. The serotonergic dorsal swim interneurons (DSIs) dynamically modulated the synaptic output of ventral swim interneuron B (VSI); immediately after DSI stimulation, there was a potentiation of VSI synaptic strength followed by a longer-lasting synaptic depression. The potentiation phase of STDN was unaffected by spike broadening produced by the potassium channel blocker 4-aminopyridine (4-AP). In contrast, the depression phase was eliminated by 4-AP. Bath-applied serotonin (5-HT) decreased VSI spike duration and increased the magnitude of the A-current (I_A), a voltage-dependent, transient, outward current. 4-AP preferentially blocked I_A and prevented the spike narrowing caused by 5-HT, uncovering the full extent of 5-HT-induced synaptic potentiation. A consistent correlation was observed between I_A and spike duration, but the correlation between synaptic strength and spike duration differed between preparations. Conductance-based simulations showed that the magnitude of A-current conductance could affect spike duration and gave an estimation of the change needed to produce spike narrowing. An artificial I_A introduced into the VSI in the presence of 4-AP by means of the dynamic-clamp technique restored spike duration and gave a further approximation of the magnitude of modulation needed for spike narrowing. Together, these results suggest a mechanism for STDN: the DSIs release 5-HT, which causes a spike duration-independent enhancement of synaptic strength and a longer-lasting enhancement of I_A that narrows the VSI spike and hence decreases VSI synaptic strength. Thus, STDN arises from the dynamics of independent intracellular signaling events.

Key words: spike-narrowing; serotonin; opisthobranch mollusc; A-current; Tritonia diomedea; dynamic clamp

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Received June 23, 2005; revised Jan. 5, 2006; accepted Jan. 6, 2006.

Correspondence should be addressed to Akira Sakurai, Department of Biology, Georgia State University, P.O. Box 4010, Atlanta, GA 30302-4010. Email: akira{at}gsu.edu

This article has been cited by other articles:

				A. Sakurai and P. S. Katz State-, Timing-, and Pattern-Dependent Neuromodulation of Synaptic Strength by a Serotonergic Interneuron J. Neurosci., January 7, 2009; 29(1): 268 - 279. [Abstract] [Full Text] [PDF]

				K. Sasaki, J. Jing, M. R. Due, and K. R. Weiss An Input-Representing Interneuron Regulates Spike Timing and Thereby Phase Switching in a Motor Network J. Neurosci., February 20, 2008; 28(8): 1916 - 1928. [Abstract] [Full Text] [PDF]

				A. Sakurai, R. J. Calin-Jageman, and P. S. Katz Potentiation Phase of Spike Timing-Dependent Neuromodulation by a Serotonergic Interneuron Involves an Increase in the Fraction of Transmitter Release J Neurophysiol, October 1, 2007; 98(4): 1975 - 1987. [Abstract] [Full Text] [PDF]

				E. G. Antzoulatos and J. H. Byrne Long-Term Sensitization Training Produces Spike Narrowing in Aplysia Sensory Neurons J. Neurosci., January 17, 2007; 27(3): 676 - 683. [Abstract] [Full Text] [PDF]

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