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The Journal of Neuroscience, March 29, 2006, 26(13):3524-3531; doi:10.1523/JNEUROSCI.3056-05.2006

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Behavioral/Systems/Cognitive
A 3-Synapse Positive Feedback Loop Regulates the Excitability of an Interneuron Critical for Sensitization in the Leech

Kevin M. Crisp¹ and Kenneth J. Muller^1,2

¹Department of Physiology and Biophysics, University of Miami School of Medicine, and ²Neuroscience Program, University of Miami, Miami, Florida 33136

Correspondence should be addressed to Kevin M. Crisp, Assistant Professor, Biology Department, Saint Olaf College, 1520 Saint Olaf Avenue, Northfield, MN 55057. Email: crisp{at}stolaf.edu

Sensitization of reflexive shortening in the leech has been linked to serotonin (5-HT)-induced changes in the excitability of a single interneuron, the S cell. This neuron is necessary for sensitization and complete dishabituation of reflexive shortening, during which it contributes to the sensory-motor reflex. The S cell does not contain 5-HT, which is released primarily from the Retzius (R) cells, whose firing enhances S-cell excitability. Here, we show that the S cell excites the R cells, mainly via a fast disynaptic pathway in which the first synapse is the electrical junction between the S cell and the coupling interneurons, and the second synapse is a glutamatergic synapse of the coupling interneurons onto the R cells. The S cell-triggered excitatory postsynaptic potential in the R cell diminishes and nearly disappears in elevated concentrations of divalent cations because the coupling interneurons become inexcitable under these conditions. Serotonin released from the R cells feeds back on the S cell and increases its excitability by activating a 5-HT₇-like receptor; 5-methoxytryptamine (5-MeOT; 10 µM) mimics the effects of 5-HT on S cell excitability, and effects of both 5-HT and 5-MeOT are blocked by pimozide (10 µM) and SB-269970 [(R)-3-(2-(2-(4-methylpiperidin-1-yl)-ethyl)pyrrolidine-1-sulfonyl)phenol] (5 µM). This feedback loop may be critical for the full expression of sensitization of reflexive shortening.

Key words: serotonin; serotonin receptor; electrical coupling; shortening; reflex; circuits

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Received July 23, 2005; revised Jan. 24, 2006; accepted Jan. 25, 2006.

Correspondence should be addressed to Kevin M. Crisp, Assistant Professor, Biology Department, Saint Olaf College, 1520 Saint Olaf Avenue, Northfield, MN 55057. Email: crisp{at}stolaf.edu

This article has been cited by other articles:

				B. D. Burrell and K. M. Crisp Serotonergic Modulation of Afterhyperpolarization in a Neuron That Contributes to Learning in the Leech J Neurophysiol, February 1, 2008; 99(2): 605 - 616. [Abstract] [Full Text] [PDF]

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