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The Journal of Neuroscience, March 1, 2001, 21(5):1767-1778
Extrinsic Modulation and Motor Pattern Generation in a Feeding
Network: a Cellular Study
Volko A.
Straub and
Paul R.
Benjamin
Sussex Centre for Neuroscience, University of Sussex, Falmer,
Brighton, BN1 9QG, United Kingdom
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.
Key words:
Lymnaea; central pattern generator; neuromodulation; serotonin; conditional bursting; PIR; hyperpolarization-activated inward current; cell culture
Copyright © 2001 Society for Neuroscience 0270-6474/01/2151767-12$05.00/0
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