A 3-synapse positive feedback loop regulates the excitability of an interneuron critical for sensitization in the leech

Kevin M. Crisp, Kenneth J Muller

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)3524-3531
Number of pages8
JournalJournal of Neuroscience
Volume26
Issue number13
DOIs
StatePublished - Mar 29 2006

Fingerprint

Leeches
Interneurons
Synapses
Serotonin
Electrical Synapses
5-Methoxytryptamine
Pimozide
Excitatory Postsynaptic Potentials
Divalent Cations
Reflex

Keywords

  • Circuits
  • Electrical coupling
  • Reflex
  • Serotonin
  • Serotonin receptor
  • Shortening

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

A 3-synapse positive feedback loop regulates the excitability of an interneuron critical for sensitization in the leech. / Crisp, Kevin M.; Muller, Kenneth J.

In: Journal of Neuroscience, Vol. 26, No. 13, 29.03.2006, p. 3524-3531.

Research output: Contribution to journalArticle

@article{b0facec267a549ce8092403a774ab30a,
title = "A 3-synapse positive feedback loop regulates the excitability of an interneuron critical for sensitization in the leech",
abstract = "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.",
keywords = "Circuits, Electrical coupling, Reflex, Serotonin, Serotonin receptor, Shortening",
author = "Crisp, {Kevin M.} and Muller, {Kenneth J}",
year = "2006",
month = "3",
day = "29",
doi = "10.1523/JNEUROSCI.3056-05.2006",
language = "English",
volume = "26",
pages = "3524--3531",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "13",

}

TY - JOUR

T1 - A 3-synapse positive feedback loop regulates the excitability of an interneuron critical for sensitization in the leech

AU - Crisp, Kevin M.

AU - Muller, Kenneth J

PY - 2006/3/29

Y1 - 2006/3/29

N2 - 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.

AB - 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.

KW - Circuits

KW - Electrical coupling

KW - Reflex

KW - Serotonin

KW - Serotonin receptor

KW - Shortening

UR - http://www.scopus.com/inward/record.url?scp=33645452198&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33645452198&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.3056-05.2006

DO - 10.1523/JNEUROSCI.3056-05.2006

M3 - Article

C2 - 16571760

AN - SCOPUS:33645452198

VL - 26

SP - 3524

EP - 3531

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 13

ER -