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The Journal of Neuroscience, August 1, 1999, 19(15):6650-6660
Coordination of Fast and Slow Rhythmic Neuronal Circuits
Marlene
Bartos1,
Yair
Manor2,
Farzan
Nadim2,
Eve
Marder2, and
Michael P.
Nusbaum1
1 Department of Neuroscience, University of
Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6074, and 2 Volen Center for Complex Systems, Brandeis
University, Waltham, Massachusetts 02454
Interactions among rhythmically active neuronal circuits that
oscillate at different frequencies are important for generating complex
behaviors, yet little is known about the underlying cellular mechanisms. We addressed this issue in the crab stomatogastric ganglion
(STG), which contains two distinct but interacting circuits. These
circuits generate the gastric mill rhythm (cycle period, ~10 sec) and
the pyloric rhythm (cycle period, ~1 sec). When the identified
modulatory projection neuron named modulatory commissural neuron 1 (MCN1) is activated, the gastric mill motor pattern is generated
by interactions among MCN1 and two STG neurons [the lateral gastric
(LG) neuron and interneuron 1]. We show that, during MCN1
stimulation, an identified synapse from the pyloric circuit onto the
gastric mill circuit is pivotal for determining the gastric mill cycle
period and the gastric-pyloric rhythm coordination. To examine the
role of this intercircuit synapse, we replaced it with a computational
equivalent via the dynamic-clamp technique. This enabled us to
manipulate better the timing and strength of this synapse. We found
this synapse to be necessary for production of the normal gastric mill
cycle period. The synapse acts, during each LG neuron interburst, to
boost rhythmically the influence of the modulatory input from MCN1 to
LG and thereby to hasten LG neuron burst onset. The two rhythms
become coordinated because LG burst onset occurs with a constant
latency after the onset of the triggering pyloric input. These results
indicate that intercircuit synapses can enable an oscillatory circuit
to control the speed of a slower oscillatory circuit, as well as
provide a mechanism for intercircuit coordination.
Key words:
stomatogastric ganglion; neuromodulation; intercircuit
coordination; disinhibition; pyloric rhythm; gastric mill rhythm; modulatory projection neuron
Copyright © 1999 Society for Neuroscience 0270-6474/99/19156650-11$05.00/0
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