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Journal of Neuroscience, Vol 14, 3019-3035, Copyright © 1994 by Society for Neuroscience
Muscarinic modulation of a pattern-generating network: control of neuronal properties
T Bal, F Nagy and M Moulins
Universite de Bordeaux I--C.N.R.S. URA 1126, Laboratoire de Neurobiologie et Physiologie Comparees, Arcachon, France.
The aim of this article is to investigate the cellular mechanisms
underlying cholinergic modulation of the pyloric network in the
stomatogastric ganglion (STG) of the Cape lobster Jasus Ialandii. Bath
application of the muscarinic agonists muscarine, oxotremorine, and
pilocarpine on the STG activates a rhythmic pattern from a quiescent
pyloric network. The mechanisms of this modulation were investigated on
individual pyloric neurons isolated both from synaptic interactions within
the network (by photoinactivation of most of the presynaptic neurons and
pharmacological blockade of the remaining synapses) and from central inputs
(by a sucrose block of the input nerve). All three muscarinic agonists
activated bursting and plateau properties of all the neurons comprising the
pyloric network. The activation was dose dependent, and was blocked by the
muscarinic antagonists atropine, pirenzepine, and scopolamine. The
oscillatory behavior triggered by the muscarinic stimulation was specific
to each type of pyloric neuron. The isolated neuron AB had the shortest
oscillation period and depolarizing phase. The constrictor neurons (LP, PY,
IC) were the slowest oscillators, and only oscillated upon hyperpolarizing
current injection. Under muscarinic modulation, the individual bursting
activities of the isolated pyloric neurons were of the same type as their
activities when isolated from the network but modulated by central inputs
(Bal et al., 1988). The VD neuron is an exception since it was a rapid
oscillator in the latter situation and became a slow oscillator when
modulated by a single muscarinic agonist. To determine the relative
importance of the muscarinic-dependent bursting properties of the
individual pyloric neurons in the operation of the intact network, a
progressive reconstruction of the synaptic circuitry was attempted. We
found that under certain conditions of muscarinic modulation a new
composite pacemaker could be created, composed of the electrically coupled
VD, AB, and PD neurons. This can result in the generation of new pyloric
patterns that were very sensitive to the membrane potential of individual
network neurons. The data also confirmed that, in a rhythmic
"pattern-generating network," the pacemaker role may not be definitely
attributed to a given neuron but instead could be assigned to other neurons
by modulation of their respective oscillatory capabilities.
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