Serotonin modulates axo-axonal coupling between neurons critical for learning in the leech

Brenda L. Moss, Abby D. Fuller, Christie L. Sahley, Brian D Burrell

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

S cells form a chain of electrically coupled neurons that extends the length of the leech CNS and plays a critical role in sensitization during whole-body shortening. This process requires serotonin, which acts in part by altering the pattern of activity in the S-cell network. Serotonin-containing axons and varicosities were observed in Faivre's nerve where the S-to-S-cell electrical synapses are located. To determine whether serotonin modulates these synapses, S-cell action-potential (AP) propagation was studied in a two-ganglion chain containing one electrical synapse. Suction electrodes were placed on the cut ends of the connectives to stimulate one S cell while recording the other, coupled S cell's APs. A third electrode, placed en passant, recorded the APs near the electrical synapse before they propagated through it. Low concentrations of the gap junction inhibitor octanol increased AP latency across the two-ganglion chain, and this effect was localized to the region of axon containing the electrical synapse. At higher concentrations, APs failed to propagate across the synapse. Serotonin also increased AP latency across the electrical synapse, suggesting that serotonin reduced coupling between S cells. This effect was independent of the direction of propagation and increased with the number of electrical synapses in progressively longer chains. Furthermore, serotonin modulated instantaneous AP frequency when APs were initiated in separate S cells and in a computational model of S-cell activity after mechanosensory input. Thus serotonergic modulation of S-cell electrical synapses may contribute to changes in the pattern of activity in the S-cell network.

Original languageEnglish (US)
Pages (from-to)2575-2589
Number of pages15
JournalJournal of Neurophysiology
Volume94
Issue number4
DOIs
StatePublished - Oct 1 2005

Fingerprint

Leeches
Electrical Synapses
Serotonin
Learning
Neurons
Action Potentials
Ganglia
Synapses
Axons
Electrodes
Octanols
Gap Junctions
Suction

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

Cite this

Serotonin modulates axo-axonal coupling between neurons critical for learning in the leech. / Moss, Brenda L.; Fuller, Abby D.; Sahley, Christie L.; Burrell, Brian D.

In: Journal of Neurophysiology, Vol. 94, No. 4, 01.10.2005, p. 2575-2589.

Research output: Contribution to journalArticle

Moss, Brenda L. ; Fuller, Abby D. ; Sahley, Christie L. ; Burrell, Brian D. / Serotonin modulates axo-axonal coupling between neurons critical for learning in the leech. In: Journal of Neurophysiology. 2005 ; Vol. 94, No. 4. pp. 2575-2589.
@article{c45355589c044c68806699d8a0241f9b,
title = "Serotonin modulates axo-axonal coupling between neurons critical for learning in the leech",
abstract = "S cells form a chain of electrically coupled neurons that extends the length of the leech CNS and plays a critical role in sensitization during whole-body shortening. This process requires serotonin, which acts in part by altering the pattern of activity in the S-cell network. Serotonin-containing axons and varicosities were observed in Faivre's nerve where the S-to-S-cell electrical synapses are located. To determine whether serotonin modulates these synapses, S-cell action-potential (AP) propagation was studied in a two-ganglion chain containing one electrical synapse. Suction electrodes were placed on the cut ends of the connectives to stimulate one S cell while recording the other, coupled S cell's APs. A third electrode, placed en passant, recorded the APs near the electrical synapse before they propagated through it. Low concentrations of the gap junction inhibitor octanol increased AP latency across the two-ganglion chain, and this effect was localized to the region of axon containing the electrical synapse. At higher concentrations, APs failed to propagate across the synapse. Serotonin also increased AP latency across the electrical synapse, suggesting that serotonin reduced coupling between S cells. This effect was independent of the direction of propagation and increased with the number of electrical synapses in progressively longer chains. Furthermore, serotonin modulated instantaneous AP frequency when APs were initiated in separate S cells and in a computational model of S-cell activity after mechanosensory input. Thus serotonergic modulation of S-cell electrical synapses may contribute to changes in the pattern of activity in the S-cell network.",
author = "Moss, {Brenda L.} and Fuller, {Abby D.} and Sahley, {Christie L.} and Burrell, {Brian D}",
year = "2005",
month = "10",
day = "1",
doi = "10.1152/jn.00322.2005",
language = "English (US)",
volume = "94",
pages = "2575--2589",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "4",

}

TY - JOUR

T1 - Serotonin modulates axo-axonal coupling between neurons critical for learning in the leech

AU - Moss, Brenda L.

AU - Fuller, Abby D.

AU - Sahley, Christie L.

AU - Burrell, Brian D

PY - 2005/10/1

Y1 - 2005/10/1

N2 - S cells form a chain of electrically coupled neurons that extends the length of the leech CNS and plays a critical role in sensitization during whole-body shortening. This process requires serotonin, which acts in part by altering the pattern of activity in the S-cell network. Serotonin-containing axons and varicosities were observed in Faivre's nerve where the S-to-S-cell electrical synapses are located. To determine whether serotonin modulates these synapses, S-cell action-potential (AP) propagation was studied in a two-ganglion chain containing one electrical synapse. Suction electrodes were placed on the cut ends of the connectives to stimulate one S cell while recording the other, coupled S cell's APs. A third electrode, placed en passant, recorded the APs near the electrical synapse before they propagated through it. Low concentrations of the gap junction inhibitor octanol increased AP latency across the two-ganglion chain, and this effect was localized to the region of axon containing the electrical synapse. At higher concentrations, APs failed to propagate across the synapse. Serotonin also increased AP latency across the electrical synapse, suggesting that serotonin reduced coupling between S cells. This effect was independent of the direction of propagation and increased with the number of electrical synapses in progressively longer chains. Furthermore, serotonin modulated instantaneous AP frequency when APs were initiated in separate S cells and in a computational model of S-cell activity after mechanosensory input. Thus serotonergic modulation of S-cell electrical synapses may contribute to changes in the pattern of activity in the S-cell network.

AB - S cells form a chain of electrically coupled neurons that extends the length of the leech CNS and plays a critical role in sensitization during whole-body shortening. This process requires serotonin, which acts in part by altering the pattern of activity in the S-cell network. Serotonin-containing axons and varicosities were observed in Faivre's nerve where the S-to-S-cell electrical synapses are located. To determine whether serotonin modulates these synapses, S-cell action-potential (AP) propagation was studied in a two-ganglion chain containing one electrical synapse. Suction electrodes were placed on the cut ends of the connectives to stimulate one S cell while recording the other, coupled S cell's APs. A third electrode, placed en passant, recorded the APs near the electrical synapse before they propagated through it. Low concentrations of the gap junction inhibitor octanol increased AP latency across the two-ganglion chain, and this effect was localized to the region of axon containing the electrical synapse. At higher concentrations, APs failed to propagate across the synapse. Serotonin also increased AP latency across the electrical synapse, suggesting that serotonin reduced coupling between S cells. This effect was independent of the direction of propagation and increased with the number of electrical synapses in progressively longer chains. Furthermore, serotonin modulated instantaneous AP frequency when APs were initiated in separate S cells and in a computational model of S-cell activity after mechanosensory input. Thus serotonergic modulation of S-cell electrical synapses may contribute to changes in the pattern of activity in the S-cell network.

UR - http://www.scopus.com/inward/record.url?scp=24944572172&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=24944572172&partnerID=8YFLogxK

U2 - 10.1152/jn.00322.2005

DO - 10.1152/jn.00322.2005

M3 - Article

C2 - 15987763

AN - SCOPUS:24944572172

VL - 94

SP - 2575

EP - 2589

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 4

ER -