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Extrinsic Modulation and Motor Pattern Generation in a Feeding network: a Cellular Study

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posted on 2023-06-08, 00:14 authored by Volko A Straub, Paul R Benjamin
Systems level studies have shown that the paired serotonergic cerebral giant cells (CGCs) of gastropod mollusks have important extrinsic modulatory actions on the central pattern generator (CPG) underlying rhythmic ingestion movements. Here we present the first study that investigates the modulatory actions of the CGCs and their released transmitter 5-HT on the CPG at the cellular level. In the snail, Lymnaea, motoneurons such as the B4, B8, and B4CL cells are part of the feeding CPG and receive serotonergic synaptic inputs from CGCs. These motoneurons were used to investigate the effect of serotonergic modulation on endogenous cellular properties of CPG neurons. Cells were isolated from the intact nervous system, and their properties were examined by pharmacological methods in cell culture. Motoneurons were also grown in coculture with CGCs to compare 5-HT effects with CGC stimulation. Three distinct modulatory effects of exogenously applied 5-HT/CGC activity were seen: all three motoneuron types were depolarized by 5-HT for prolonged periods leading to firing. Conditional bursting accompanied this depolarization in the B4/B8 cells, but not in B4CL cells. The frequency of the bursting was increased with increased CGC tonic firing. An increase in the size of postinhibitory rebound (PIR) occurred with 5-HT application in all three cell types, because of an increase in a CsCl-sensitive, hyperpolarization-activated inward current. Similar modulatory effects on membrane potential, endogenous bursting, and PIR properties could be observed in the intact nervous system and were necessary for motoneuron activation during feeding. Part of the systems gating and frequency control functions of the CGCs appear to be caused by these modulatory effects on feeding motoneurons.

History

Publication status

  • Published

File Version

  • Published version

Journal

Journal of Neuroscience

ISSN

0270-6474

Issue

5

Volume

21

Page range

1767-1778

Pages

12.0

Department affiliated with

  • Neuroscience Publications

Notes

First author was a D.Phil student when the work was done. I selected the topic, made the major intellectual contribution to the development of the ideas involved and was responsible for 70% of the writing of the paper.

Full text available

  • Yes

Peer reviewed?

  • Yes

Legacy Posted Date

2012-02-06

First Open Access (FOA) Date

2016-03-22

First Compliant Deposit (FCD) Date

2016-08-17

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